Science 6.11.2020

CONTENTS INSIGHTS

6 NOVEMBER 2020 • VOLUME 370 • ISSUE 6517 PERSPECTIVES

ILLUSTRATIONS (TOP TO BOTTOM): STEPHANIE ABRAMOWICZ; A. KITTERMAN AND V. ALTOUNIAN/SCIENCE NEWS 654 654 A surprising fossil vertebrate
An ancient amphibian converged
IN BRIEF 647 New chip-based lasers promise on a chameleon-like way of feeding
practical terahertz imaging
640 News at a glance Semiconductor lasers work with small coolers, By D. B. Wake
enabling medical imaging and contraband
IN DEPTH detection By R. F. Service RESEARCH ARTICLE p. 687
648 Black holes by the dozens
642 ‘A very, very bad look’ for challenge theorists 655 The genetic law of the minimum
remdesivir Trove of gravitational wave detections allows The genetic code evolved to
FDA and Europe anointed it as black holes to be studied en masse By A. Cho reduce the impact of nutrient limitations
a key therapy just after a major study
found it has little value PODCAST By M. F. Polz and O. X. Cordero

By J. Cohen and K. Kupferschmidt F E AT U R E S RESEARCH ARTICLE p. 683

644 Europe is locking down 649 The long shot 657 Regulation in common:
again—but its strategy is unclear A little company chases its bigger Sponge to zebrafish
Without a plan to eliminate the virus, competitors in the race for a coronavirus Developmental enhancers from a sponge
countries may face shutdowns over and vaccine By M. Wadman regulate gene expression in
over, scientists warn By K. Kupferschmidt zebrafish neurons By N. Harmston
652 ‘Nothing is impossible,’
645 Growth spurt for height genetics says lab ace Nita Patel RESEARCH ARTICLE p. 681
By tallying thousands of genetic variants, By M. Wadman
researchers account for height’s 658 Nudging people to court
remaining “missing heritability” VIDEO Behavioral interventions may improve
court attendance, but how
By J. Kaiser Published by AAAS to reform the system remains unclear

646 How the horse powered human By I. Kohler-Hausmann
prehistory
Wide-ranging warriors made Mongolian RESEARCH ARTICLE p. 682
empire a melting pot, sweeping gene study
shows By A. Curry 660 Food for thought
The nuclear metabolic-epigenetic axis
SCIENCE sciencemag.org bridges the environment and genes
to modulate behavior By G. Egervari et al.

662 Steering iceberg armadas
The Asian-Pacific tropics likely instigated
millennial-scale climate changes

By J. M. Jaeger and A. E. Shevenell

REPORT p. 716

663 Public health during the
pandemic in India
Data from two Indian states give detail
about variation in transmission and
disease outcomes By J. John and G. Kang

RESEARCH ARTICLE p. 691

POLICY FORUM

665 Species protection will take more
than rule reversal
Key improvements are needed for
implementation of the Endangered Species
Act By Y.-W. Li et al.

BOOKS ET AL.

667 The ascent of Wikipedia
Scholars reflect on 20 years of
crowdsourced knowledge By A. Robinson

668 Recognizing the work of women
Despite several stumbles, a new volume
about women in paleontology will likely prove
valuable to future scholars By J. Miller-Camp

6 NOVEMBER 2020 • VOL 370 ISSUE 6517 633

CONTENTS

LETTERS RESEARCH ARTICLES 691 Coronavirus
Epidemiology and transmission dynamics
669 Aquaculture jeopardizes migrating 681 Enhancer genomics of COVID-19 in two Indian states
Oriental storks Deep conservation of the enhancer R. Laxminarayan et al.
regulatory code in animals
By Y. Sun et al. E. S. Wong et al. PERSPECTIVE p. 663

669 Indigenous rights to Patagonia RESEARCH ARTICLE SUMMARY; FOR FULL TEXT: REPORTS
DX.DOI.ORG/10.1126/SCIENCE.AAX8137
By P. A. Marquet et al. PERSPECTIVE p. 657 698 Organic devices
Large-area low-noise flexible organic
670 Fisheries rely on threatened 682 Criminal justice photodiodes for detecting faint visible light
salt marshes Behavioral nudges reduce failure to appear C. Fuentes-Hernandez et al.
for court A. Fishbane et al.
By R. Baker et al. 701 Topological optics
RESEARCH ARTICLE SUMMARY; FOR FULL TEXT: Nonlinearity-induced photonic topological
RESEARCH DX.DOI.ORG/10.1126/SCIENCE.ABB6591 insulator L. J. Maczewsky et al.
PERSPECTIVE p. 658
IN BRIEF 705 Climate change
683 Metabolic genomics Global food system emissions could preclude
677 From Science and other journals Resource conservation manifests in the achieving the 1.5° and 2°C climate change
genetic code L. Shenhav and D. Zeevi targets M. A. Clark et al.
REVIEW
PERSPECTIVE p. 655 708 Batteries
680 Climate change Rational design of layered oxide materials
Past climates inform our future J. E.Tierney et al. 687 Paleontology for sodium-ion batteries C. Zhao et al.
Enigmatic amphibians in mid-Cretaceous
REVIEW SUMMARY; FOR FULL TEXT: amber were chameleon-like 712 Ecological monitoring
DX.DOI.ORG/10.1126/SCIENCE.AAY3701 ballistic feeders J. D. Daza et al. Ecological insights from three decades of
animal movement tracking across a changing
PERSPECTIVE p. 654 Arctic S. C. Davidson et al.

SPECIAL SECTION PODCAST

OSIRIS-REx at Bennu 716 Paleoclimate
Phasing of millennial-scale climate
INTRODUCTION ON THE COVER variability in the Pacific and Atlantic Oceans
M. H. Walczak et al.
672 Sampling the early solar system The near-Earth carbonaceous asteroid
(101955) Bennu, as observed by the PERSPECTIVE p. 662
RESEARCH OSIRIS-REx spacecraft. A lidar-derived
shape model is overlain in grayscale with 721 Ecological genomics
674 Variations in color and reflectance the albedo, and in color with a map of the Genomic architecture of a genetically
on the surface of asteroid (101955) abundance of carbon-bearing material assimilated seasonal color pattern
Bennu D. N. DellaGiustina et al. (center, see page 675) and a false-color K. R. L. van der Burg et al.
image indicating the near-ultraviolet and
RESEARCH ARTICLE SUMMARY; 725 Coronavirus
FOR FULL TEXT: DX.DOI.ORG/10.1126/ near-infrared spectral Free fatty acid binding pocket in the locked
SCIENCE.ABC3660 slopes (right, see page structure of SARS-CoV-2 spike protein
674). Graphic: NASA’s C. Toelzer et al.
675 Widespread carbon-bearing materials Scientific Visualization
on near-Earth asteroid (101955) Bennu Studio; Data: Daly et al. D E PA R T M E N T S
A. A. Simon et al. Sci. Adv. 6, eabd3649/
DellaGiustina et al./ 639 Editorial
RESEARCH ARTICLE SUMMARY; Simon et al./OSIRIS- Gradually, then suddenly
FOR FULL TEXT: DX.DOI.ORG/10.1126/ REx Team
SCIENCE.ABC3522 By H. Holden Thorp
SEE ALSO SCIENCE ADVANCES RESEARCH
676 Bright carbonate veins on asteroid ARTICLES BY D. J. SCHEERES ET AL. 10.1126/ 738 Working Life
(101955) Bennu: Implications for aqueous SCIADV.ABC3350, M. G. DALY ET AL. 10.1126/ A sabbatical reboot
alteration history H. H. Kaplan et al. SCIADV.ABD3649, AND B. ROZITIS ET AL.
10.1126/SCIADV.ABC3699 By Thomas Gernon
RESEARCH ARTICLE SUMMARY;
FOR FULL TEXT: DX.DOI.ORG/10.1126/ Science Staff ............................................. 636
SCIENCE.ABC3557 Science Careers .........................................734

SCIENCE (ISSN 0036-8075) is published weekly on Friday, except last week in December, by the American Association for the Advancement of Science, 1200 New York Avenue, NW, Washington, DC 20005. Periodicals mail
postage (publication No. 484460) paid at Washington, DC, and additional mailing offices. Copyright © 2020 by the American Association for the Advancement of Science. The title SCIENCE is a registered trademark of the AAAS. Domestic
individual membership, including subscription (12 months): $165 ($74 allocated to subscription). Domestic institutional subscription (51 issues): $2148; Foreign postage extra: Air assist delivery: $98. First class, airmail, student, and
emeritus rates on request. Canadian rates with GST available upon request, GST #125488122. Publications Mail Agreement Number 1069624. Printed in the U.S.A.
Change of address: Allow 4 weeks, giving old and new addresses and 8-digit account number. Postmaster: Send change of address to AAAS, P.O. Box 96178, Washington, DC 20090–6178. Single-copy sales: $15 each plus shipping and
handling available from backissues.sciencemag.org; bulk rate on request. Authorization to reproduce material for internal or personal use under circumstances not falling within the fair use provisions of the Copyright Act can be obtained
through the Copyright Clearance Center (CCC), www.copyright.com. The identification code for Science is 0036-8075. Science is indexed in the Reader’s Guide to Periodical Literature and in several specialized indexes.

SCIENCE sciencemag.org 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 635

Published by AAAS

Editor-in-Chief Holden Thorp, [email protected] BOARD OF REVIEWING EDITORS (Statistics board members indicated with S)

Executive Editor Monica M. Bradford Adriano Aguzzi, U. Hospital Zürich Ramon Gonzalez, Margaret Palmer, U. of Maryland
Editors, Research Valda Vinson, Jake S. Yeston Editor, Insights Lisa D. Chong Takuzo Aida, U. of Tokyo U. of South Florida Elizabeth Levy Paluck,
Leslie Aiello, Sandra González-Bailón, Princeton U.
DEPUTY EDITORS Julia Fahrenkamp-Uppenbrink (UK), Stella M. Hurtley (UK), Phillip D. Szuromi, Sacha Vignieri SR. EDITORIAL FELLOW Wenner-Gren Foundation UPenn. Jane Parker,
Andrew M. Sugden (UK) SR. EDITORS Gemma Alderton (UK), Caroline Ash (UK), Brent Grocholski, Pamela J. Hines, Di Jiang, Marc Deji Akinwande, UT Austin Elizabeth Grove, U. of Chicago Max Planck Inst. Cologne
S. Lavine (Canada), Yevgeniya Nusinovich, Ian S. Osborne (UK), Beverly A. Purnell, L. Bryan Ray, H. Jesse Smith, Keith T. Smith Judith Allen, U. of Manchester Nicolas Gruber, ETH ZÜrich Giovanni Parmigiani,
(UK), Jelena Stajic, Peter Stern (UK), Valerie B. Thompson, Brad Wible, Laura M. Zahn ASSOCIATE EDITORS Michael A. Funk, Priscilla Marcella Alsan, Harvard U. Hua Guo, U. of New Mexico Dana-Farber Cancer Inst. (S)
N. Kelly, Tage S. Rai, Seth Thomas Scanlon (UK), Yury V. Suleymanov LETTERS EDITOR Jennifer Sills LEAD CONTENT PRODUCTION EDITORS Sebastian Amigorena, Kip Guy, Daniel Pauly, U. of British Columbia
Harry Jach, Lauren Kmec CONTENT PRODUCTION EDITORS Amelia Beyna, Jeffrey E. Cook, Chris Filiatreau, Julia Katris, Nida Masiulis, Institut Curie UK Coll. of Pharm. Samuel Pfaff,
Suzanne M. White SR. EDITORIAL COORDINATORS Carolyn Kyle, Beverly Shields EDITORIAL COORDINATORS Aneera Dobbins, Joi S. Granger, James Analytis, UC Berkeley Taekjip Ha, Johns Hopkins U. Salk Inst.
Jeffrey Hearn, Lisa Johnson, Maryrose Madrid, Ope Martins, Shannon McMahon, Jerry Richardson, Hilary Stewart (UK), Alana Trevor Archer, NIEHS, NIH Christian Haass, Julie Pfeiffer,
Warnke, Alice Whaley (UK), Anita Wynn PUBLICATIONS ASSISTANTS Jeremy Dow, Alexander Kief, Ronmel Navas, Brian White EXECUTIVE Paola Arlotta, Harvard U. Ludwig Maximilians U. UT Southwestern Med. Ctr.
ASSISTANT Jessica Slater ASI DIRECTOR, OPERATIONS Janet Clements (UK) ASI SR. OFFICE ADMINISTRATOR Jessica Waldock (UK) Johan Auwerx, EPFL Sharon Hammes-Schiffer, Philip Phillips, UIUC
David Awschalom, U. of Chicago Yale U. Matthieu Piel, Institut Curie
News Editor Tim Appenzeller Clare Baker, U. of Cambridge Wolf-Dietrich Hardt, ETH ZÜrich Kathrin Plath, UCLA
Nenad Ban, ETH ZÜrich Louise Harra, U. Coll. London Martin Plenio, Ulm U.
NEWS MANAGING EDITOR John Travis INTERNATIONAL EDITOR Martin Enserink DEPUTY NEWS EDITORS Elizabeth Culotta, Lila Guterman, Franz Bauer, Jian He, Clemson U. Katherine Pollard,
David Grimm, Eric Hand (Europe), David Malakoff SR. CORRESPONDENTS Daniel Clery (UK), Jon Cohen, Jeffrey Mervis, Elizabeth Pontificia U. Católica de Chile Carl-Philipp Heisenberg, UCSF
Pennisi ASSOCIATE EDITORS Jeffrey Brainard, Catherine Matacic NEWS REPORTERS Adrian Cho, Jennifer Couzin-Frankel, Jocelyn Ray H. Baughman, IST Austria Elvira Poloczanska,
Kaiser, Kelly Servick, Robert F. Service, Erik Stokstad, Paul Voosen, Meredith Wadman INTERNS Lucy Hicks, Cathleen O'Grady UT Dallas Ykä Helariutta, U. of Cambridge Alfred-Wegener-Inst.
CONTRIBUTING CORRESPONDENTS Warren Cornwall, Ann Gibbons, Mara Hvistendahl, Sam Kean, Eli Kintisch, Kai Kupferschmidt Carlo Beenakker, Leiden U. Janet G. Hering, Eawag Julia Pongratz,
(Berlin), Andrew Lawler, Mitch Leslie, Eliot Marshall, Virginia Morell, Dennis Normile (Shanghai), Elisabeth Pain (Careers), Yasmine Belkaid, NIAID, NIH Hans Hilgenkamp, U. of Twente Ludwig Maximilians U.
Charles Piller, Michael Price, Tania Rabesandratana (Barcelona), Joshua Sokol, Emily Underwood, Gretchen Vogel (Berlin), Philip Benfey, Duke U. Kai-Uwe Hinrichs, U. of Bremen Philippe Poulin, CNRS
Lizzie Wade (Mexico City) CAREERS Donisha Adams, Rachel Bernstein (Editor), Katie Langin (Associate Editor) COPY EDITORS Julia Gabriele Bergers, VIB Deirdre Hollingsworth, Jonathan Pritchard, Stanford U.
Cole (Senior Copy Editor), Cyra Master (Copy Chief) ADMINISTRATIVE SUPPORT Meagan Weiland Kiros T. Berhane, Columbia U. U. of Oxford Lei Stanley Qi, Stanford U.
Bradley Bernstein, Lora Hooper, Félix A. Rey, Institut Pasteur
Creative Director Beth Rakouskas Mass. General Hospital UT Southwestern Med. Ctr. Trevor Robbins, U. of Cambridge
Joseph J. Berry, NREL Fred Hughson, Princeton U. Joeri Rogelj,
DESIGN MANAGING EDITOR Marcy Atarod GRAPHICS MANAGING EDITOR Alberto Cuadra PHOTOGRAPHY MANAGING EDITOR William Douthitt Alessandra Biffi, Randall Hulet, Rice U. Imperial Coll. London
WEB CONTENT STRATEGY MANAGER Kara Estelle-Powers DESIGN EDITOR Chrystal Smith DESIGNER Christina Aycock GRAPHICS Harvard Med. Auke Ijspeert, EPFL Amy Rosenzweig,
EDITOR Nirja Desai INTERACTIVE GRAPHICS EDITOR Xing Liu SENIOR SCIENTIFIC ILLUSTRATORS Valerie Altounian, Chris Bickel Peer Bork, EMBL Akiko Iwasaki, Yale U. Northwestern U.
SCIENTIFIC ILLUSTRATOR Alice Kitterman SENIOR GRAPHICS SPECIALISTS Holly Bishop, Nathalie Cary SENIOR PHOTO EDITOR Emily Petersen Chris Bowler, Stephen Jackson, Mike Ryan, UT Austin
PHOTO EDITOR Kaitlyn Dolan WEB DESIGNER Jennie Pajerowski École Normale Supérieure USGS & U. of Arizona Shimon Sakaguchi, Osaka U.
Ian Boyd, U. of St.Andrews Erich Jarvis, Rockefeller U. Miquel Salmeron,
Chief Executive Officer and Executive Publisher Sudip Parikh Emily Brodsky, UC Santa Cruz Kai Johnsson, EPFL Lawrence Berkeley Nat. Lab
Ron Brookmeyer, UCLA (S) Peter Jonas, ISTAustria Nitin Samarth, Penn State U.
Publisher, Science Family of Journals Bill Moran Christian Büchel, UKE Hamburg Matt Kaeberlein, Jürgen Sandkühler,
Dennis Burton, Scripps Res. U. of Wash. Med. U. of Vienna
DIRECTOR, BUSINESS SYSTEMS AND FINANCIAL ANALYSIS Randy Yi DIRECTOR, BUSINESS OPERATIONS & ANALYSIS Eric Knott DIRECTOR OF ANALYTICS Carter Tribley Butts, UC Irvine William Kaelin Jr., Erica Ollmann Saphire,
Enrique Gonzales MANAGER, BUSINESS OPERATIONS Jessica Tierney SENIOR BUSINESS ANALYST Cory Lipman, Meron Kebede FINANCIAL György Buzsáki, Dana-Farber Cancer Inst. La Jolla Inst.
ANALYST Alexander Lee ADVERTISING SYSTEM ADMINISTRATOR Tina Burks SENIOR SALES COORDINATOR Shirley Young DIGITAL/PRINT STRATEGY NYU School of Med. Daniel Kammen, UC Berkeley Alexander Schier, Harvard U.
MANAGER Jason Hillman QUALITY TECHNICAL MANAGER Marcus Spiegler ASSISTANT MANAGER DIGITAL/PRINT Rebecca Doshi SENIOR CONTENT Blanche Capel, Duke U. V. Narry Kim, Seoul Nat. U. Wolfram Schlenker, Columbia U.
SPECIALISTS Steve Forrester, Jacob Hedrick, Antoinette Hodal, Lori Murphy PRODUCTION SPECIALIST Kristin Wowk DIGITAL PRODUCTION Annmarie Carlton, UC Irvine Robert Kingston, Susannah Scott,
MANAGER Lisa Stanford CONTENT SPECIALIST Kimberley Oster ADVERTISING PRODUCTION OPERATIONS MANAGER Deborah Tompkins Nick Chater, U. of Warwick Harvard Med. UC Santa Barbara
DESIGNER, CUSTOM PUBLISHING Jeremy Huntsinger SR. TRAFFIC ASSOCIATE Christine Hall SPECIAL PROJECTS ASSOCIATE Sarah Dhere M. Keith Chen, UCLA Nancy Knowlton, Rebecca Sear, LSHTM
Zhijian Chen, Smithsonian Institution Anuj Shah, U. of Chicago
ASSOCIATE DIRECTOR, BUSINESS DEVELOPMENT Justin Sawyers GLOBAL MARKETING MANAGER Allison Pritchard DIGITAL MARKETING MANAGER UT Southwestern Med. Ctr. Etienne Koechlin, Vladimir Shalaev, Purdue U.
Aimee Aponte JOURNALS MARKETING MANAGER Shawana Arnold MARKETING ASSOCIATES Tori Velasquez, Mike Romano, Ashley Ib Chorkendorff, Denmark TU École Normale Supérieure Jie Shan, Cornell U.
Hylton DIGITAL MARKETING SPECIALIST Asleigh Rojanavongse SENIOR DESIGNER Kim Huynh James J. Collins, MIT Alex L. Kolodkin, Beth Shapiro, UC Santa Cruz
Robert Cook-Deegan, Johns Hopkins U. Jay Shendure, U. of Wash.
DIRECTOR AND SENIOR EDITOR, CUSTOM PUBLISHING Sean Sanders ASSISTANT EDITOR, CUSTOM PUBLISHING Jackie Oberst Arizona State U. Julija Krupic, U. of Cambridge Steve Sherwood,
Alan Cowman, Thomas Langer, U. of New South Wales
DIRECTOR, PRODUCT & PUBLISHING DEVELOPMENT Chris Reid DIRECTOR, BUSINESS STRATEGY AND PORTFOLIO MANAGEMENT Sarah Whalen Walter & Eliza Hall Inst. Max Planck Inst. Cologne Brian Shoichet, UCSF
ASSOCIATE DIRECTOR, PRODUCT MANAGMENT Kris Bishop PRODUCT DEVELOPMENT MANAGER Scott Chernoff PUBLISHING TECHNOLOGY Carolyn Coyne, U. of Pitt. Mitchell A. Lazar, UPenn. Robert Siliciano,
MANAGER Michael Di Natale SR. PRODUCT ASSOCIATE Robert Koepke SPJ ASSOCIATE Samantha Bruno Fuller Roberta Croce, VU Amsterdam Wendell Lim, UCSF JHU School of Med.
Ismaila Dabo, Penn State U. Jianguo Liu, Michigan State U. Lucia Sivilotti, U. Coll. London
DIRECTOR, INSTITUTIONAL LICENSING Iquo Edim ASSOCIATE DIRECTOR, RESEARCH & DEVELOPMENT Elisabeth Leonard MARKETING MANAGER Jeff L. Dangl, UNC Luis Liz-Marzán, CIC biomaGUNE Alison Smith, John Innes Centre
Kess Knight SENIOR INSTITUTIONAL LICENSING MANAGER Ryan Rexroth INSTITUTIONAL LICENSING MANAGER Marco Castellan MANAGER, Chiara Daraio, Caltech Omar Lizardo, UCLA Richard Smith,
AGENT RELATIONS & CUSTOMER SUCCESS Judy Lillibridge SENIOR OPERATIONS ANALYST Lana Guz FULFILLMENT COORDINATOR Melody Nicolas Dauphas, Jonathan Losos, UNC (S)
Stringer SALES COORDINATOR Josh Haverlock U. of Chicago Wash. U. in St. Louis Mark Smyth, QIMR Berghofer
Christian Davenport, Ke Lu, Inst. of Metal Res., CAS Pam Soltis, U. of Florida
DIRECTOR, GLOBAL SALES Tracy Holmes US EAST COAST AND MID WEST SALES Stephanie O'Connor US WEST COAST SALES Lynne Stickrod U. of Michigan Christian Lüscher, U. of Geneva John Speakman, U. of Aberdeen
US SALES MANAGER, SCIENCE CAREERS Claudia Paulsen-Young US SALES REP, SCIENCE CAREERS Tracy Anderson ASSOCIATE DIRECTOR, Frans de Waal, Emory U. Jean Lynch-Stieglitz, Tara Spires-Jones,
ROW Roger Goncalves SALES REP, ROW Sarah Lelarge SALES ADMIN ASSISTANT, ROW Bryony Cousins DIRECTOR OF GLOBAL Claude Desplan, NYU Georgia Inst. of Tech. U. of Edinburgh
COLLABORATION AND ACADEMIC PUBLISHING RELATIONS, ASIA Xiaoying Chu ASSOCIATE DIRECTOR, INTERNATIONAL COLLABORATION Grace Sandra DÍaz, Fabienne Mackay, Allan C. Spradling,
Yao SALES MANAGER Danny Zhao MARKETING MANAGER Kilo Lan ASCA CORPORATION, JAPAN Kaoru Sasaki (Tokyo), Miyuki Tani U. Nacional de CÓrdoba QIMR Berghofer Carnegie Institution for Sci.
(Osaka) COLLABORATION/CUSTOM PUBLICATIONS/JAPAN Adarsh Sandhu Ulrike Diebold,TU Wien Anne Magurran, U. of St.Andrews V. S. Subrahmanian,
Hong Ding, Inst. of Physics, CAS Asifa Majid, U. of York Dartmouth
DIRECTOR, COPYRIGHT, LICENSING AND SPECIAL PROJECTS Emilie David RIGHTS AND LICENSING COORDINATOR Jessica Adams RIGHTS AND Dennis Discher, UPenn. Oscar Marín, King’s Coll. London Ira Tabas, Columbia U.
PERMISSIONS ASSOCIATE Elizabeth Sandler CONTRACTS AND LICENSING ASSOCIATE Lili Catlett Jennifer A. Doudna, UC Berkeley Charles Marshall, UC Berkeley Sarah Teichmann,
Raissa M. D'Souza, UC Davis Christopher Marx, U. of Idaho Wellcome Sanger Inst.
MAIN HEADQUARTERS EDITORIAL PRODUCT ADVERTISING AAAS BOARD OF DIRECTORS Bruce Dunn, UCLA David Masopust, U. of Minnesota Rocio Titiunik, Princeton U.
& CUSTOM PUBLISHING William Dunphy, Caltech Geraldine Masson, CNRS Shubha Tole,
Science/AAAS [email protected] CHAIR Steven Chu Christopher Dye, U. of Oxford Jason Matheny, Georgetown U. Tata Inst. of Fundamental Res.
1200 New York Ave. NW advertising.sciencemag.org/ PRESIDENT Claire M. Fraser Scott Edwards, Harvard U. C. Robertson McClung, Kimani Toussaint, Brown U.
Washington, DC 20005 NEWS products-services PRESIDENT-ELECT Susan G.Amara Todd Ehlers, U. of TÜbingen Dartmouth Wim van der Putten,
TREASURER Carolyn N. Ainslie Jennifer Elisseeff, Rodrigo Medellín, Netherlands Inst. of Ecology
SCIENCE INTERNATIONAL [email protected] [email protected] Johns Hopkins U. U. Nacional Autónoma de México Reinhilde Veugelers, KU Leuven
CHIEF EXECUTIVE OFFICER Tim Elston, U. of North Carolina Graham Medley, LSHTM Bert Vogelstein, Johns Hopkins U.
Clarendon House INFORMATION FOR AUTHORS CLASSIFIED ADVERTISING Andrea Encalada, Jane Memmott, U. of Bristol Kathleen Vohs, U. of Minnesota
Clarendon Road Sudip Parikh U. San Francisco de Quito C. Jessica Metcalf, Princeton U. David Wallach,
Cambridge, CB2 8FH, UK sciencemag.org/authors/ advertising.sciencemag.org/ BOARD Cynthia M. Beall Nader Engheta, U. of Penn. Baoxia Mi, UC Berkeley Weizmann Inst.
science-information-authors science-careers Rosina M. Bierbaum Karen Ersche, U. of Cambridge Edward Miguel, UC Berkeley Jane-Ling Wang, UC Davis (S)
SCIENCE CHINA Ann Bostrom Beate Escher, Tom Misteli, NCI, NIH Jessica Ware,
REPRINTS AND PERMISSIONS [email protected] Stephen P.A. Fodor UFZ & U. of Tübingen Yasushi Miyashita, U. of Tokyo Amer. Mus. of Natural Hist.
Room 1004, Culture Square S. James Gates, Jr. Barry Everitt, U. of Cambridge Alison Motsinger-Reif, David Waxman, Fudan U.
No. 59 Zhongguancun St. sciencemag.org/help/ JOB POSTING CUSTOMER SERVICE Laura H. Greene Vanessa Ezenwa, U. of Georgia NIEHS, NIH (S) Jonathan Weissman,
Haidian District, Beijing, 100872 reprints-and-permissions Kaye Husbands Fealing Michael Feuer, Danielle Navarro, UCSF
employers.sciencecareers.org Maria M. Klawe GWU U. of New South Wales Chris Wikle, U. of Missouri (S)
SCIENCE JAPAN MEDIA CONTACTS Robert B. Millard Toren Finkel, Daniel Nettle, Newcastle U. Terrie Williams, UC Santa Cruz
[email protected] Alondra Nelson U. of Pitt. Med. Ctr. Daniel Neumark, UC Berkeley Ian A. Wilson, Scripps Res. (S)
ASCA Corporation [email protected] William D. Provine Gwenn Flowers, Simon Fraser U. Beatriz Noheda, U. of Groningen Yu Xie, Princeton U.
Sibaura TY Bldg. 4F, 1-14-5 MEMBERSHIP AND INDIVIDUAL Peter Fratzl, Helga Nowotny, Jan Zaanen, Leiden U.
Shibaura Minato-ku MULTIMEDIA CONTACTS SUBSCRIPTIONS Max Planck Inst. Potsdam Vienna Sci., Res. & Tech. Fund Kenneth Zaret,
Tokyo, 108-0073 Japan Elaine Fuchs, Rockefeller U. Rachel O’Reilly, U. of Birmingham UPenn. School of Med.
[email protected] sciencemag.org/subscriptions Eileen Furlong, EMBL Harry Orr, U. of Minnesota Jonathan Zehr, UC Santa Cruz
[email protected] Jay Gallagher, U. of Wisconsin Pilar Ossorio, U. of Wisconsin Bing Zhu, Inst. of Biophysics, CAS
MEMBER BENEFITS Daniel Geschwind, UCLA Andrew Oswald, U. of Warwick Xiaowei Zhuang, Harvard U.
INSTITUTIONAL SALES Karl-Heinz Glassmeier, Isabella Pagano, Maria Zuber, MIT
AND SITE LICENSES aaas.org/membercentral TU Braunschweig Istituto Nazionale di Astrofisica

sciencemag.org/librarian

Science serves as a forum for discussion of important issues related to the advancement of science by publishing material on
which a consensus has been reached as well as including the presentation of minority or conflicting points of view. Accordingly,
all articles published in Science—including editorials, news and comment, and book reviews—are signed and reflect the individual
views of the authors and not official points of view adopted by AAAS or the institutions with which the authors are affiliated.

636 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 sciencemag.org SCIENCE

Published by AAAS

EDITORIAL

Gradually, then suddenly

R acism, climate denial, and coronavirus disease said, “I don’t think science knows, actually.” Perhaps
2019 (COVID-19) are major crises standing in Trump knew he was saying something untrue but that
the way of a prosperous future for the United many Americans agree with. Will wholesale environ-
States, and resolution of all three could be en- mental destruction have to occur before the United
abled by science that is persistently ignored. In States does something about climate change?
Ernest Hemingway’s novel The Sun Also Rises,
When it comes to COVID-19, White House Chief of

a character named Mike is asked how he went Staff Mark Meadows admitted, “We’re not going to con-

bankrupt. “Two ways,” he answers. “Gradually, then sud- trol the pandemic,” making clear that Trump’s only strat- H. Holden Thorp
Editor-in-Chief,
denly.” The resistance of U.S. policy to science has egy is to wait for therapeutics and vaccines to soften the Science journals.
[email protected];
followed a similar path: It gradually built up over 40 blow. Although prospects for both look promising, we @hholdenthorp

years, beginning with the election of Ronald Reagan, are months, if not a year, away from reasonable supplies

but suddenly reached a tipping point in the chaos of of either. In the same interview, Meadows said that we

2020. Will the path to resolution would defeat the virus “because

also be gradual and then sudden, we’re Americans.” Such national-

and if so, at what cost? “Racism, climate istic exceptionalism is embarrass-
A saying incorrectly attributed denial, and ing. The virus doesn’t “know” who
is an American. Must hundreds of
to Winston Churchill holds that thousands more people die before
Americans always do the right the United States recognizes that
thing but only after all other pos-

sibilities have been exhausted. COVID-19 are major humility in the face of challenge is
Whatever the source, the idea the way to save lives?

lives on because it resonates and crises standing Now that so many possibilities
is no more apparent than in the have been tried and exhausted,

failure of the United States to ag- in the way of a can science help push the coun-
gressively deal with 400 years of try toward resolving these issues?

racial injustice. Slavery ended, prosperous future Science must deal with the sys-
but only after a civil war and temic racism that persists in our

decades of delay. The civil rights for the enterprise. There are scientifi-
movement created important cally sound measures that could

positive change, but only after United States…” promote greater racial justice in
civil rights leaders Dr. Martin America, but the scientific com-

Luther King Jr. and John Lewis munity is in no position to advo-

boxed in President Lyndon John- cate for racial justice if its own

son so that he had little choice house is not in order, and that

but to champion legislation or be associated by his- requires difficult soul-searching about the underrepre-

tory with staunch segregationist George Wallace. Will sentation of racial and ethnic groups as well as norms

people of color in the United States have to endure and practices of science that are not inclusive. Scientists

yet more violence from white supremacists before the must continue to speak out. Skepticism of the peril of

next inflection toward racial justice? COVID-19 has brought forth the response of science in

As for confronting climate change, the prospects ways never before seen. Scientists must hold on to that

seem distant. Support for climate science has been voice once the world gets past the pandemic. The old

steadily undermined by politicians catering to busi- ideal of keeping politics out of science has not served

nesses dependent on fossil fuels and by religious con- the United States well. And scientists must continue to

servatives suspicious of science because it argues for do the best science. Eventually, society will ask for help.

evolution. When California’s Secretary for Natural Re- Let’s make sure science has the goods when they do.

sources Wade Crowfoot challenged President Donald

Trump on climate change, the president laughed and –H. Holden Thorp

PHOTO: CAMERON DAVIDSON 10.1126/science.abf5396
6 NOVEMBER 2020 • VOL 370 ISSUE 6517 639
SCIENCE sciencemag.org

Published by AAAS

NEWS “ ”We’re in for a whole lot of hurt. It’s not a good situation.
Anthony Fauci, director of the U.S. National Institute of Allergy and Infectious Diseases,
describing in The Washington Post the Trump administration’s
disjointed, inadequate approach to controlling COVID-19 as U.S. infections rise.

IN BRIEF
Edited by Jeffrey Brainard

A man prepared to vote last week in a trailer outside of SoFi Stadium in Inglewood, California. Poll workers and early voters across the United States donned safety gear
to complete balloting for the country’s elections before the final day of voting on 3 November. To reduce crowds, many election officials set up makeshift polling places.

Probe of virus origin begins online of the effort, but he didn’t say when. U.S. disease spread. The survey suggests a big PHOTO: BRITTANY MURRAY/MEDIANEWS GROUP/LONG BEACH PRESS-TELEGRAM VIA GETTY IMAGES
President Donald Trump has criticized hurdle is reaching people at all; 80% of
COVID-19 | After an in-person planning WHO for not confronting China about participants said they don’t pick up phone
visit in August, a long-awaited investigation how it has handled the virus, but the calls from unknown numbers, and only
into the origins of the pandemic coronavirus, agency has chosen to encourage coopera- 67% said they would check voicemail from
organized jointly by the World Health tion, noting it has no authority to compel such numbers.
Organization (WHO) and China, got off to China’s assistance.
a virtual start on 30 October, when Chinese Slovakia tries wide virus testing
and international teams exchanged infor- Contact tracing faces doubts
mation during an online meeting. They COVID 19 | Slovakia last week tested more
described progress tracing the virus to its PU B L I C H E A LT H | U.S. health officials than half of its 5.5 million people for
presumed animal source, according to a tracking down people potentially exposed the pandemic coronavirus. The government
statement released by China’s National to the virus that causes COVID-19 likely hopes the ambitious program will avert
Health Commission. But the session was confront several layers of discomfort the need for a second lockdown as cases
private, and neither China nor WHO and mistrust, according to survey results surge in Europe. Of the 3.6 million residents
identified the scientists involved. The New published last week by the Pew Research tested last weekend, 38,359 tested positive
York Times reported one American is on Center. The group asked 10,211 adult and are required to self-isolate for 10 days
the WHO team, whose members China Americans in July how comfortable they or face a fine of €1650 ($1918). Those who
got to approve. The newspaper, citing were with various steps in the contact decline to be tested are also required to iso-
WHO documents, also says the Chinese tracing process and how likely they were late. The antigen tests being used are faster
side will conduct the key studies in that to participate. Only 48% said they would but less accurate than polymerase chain
country, with the WHO team reviewing be comfortable or likely to engage in reaction tests, prompting critics to warn
them. Michael Ryan, WHO’s executive all three key steps: speaking to a public that they may fail to diagnose up to 30%
director for health emergencies, said at a health official, sharing information about of positive cases, which risks letting infected
30 October press briefing “we fully expect” recently visited locations and contacts, people spread COVID-19. Another wave of
WHO investigators to visit China as part and quarantining to prevent further mass testing is planned for 6–8 November.

640 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 sciencemag.org SCIENCE

Published by AAAS

NIH finalizes data-sharing rule C O N S E R VAT I O N

BIOMEDICINE | Starting in January 2023, United States removes gray wolf from endangered list
all biomedical researchers newly funded
by the U.S. National Institutes of Health T he Trump administration last week announced it is removing the protections of
(NIH) will be required to share data from the U.S. Endangered Species Act for the estimated 6000 gray wolves (Canis lupus,
their studies or explain why they can’t. above) living in the lower 48 states. The decision to give state and tribal agencies
The new policy updates a 2003 require- primary responsibility for wolf management reflects “the best scientific and com-
ment that covered only large projects mercial data available,” Secretary of the Interior David Bernhardt said on 29 October.
with more than $500,000 per year in But many conservation groups disagree and say they will sue to overturn the delisting,
funding. Now, all scientists submitting a which takes effect 4 January 2021. They argue that gray wolf populations in the lower
grant application must include a plan for 48 states, which some 45 years ago had dwindled to fewer than 1500 individuals, are
sharing data produced by their research, not fully restored. The critics also contend that the administration has ignored research
preferably in established repositories. indicating that lifting federal safeguards could endanger some populations by allowing
NIH will allow certain exceptions, such greater hunting. Courts have rejected previous efforts to entirely end federal protection
as when ethical or legal reasons preclude for the wolves, and a new U.S. administration could seek to reverse the decision.
disclosing anonymized information about
PHOTO: THOMAS MANGELSEN/MINDEN PICTURES people studied in clinical trials. Although tested the concept on a large scale start- BY THE NUMBERS
a draft policy released 1 year ago merely ing in 1999 and has now been upgraded
urged “timely” sharing, the final policy with extra heating power. 300 million
sets a deadline: when a study is published
or a grant ends, whichever comes first. U.S. withdraws from Paris accord Estimate of potentially habitable planets
NIH can cancel a grant or withhold in the Milky Way, extrapolated from
future funding for failure to comply C L I M AT E C H A N G E | The United States the 2800 exoplanets discovered by
with the policy. this week was scheduled to formally
withdraw from the Paris agreement to NASA’s Kepler satellite and data from
Millions sought for Arecibo repair control greenhouse gas emissions, as the European Space Agency about
President Donald Trump had announced
ASTRONOMY | Managers of the Arecibo in 2017. But “depending on the result stars’ brightness. The estimate applies
radio telescope, the world’s second of the U.S. election, this may be nothing to Earth-size planets that orbit Sun-like
largest, have asked the National more than a footnote in history,” note
Science Foundation (NSF) for at least Nathaniel Keohane and Kelley Kizzier stars and are warm enough to have
$10.5 million for repairs, United Press of the Environmental Defense Fund, an liquid water on their surfaces. (Upcoming
International reported this week. In advocacy group. If Democrat Joe Biden
August, a support cable slipped out of wins the presidency, he has said the issue of The Astronomical Journal)
a socket and damaged part of the instru- United States, the world’s second largest
ment’s dish, which is nestled in hills emitter, will immediately rejoin the pact. 16%
in Puerto Rico. An investigation has not Other countries are expected to press a
yet determined why the device failed, Biden administration to set an ambitious Share of U.S. patent applications in 2018
but as a precaution, managers may goal for reducing carbon. China and for inventions involving artificial intel-
replace other cables at risk, which could the European Union have recently
bring the final repair bill past $20 million, promised emissions cuts deeper than ligence, up from 9% in 2002. More than
said Ray Lugo of the University of their original commitments. 60,000 applications were filed in 2018.
Central Florida, which manages the
telescope for NSF, the owner. (U.S. Patent and Trademark Office)

Spherical fusion reactor turns on

ENERGY | The United Kingdom’s revamped
fusion reactor, known as the Mega Amp
Spherical Tokamak (MAST) Upgrade,
achieved its first plasma last week after a
7-year rebuild. The £55 million device
may provide a stepping stone to an energy-
producing facility. Doughnut-shaped
tokamaks aim to generate energy by using
powerful magnets to contain an ionized
gas—or plasma—of hydrogen isotopes,
heated by microwaves and particle
beams to encourage fusion of the nuclei.
Spherical tokamaks are shaped more like
a cored apple than a doughnut, which
researchers believe makes the roiling
plasma more stable. MAST Upgrade first

SCIENCE sciencemag.org 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 641

Published by AAAS

IN DEPTH

President Donald Trump and FDA Commissioner Stephen Hahn (right) met with Gilead CEO Daniel O’Day (left) after remdesivir received an emergency use authorization.

COVID-19

‘A very, very bad look’ for remdesivir

FDA and Europe anointed it as a key therapy just after a major study found it has little value

By Jon Cohen and Kai Kupferschmidt usual circumstances that gave the company mas the very day of the remdesivir approval.
Gilead, for its part, acknowledges it had seen
important advantages. FDA never consulted an early draft of the Solidarity results before
signing the EU deal. But Gilead has aggres-
O ctober was a good month for Gil- a group of outside experts that it has at the sively challenged the validity of the data, in
ead Sciences, the giant U.S. manu- ready to weigh in on complicated antiviral part because the study was done in countries
facturer of antivirals. On 8 October, drug issues. FDA can tap that group, the with widely varying health care standards.
the company inked an agreement to Antimicrobial Drugs Advisory Committee
supply the European Union with its (AMDAC), to review all available data on That criticism has angered Solidarity in-
vestigators. Half the patients who received
drug remdesivir as a treatment for experimental treatments and then make rec- remdesivir were treated in Europe and Can-
ada, WHO notes, and the others were not
COVID-19—a deal potentially worth more ommendations about drug approvals—yet it necessarily in countries with substandard
health care. “It’s appalling to see how Gil-
than $1 billion. Two weeks later, on 22 Octo- has not convened once during the pandemic. ead tries to badmouth the Solidarity trial,”
says Marie-Paule Kieny, director of research
ber, remdesivir became the first COVID-19 The EU, meanwhile, agreed to the rem- at the French medical research agency IN-
SERM and a former WHO officer.
drug approved by the U.S. Food and Drug desivir purchase price exactly 1 week before
HOPES THAT FADED
Administration (FDA). The deci- the disappointing Solidarity trial On 10 January, 2 days after China revealed
SARS-CoV-2 causes COVID-19, researchers
sions mean Gilead can cash in big results came out. It was unaware of published an encouraging study in Nature
Communications about remdesivir, origi-
in two major markets, both with Science’s those results, but Gilead knew the nally developed to fight the Ebola and hepa-
titis C viruses. In both test tube and mouse
soaring COVID-19 cases. COVID-19 trial was a bust; it had begun to re- studies, it had powerful inhibitory effects
But they baffled scientists who reporting is view the data on 23 September. on a SARS-CoV-2 relative that causes Mid-
supported by the dle East respiratory syndrome. Two weeks
have closely watched the clinical Pulitzer Center “This is a very, very bad look later, doctors treated the first confirmed
trials of remdesivir unfold over for the FDA, and the dealings be- U.S. case with the drug and reported the
the past 6 months—and who have and the tween Gilead and EU make it an- 35-year-old man improved rapidly.
many questions about its worth. Heising-Simons other layer of badness,” says Eric
An interim analysis from a large-scale clin-
Foundation. ical trial by the National Institutes of Health
(NIH), announced on 29 April, showed the
At best, one large, well-designed Topol, a cardiologist at the Scripps drug reduced the median recovery time of
severely ill, hospitalized COVID-19 patients
study found that remdesivir, which must Research Translational Institute. from 15 days to 11 days. A second study, in
China, appeared the same day and found no
be infused intravenously, modestly reduced FDA has no obligation to convene the

the time to recover from COVID-19 in hos- panel for its decisions, stresses AMDAC mem-

pitalized patients with severe illness. A few ber David Hardy, an HIV/AIDS scientist of

smaller studies found no impact on the the University of California, Los Angeles. Yet

disease whatsoever, and none has found Hardy is “amazed” the agency didn’t consult

that the antiviral reduces patients’ level of it in this case. “This sets the standard for the

SARS-CoV-2, the causative virus. Then, on first COVID-19 antiviral,” he says. “That really

15 October, the fourth and largest study is something that’s very, very important.” PHOTO: ALEX BRANDON/AP PHOTO

delivered what some believed was a coup FDA did not respond to Science’s request

de grâce: The World Health Organization’s to discuss why it opted against convening

(WHO’s) giant Solidarity trial showed that the committee, noting only that it is “at the

remdesivir does not reduce mortality or the discretion” of division directors. But FDA’s

time COVID-19 patients take to recover. inaction stands in sharp contrast to its han-

Science has learned that both FDA’s deci- dling of COVID-19 vaccines; it convened an

sion and the EU deal came about under un- advisory group to discuss potential dilem-

642 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 sciencemag.org SCIENCE

Published by AAAS

NEWS

statistically significant benefit, however. Two before joining the trial and will receive the complicated decisions given the imperfect
days later, FDA granted an emergency use au- full data set once the study is complete, and nature of the data. … The urgency of the clini-
thorization (EUA) that allowed the drug to be that FDA traditionally reviews all available cal use gives all the more reasons to have an
given for severe COVID-19, a move President data, including unpublished findings. open discussion,” says Baden, whose group
Donald Trump praised in an Oval Office press last met in October 2019.
event with Daniel O’Day, CEO of Gilead. Clifford Lane of the National Institute of
Allergy and Infectious Diseases, who helped EUROPE IN THE DARK
But the mixed messages about the drug run the NIH study, says its main difference EMA, Europe’s FDA counterpart, in July gave
continued: In August, a Gilead-sponsored with Solidarity is “the degree of granularity” “conditional approval” to remdesivir—similar
study showed patients with moderate pneu- of the analyses of subgroups that may have to an EUA—but it has yet to give its full bless-
monia treated for 5 days with remdesivir im- benefited. “I think the Solidarity data are ing. The European Union nevertheless has
proved more quickly than those who received fine,” Lane says. “It’s a very large study and it negotiated a “joint procurement agreement”
standard care, but oddly, those treated for has a very robust endpoint.” with Gilead, signed on 8 October, that secures
10 days did not. Nevertheless, shortly after- as many as 500,000 treatment courses for
ward, FDA expanded remdesivir’s EUA to in- Richard Peto, a University of Oxford stat- $1.2 billion. A spokesperson for the European
clude all hospitalized COVID-19 patients. istician and epidemiologist who helped de- Commission confirms to Science it was not
sign Solidarity and analyze the data, stresses informed of the drug’s failure in the Solidar-
To Topol, FDA’s move resembled heavily that the WHO trial cannot prove remdesivir ity trial until the next day: “There was no dis-
criticized EUAs issued earlier for the ma- has no benefit for COVID-19. “Gilead and the cussion with WHO about the ongoing study
laria drug hydroxychloroquine—which the FDA have sort of maneuvered us into a posi- prior to signing the contract.”
agency later rescinded—and antibody-rich tion where we’re being asked to try and prove
“convalescent” plasma. In an open letter remdesivir does nothing rather than asking When Science asked Gilead why it didn’t
to FDA Commissioner Stephen Hahn, he the usual way round, which is, ‘Can the man- disclose the Solidarity data during the ne-
wrote: “These repeated breaches demon- ufacturers prove it does something?’” gotiations, the company said the draft
strate your willingness to ignore the lack of manuscript it received from WHO in late
scientific evidence, and to be complicit with It’s still possible that remdesivir might September was “heavily redacted.” WHO says
the Trump Administration’s politicization of help people at early stages of disease, says
America’s healthcare institutions.” Martin Landray of Oxford, who is co-leading

Many scientists expected WHO’s Solidar- Remdesivir’s route to approval
ity trial—which had 2750 patients on remde-
sivir, about three times as many as all other The antiviral drug won U.S. approval for treating COVID-19 and a potentially lucrative deal with the European
published trials put together—to resolve the Union even as initial studies suggesting modest efficacy were followed by disappointing Solidarity trial data.
drug’s worth. Conducted in 30 countries, Sol-
idarity compared remdesivir and three other 29 April 1 May 23 September 8 October 9–10 October 15 October 22 October
repurposed drugs with each other and the NIH trial EU/Gilead EU and FDA
standard of care. (Unlike the NIH and Chi- suggests FDA allows Gilead learns $1.2 billion learn Solidarity WHO announces FDA approval
nese trials, it did not use a placebo.) None of beneHt agreement result
the drugs lowered mortality among hospital- emergency Solidarity result Solidarity result
ized patients, it found, and the investigators
also noted that remdesivir did not affect use
“the duration of hospitalization” or whether
COVID-19 patients required ventilators. Jan. Feb. Mar. Apr. May Jun. Jul. Aug. Sep. Oct. Nov. Dec.

GRAPHIC: C. BICKEL/SCIENCE Solidarity described the results to FDA rep- the world’s largest study of various COVID-19 the only information blacked out was results
resentatives on 10 October and in a preprint treatments. But it “definitely doesn’t work in relating to the other drugs used in the trial
posted 5 days later. But 1 week after that, FDA the sickest patients where the biggest gains because of confidentiality agreements.
approved the drug, having reviewed data would be.” Treating patients earlier comes
only from the NIH study and two Gilead- at a price. “You won’t save many lives, and Although the agreement with Gilead
sponsored trials. It had ignored the Solidarity you’ll have to treat a lot of patients,” he says. locks EU members into a price of about
data as well as the findings in China. “And it’ll cost you a fortune.” $2400 for a full course of remdesivir, it does
not obligate any countries to purchase the
That infuriated the Solidarity team. “The At the same time, the trials have not ruled drug, the Commission spokesperson says.
mantra I’ve always heard as a joke about out the possibility of harmful side effects. In But Yannis Natsis of the nonprofit Euro-
the FDA is that they say ‘In God we trust, late August, WHO noted a disproportionately pean Public Health Alliance says that given
everyone else has to provide data,’” Kieny high number of reports of liver and kidney the Solidarity results, the European Union
says. “So look at all the data.” problems in patients on remdesivir. And the “should at least renegotiate the volume of
European Medicines Agency (EMA) said last the doses and the price.”
Gilead Chief Medical Officer Merdad month that its safety committee had begun
Parsey argued in an open letter posted the to assess reports of acute kidney injuries in To Kieny, this investment in a drug that
day of FDA’s remdesivir approval that Soli- some patients taking the drug. may help just a few patients is an “enor-
darity “does not negate other study results— mous” waste. “You can always say, ‘OK, now,
particularly from a trial designed with the To many scientists, such complexities if I disaggregate the population and if I take
strictest of scientific standards,” like NIH’s underscore that FDA should have consulted only those who have a blue eye and a wooden
study. The company further noted that the AMDAC, its panel of outside experts, for a vig- leg, maybe this is very effective,’” she says.
Solidarity results have not been peer re- orous debate. It could have “elevated the dis-
viewed and told Science WHO had yet to cussion,” says AMDAC Chair Lindsey Baden, On 28 October, Gilead told investors that
provide Gilead “the underlying data sets or an infectious disease specialist at Brigham remdesivir has brought in $873 million so
statistical analysis plan” for the trial. and Women’s Hospital. “Hydroxychloroquine, far this year. “We’re proud to be at the front
convalescent plasma, remdesivir—these are end of this with a very potent antiviral,”
WHO says Gilead knew the analysis plan O’Day said. j

SCIENCE sciencemag.org 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 643

Published by AAAS

A terrace in Quedlinburg remained empty after
Germany’s new lockdown took effect on 2 November.

COVID 19 the spring, with varying degrees of intensity.
Europe has had a more science-driven pan-
Europe is locking down again—
but its strategy is unclear demic response than the United States, but
unlike many Asian countries, it was unable
Without a plan to eliminate the virus, countries may face to avert a resurgence. Instead of using the
shutdowns over and over, scientists warn summer to drive cases down to practically
zero, Europe celebrated the holiday season.
By Kai Kupferschmidt, in Berlin blissful summer lull, countries still held People seemed to lose their fear of the virus, PHOTO: KLAUS-DIETMAR GABBERT/PICTURE ALLIANCE/GETTY IMAGES
out hope that more limited, targeted mea- says Michael Meyer-Hermann, a modeler at
S hortly before 11 p.m. on 1 November, a sures could prevent a second wave (Science, the Helmholtz Centre for Infection Research
waitress passed out paper cups to the 4 September, p. 1151). Now, that wave is here, who was involved in drawing up Germany’s
customers crowded around the tables with the force of a tsunami. Europe has sur- lockdown plans. They increasingly flouted
outside Luzia, a bar in Berlin’s lively passed the United States in cases per capita; rules on physical distancing, mask wearing,
Kreuzberg district. “I’m sorry, but last week, it accounted for half of the more and avoiding large gatherings.
you all have to leave,” she said. “God, than 3 million cases reported to the World
in 2 minutes it’s going to be lockdown,” a Health Organization (WHO). “Europe is at “The infectious seeds in the commu-
woman at one table said, as guests poured the epicenter of this pandemic once again,” nity have always remained above a certain
the remainder of their cocktails into the WHO’s regional director for Europe, Hans threshold, where if you relax the physical dis-
cups. The fun was over: For the second time Kluge, said on 29 October. tancing, it’s all going to come back,” says Uni-
this year, Luzia had to close on the German versity of Hong Kong epidemiologist Gabriel
government’s orders. Most countries are reacting without a Leung. Numbers crept up and overwhelmed
long-term plan, simply trying to avoid the the other pillar of virus control: testing, iso-
All restaurants, bars, gyms, and theaters worst. Officials differ about the best way to lating cases, and tracing and quarantining
in Europe’s largest economy will remain shut bring the numbers down again, and how their contacts. The fact that life has largely
until at least the end of the month in a new low a level they should strive for. And no moved indoors in recent weeks likely aided
bid to halt the spread of COVID-19. Hotels are one knows what comes next. Short of vac- the resurgence, and cooler air may also favor
no longer allowed to host tourists. Residents cines to save the day, countries may face an the virus. “I think winter does make things
have been asked to meet people from only exhausting series of lockdowns—a sawtooth much harder,” says Adam Kucharski of the
one other household. Florent, the manager at pattern, “up and down and up and down,” London School of Hygiene & Tropical Medi-
Luzia, took some hope from the fact that Ger- that could wreck the economy, says Albert cine. “Countries have probably been doing
many was locking down while cases were still Osterhaus, a virologist at the University of control on ‘easy’ setting over the summer.”
lower than in neighboring countries. “Hope- Veterinary Medicine, Hanover. “There is no
fully we’ll reopen in a month,” he said. strategy in Europe,” he concludes. Not everyone is convinced lockdowns are
the answer. On 28 October, the day Chan-
With COVID-19 cases mounting and The lockdown seemed an almost shock- cellor Angela Merkel announced the new
threatening to overwhelm health care capac- ingly blunt tool when China first applied it measures, Germany’s National Association
ity, much of Europe has taken similar mea- in Hubei province on 23 January. But it also of Statutory Health Insurance Physicians
sures to curb human contacts. Two months proved remarkably effective, and countries presented a strategy paper arguing against a
ago, as numbers began to creep up after a around the world took the same approach in lockdown. “We cannot put the entire country,
or even a continent, into an induced coma
for weeks or months,” said Andreas Gassen,
head of the association. Another co-author,
virologist Jonas Schmidt-Chanasit of the Ber-
nhard Nocht Institute for Tropical Medicine,
is convinced Germany’s prelockdown restric-
tions would be enough to keep the virus from
resurging—if they were strictly followed. In-
stead of closing tens of thousands of public
places and spending billions to keep them
afloat, Germany should spend money on
communicating the need to better follow the
rules, enforcing them strictly, and even cre-
ating some opportunities for people to safely
enjoy riskier things such as parties, he says.

But most scientists say lockdowns are now
unavoidable, although they need not be as
draconian as in the spring, Kucharski says.
Back then, “Countries were just doing abso-
lutely everything at the same time,” he says.
Now, they can skip measures that severely
restrict people’s lives but don’t contribute
much to virus control. “There’s no reason
we need to lock people in their home,” for

644 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 sciencemag.org SCIENCE

Published by AAAS

NEWS | IN DEPTH

instance, as long as they keep their distance BIOLOGY
outside, says Devi Sridhar, chair of global
public health at the University of Edinburgh. Growth spurt for height genetics

The biggest difference from the spring By tallying thousands of genetic variants, researchers
may be that may countries are keeping account for height’s remaining “missing heritability”
schools open. Karl Lauterbach, a health
policy expert and member of the Bund- By Jocelyn Kaiser by the GWA studies, gene-gene interactions,
estag for the Social-Democratic Party
who helped design Germany’s “lockdown and that the twin studies were wrong. But
light,” says it’s clear schools do contribute
to the spread of the virus. “Merkel asked: F or height, DNA is largely destiny. Peter Visscher, leader of Yengo’s team,
‘Am I sure we can do this without clos- Studies of identical and fraternal argued it was partly a matter of finding
ing schools?’ I said no, but probably yes,” twins suggest up to 80% of variation many more common variants with very
Lauterbach says. But the harm of school in height is genetic. But the genes small effects. He estimated that such vari-
closures was deemed too great, he says. responsible have largely eluded re- ants should account for 40% to 50% of

Calculations suggest Germany needs to searchers. Now, by amassing genome the genetic component of height. Pick-
reduce contacts between people by roughly
75% from the current level, Lauterbach says. data for 4 million people—the largest such ing out the faint signals would require
“That is incredibly hard if you want to keep
schools and most businesses open.” But bars study ever—geneticists have accounted for a studying the DNA of a huge number of
and restaurants account for many contacts
while providing only about 1% of Germany’s major share of this “missing heritability,” at people, however.
gross domestic product, making them “kind
of the perfect target for pandemic measures.” least for people of European ancestry. In this By 2018, Visscher’s team and other mem-

The first wave of lockdowns provided group, they’ve identified nearly 10,000 DNA bers of a global consortium called GIANT
other lessons. For one, framing the debate
as a choice between public health and the markers that appear to fully explain the influ- had pooled DNA data for 700,000 people
economy is wrong, Sridhar says: “In the lon-
ger term, having uncontrolled spread is much ence of common genetic variants over height. and found 3300 common markers that
worse for the economy. That’s what we’ve
seen across the world.” Also, locking down “This is a genuine landmark,” says explained 25% of the variation in height.
later means locking down longer. “If you wait
until your infection level is quite high, proba- Daniel MacArthur of the Garvan Institute Now, by looking across DNA from 201 GWA
bly your 2-week lockdown is going to become
a 3-month lockdown,” Sridhar says. of Medical Research in Australia. studies with 4.1 million participants, GI-

Europe’s bigger question, however, is what If the missing genetic contributors to other ANT has brought the total to roughly 9900
comes next. Osterhaus says the strategy
should be to get cases to zero using a hard traits and diseases can be identified, and ex- common markers, accounting for 40%
and long lockdown, combined with strict bor-
der controls and quarantines to keep the vi- tended to other ancestries, the results could of the variation. Other markers located
rus out. That strategy, applied successfully by
China, Australia, and New Zealand, may be “inform new biology and con- nearby and likely inherited
politically unpalatable, however, and would
require intense coordination between coun- “This is a genuinetribute to personalized medi- together account for another
tries. “I can understand why that didn’t hap- 10% of height variability.
pen,” Leung says. “But the virus couldn’t care cine,” suggests Loïc Yengo of
less whether there are good or not so good
reasons.” Others are urging governments to the University of Queensland landmark.” That’s still short of the 80%
follow South Korea’s example: Drive cases to in St. Lucia, Australia, whose predicted by twin studies. But
low numbers while improving the system of
testing, tracing, and case isolation enough to team presented the work online Daniel MacArthur, last year, Visscher’s group drew
keep the virus from resurging.
this week at the annual meet- Garvan Institute on whole-genome sequenc-
For now, Europe appears to be stuck in a
third scenario: intermittently locking down ing of the American Society of of Medical Research ing data of a smaller number
to prevent the health system from buckling.
“These circuit breakers are almost kicking Human Genetics. For example, of people to demonstrate that
the problem down the road,” Kucharski says.
“The hope is that vaccines and treatments geneticists could more accurately assess peo- rare variants—those carried by fewer than
and better options will be available in the
new year.” Lauterbach says he favored a lon- ple’s risk of diseases from genome scans. But one in 100 people—should explain another
ger lockdown in summer to go for elimina-
tion. But that would be too hard in winter, he the study leaves some scientists dissatisfied 30% of height’s variation. (The result was
says. “All we can do now is break the wave,” he
says. “But the water level will remain high.” j because it identifies only markers linked to released in a March 2019 preprint that the

genes that sway height, not the genes. team is revising.)

The mystery of missing heritability dates Some geneticists say they aren’t surprised

back to the late 2000s, when researchers that heritability gaps can be filled once

began to use new tools to scan human ge- enough people had their DNA scanned. “It

nomes for common markers linked to dis- was expected,” says Aravinda Chakravarti of

eases and traits. They expected the results New York University. The problem remains

of these genomewide association (GWA) that few of the height-linked DNA markers

studies to match evidence from the genet- have been tied to specific genes that clearly

ics of twins and families, such as the over- alter the trait. “It’s mostly all still ‘missing’

whelming influence in wealthy countries of in a biological sense,” says David Goldstein

genes on height, rather than environmental of Columbia University.

factors such as diet or childhood infections. The new findings brighten prospects for

But it turned out that each identified tracking down those genes, Yengo says. In-

marker, which may be in or just near a rele- stead of being scattered randomly across

vant gene, only contributes slightly to a trait the entire genome, which would make it

or disease risk, and tallying them up didn’t challenging to ever get a handle on the

solve the problem. For height, the first specific genes and their roles, the 9900

40 DNA markers linked to the trait ex- or so markers are confined to only about

plained just 5% of its variation. 30% of the genome. And many cluster in

A number of possible explanations areas known to contain genes involved

emerged, including rare gene variants missed in growth. j

SCIENCE sciencemag.org 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 645

Published by AAAS

NEWS | IN DEPTH

The horse was the heart of the mysterious Iron Age Xiongnu empire in Mongolia, as suggested by a decorative bronze belt plate showing two horses grappling.

ARCHAEOLOGY

How the horse powered human prehistory

Wide-ranging warriors made Mongolian empire a melting pot, sweeping gene study shows

By Andrew Curry was not involved in the paper. “The horse introduced their dairy-oriented pastoralist PHOTO: NATIONAL MUSEUM OF MONGOLIA
provided new range in patterns of human lifestyle there. But they left no lasting genetic
U ntil now, the only accounts of the mobility and allowed people to travel long traces in Mongolia, the oldest samples in the
Xiongnu came from their enemies. distance faster.” new study show.
Chinese records from 2200 years ago
describe how these fierce mounted Horses were probably domesticated The ancient DNA does show that
archers from the wide-open steppes by the Botai culture around 3500 B.C.E. 1000 years later, another group from the
of today’s Mongolia clashed with near what is modern Kazakhstan (Science, steppes, called the Sintashta, left a lasting
armies in what is now northwestern China. 11 May 2018, p. 587). Horses may have been imprint. They also brought fateful cultural
Their onslaughts spurred the Chinese to mainly used for meat and milk at first, and changes to Mongolia’s grasslands, as earlier
build what would become known as the later began to pull wheeled chariots. archaeological studies had shown. Starting
Great Wall of China on their northern in about 1200 B.C.E., equestrian innovations
border, as protection against the mounted To learn more about human migra- including selective breeding for size and en-
nomads. They also started to raise cavalry tion across Central Asia, a team led by durance, plus bridle bits, riding pants, and
armies of their own. Choongwon Jeong of Seoul National Uni- even early saddles, appeared in the record,
versity and Harvard University’s Christina says archaeologist William Taylor of the
The equestrian empire of the Xiongnu left Warinner sampled and sequenced DNA University of Colorado, Boulder, a co-author
no written records. But biology is now filling from human remains found in Mongolia. on both papers.
out their story, and those of other Central The results, which they report this week in
Asian cultures in antiquity. Two studies—a Cell, span the period from 5000 B.C.E. all the Mongolians of the time were obviously rid-
sweeping survey of ancient DNA from more way to the heyday of another horse-riding ing horses, as vividly confirmed by the sec-
than 200 individuals across 6000 years culture—that of Genghis Khan’s Mongol ond paper, in the Proceedings of the National
and an analysis of horse skeletons from Empire, around 1000 C.E. Academy of Sciences. The authors, Chinese
just before the rise of the Xiongnu—trace and U.S. archaeologists, report that horse
population movements across Central Asia Genetic studies of Western European skeletons buried around 350 B.C.E. in the
and the key role played by horsemanship. populations have shown that around 3000 Tian Shan mountains, now part of China’s
The results “show the horse was probably B.C.E., the Yamnaya—mobile herders of cat- Xinjiang province, show bone abnormali-
the driver of some of the ancestry shifts we tle, sheep, and goats—pushed west from the ties from riding, including spinal damage
see in the human population,” says Ludovic steppes of what is today Russia and Ukraine from the weight of a rider and changes to
Orlando of Paul Sabatier University, who and triggered a dramatic genetic turnover in the bones of the mouth from bits and bridles.
Europe. Skeletons from Bronze Age Mongolia “Put the lower back pathologies together
had shown the Yamnaya also moved east and

646 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 sciencemag.org SCIENCE

Published by AAAS

with evidence for a bridle, and it all suggests TECHNOLOGY
horses were being ridden,” says Sandra Olsen,
an archaeologist at the University of Kansas, New chip-based lasers promise
Lawrence, who was not part of either study. practical terahertz imaging

Not long after, the Xiongnu emerged. Semiconductor lasers work with small coolers, enabling
They translated their skills on horseback medical imaging and contraband detection
into a sophisticated means of waging war
and organizing an empire over vast dis- By Robert F. Service injected into the structure cascade down
tances. Starting in about 200 B.C.E., the
Xiongnu marshalled nomadic tribes from hundreds of energy steps, shedding a pho-
across Eurasia into a formidable force, turn-
ing the steppes into a political center rival- C ompact, chip-based lasers have con- ton at each one. Those photons were infra-
ing neighboring China. “The Xiongnu have quered much of the electromagnetic red in the first QCL, but in 2002 researchers
been a source of constant worry and harm spectrum, from ultraviolet to in- in Italy and the United Kingdom created
to China,” one contemporary Chinese histo- frared, enabling technologies from QCL lasers that emitted terahertz photons.
rian wrote. “They move about in search of digital communications and barcode
water and pasture and have no walled cit- Those devices needed to be chilled to
ies or fixed dwellings, nor do they engage in
any kind of agriculture.” readers to laser pointers and print- 50 K, but last year, researchers led by physi-

Jeong’s study of DNA from 60 human ers. But one key region of the spectrum re- cist Jérôme Faist at ETH Zurich unveiled
skeletons from the Xiongnu’s 300-year-run
shows how the region was transformed into mained untamed: the terahertz band, which a terahertz QCL made up of hundreds of
a multiethnic empire. After more than 1000
years in which three distinct, stable human lies between infrared light and microwaves. alternating layers of gallium arsenide and
populations lived side by side on the Mon-
golian steppe, genetic diversity rose sharply Engineers hankered for a ready source of aluminum gallium arsenide (AlGaAs) that
around 200 B.C.E. Populations from west-
ern and eastern Mongolia mixed with each terahertz radiation, which can penetrate works at 210 K. It still required bulky and
other and with people carrying genes from
as far away as present-day Iran and Central opaque objects and probe chemical finger- expensive cryogenic coolers, however.
Asia. Such wide-ranging mixing has “never
been seen before at that scale,” Jeong says. prints inside. But compact terahertz lasers At higher temperature the electrons be-
“You can see the entire Eurasian genetic
profile in the Xiongnu people.” have only worked at ultralow temperatures, come unruly, leaping barriers between layers

The results suggest mastery of the horse limiting them mostly to laboratory settings. rather than cascading through the structure
made possible stunning long-distance voy-
ages on Central Asia’s sea of grass. Archaeo- No longer. In this week’s one step at a time. “Over-the-
logical finds in the graves of Xiongnu elites,
such as Roman glass, Persian textiles, and issue of Nature Photonics, barrier electron leakage was
Greek silver, had suggested distant con-
nections. But the genetic evidence suggests researchers report creating the killer,” says Qing Hu, an
something more than trade. Eleven Xiongnu-
period skeletons showed genetic signatures a grain-of-rice–size terahertz electrical engineer at the Mas-
similar to those of the Sarmatians, nomad
warriors who dominated the region north laser on a chip that operates sachusetts Institute of Tech-
of the Black Sea, 2000 kilometers across the
open steppe from Mongolia. at 250 K, or –23°C, a tempera- nology. So Hu and colleagues

“There’s no written evidence of [Xion- ture reachable with a plug-in added more aluminum to the
gnu] contact with Sarmatians, and it’s not
well-attested archaeologically. It’s really cooler the size of a cracker. AlGaAs barriers to better con-
surprising they’re mixing over these long
distances,” says Tsagaan Turbat, an archaeo- “This is a great achieve- fine the electrons. Hu’s team
logist at the Mongolian Academy of Scienc-
es’s Institute of Archaeology. “This kind of ment,” says Miriam Vitiello, also had to prevent electrons
information is really a game changer.”
a condensed matter physicist from interacting in a way that
In the future, researchers hope the ge-
nomes will help reveal how the mysterious at the Nanoscience Institute caused them to leak through
nomad empire worked. The Xiongnu are
“doing the things that empires do—forcing of Italy’s National Research A terahertz laser sits on top of the AlGaAs barriers.
or enticing people to move,” says Univer-
sity of Michigan, Ann Arbor, archaeologist Council. “It has been a long- a small cooler. Now, the researchers have
Bryan Miller. “Are people sent out to rule,
or are local elites allowed to continue?” he term goal in the community shown that by tailoring the
asks. “Only genetics could answer that.” j
to push up the temperature of terahertz la- layered structure even more precisely—

sers,” she adds. “There is now a plethora of some layers were just seven atoms thick—

applications that can be done,” from medical they could make electrons behave at tem-

imaging to explosives detection at airports. peratures warm enough to be reached with

PHOTO: ALI KHALATPOUR/MASSACHUSETTS INSTITUTE OF TECHNOLOGY Standard chip-based lasers generate pho- standard compact thermoelectric coolers.

tons when electrons fall into electron vacan- What’s more, Hu says, the same strategy

cies within a semiconductor alloy, whose should enable the team to eventually make

makeup determines the color. Gallium ni- room temperature terahertz lasers.

tride, for example, emits blue light, whereas Room temperature terahertz sources

gallium arsenide emits red. No semi- could be paired with terahertz detectors

conductor alloys emit photons in the tera- that also work at room temperature, which

hertz range. (“Terahertz” refers to the light’s Vitiello and other researchers are now de-

frequency: trillions of cycles per second.) veloping. That marriage could lead to tech-

In 1994, however, researchers at AT&T Bell nologies such as terahertz imagers able to

Labs created a new kind of laser in which distinguish skin cancer from normal tissue

the semiconductor’s structure, not just its without a biopsy or watch airline passen-

chemistry, determined the wavelength. gers and cargo for hidden explosives, ille-

Called a quantum cascade laser (QCL), gal drugs, and even pharmaceutical fakes.

it contained hundreds of layers of semi- Faist says: “We have hoped for this for a

conductors of precise thicknesses. Electrons very long time.” j

SCIENCE sciencemag.org 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 647

Published by AAAS

NEWS | IN DEPTH

ASTROPHYSICS

Black holes by the dozens challenge theorists

Trove of gravitational wave detections allows black holes to be studied en masse

By Adrian Cho a different direction—and especially if they tent with such a mechanism producing only

spin in the opposite sense of the orbit—the one-quarter of the mergers.

A s children once did before Christmas, black holes probably formed separately and Analyses of all the events also show that
astrophysicists have been eagerly paired up later. when it comes to black holes, “the diversity
awaiting the arrival of a catalog. This is surprisingly large,” says Frank Ohme, a
one lists not toys, but cataclysmic col- It’s hard to tell how the spins of a single pair gravitational wave astronomer at the Max
lisions of objects such as black holes— of black holes align from the burst of gravita- Planck Institute for Gravitational Phys-
tional waves emitted during the merger, says

the ghostly ultraintense gravitational Maya Fishbach, an astrophysicist and LIGO ics. From details of the mergers’ chirplike

fields left behind when massive stars collapse. member from Northwestern University. But signals, scientists can calculate the masses

Last week, it arrived, courtesy of the world’s by analyzing the events en masse, scientists of the colliding black holes. They expected

network of gravitational wave detectors. “It’s have teased out evidence that at least some of to find a “mass gap” between about 45 and

very exciting!” says Selma de Mink, an astro- the mergers involve reversed spins, suggest- 135 solar masses—the result of particle phys-

physicist at Harvard University. “There will ing black hole pairs form in more than one ics processes that should blow apart stars

definitely be a flurry of papers rushing to way. “It seems like there might be multiple within a certain mass range before they can

take the first stabs at the data.” things going on,” Fishbach says. collapse into black holes.

The observations come from three huge L- Rodriguez has argued that the black holes However, LIGO and Virgo have spotted

shaped optical instruments called interfero- could form separately in knots of old stars mergers involving black holes within the

meters that sense gravitational waves, the called globular clusters and then pair up. gap, including one weighing 85 solar masses.

infinitesimal stretching of space triggered by He notes that the overall rate of black hole De Mink, who models the evolution of black

the collisions. Two belong to the Laser Inter- mergers that LIGO and Virgo see seems to hole pairs from binary star systems, says the

ferometer Gravitational-Wave Observatory roughly match the rate his model predicts. “I mass gap is “such a clear prediction from the

(LIGO), instruments with arms 4 kilometers shouldn’t toot my own horn—but I totally am models that it’s hard to believe” it’s not there.

long in Louisiana and Washington that in going to,” he says. But he notes that because Similarly, scientists expected another forbid-

2015 first sensed the chirp of gravitational of the uncertainties, the data are also consis- den range below five solar masses, based not

waves from two black holes spiraling on theoretical modeling, but on obser-

into each other. Virgo, an interferometer vations of individual black holes peace-

near Pisa, Italy, with 3-kilometer-long fully orbiting normal stars. But one

arms, joined the hunt in 2017. black hole falls below that limit.

LIGO and Virgo had already spot- Researchers can even probe how

ted 11 events including a merger of the number of black hole mergers

two neutron stars, which shed light may have changed over cosmic time,

on how the universe forges heavy ele- Fishbach says. The new data show

ments. Now, the team has cataloged the rate 8 billion years ago was no

37 additional black hole mergers, an- more than 10 times what it is now, she

other neutron star merger, and one pos- says, tightening the limit by a factor

sible merger of a black hole and neutron of 10,000.

star. The catalog and statistical analyses, Such data will challenge theorists as

posted 28 October on the physics pre- never before, says Ilya Mandel, a theo-

print server arXiv, “are superimportant,” retical astrophysicist at Monash Univer-

says Carl Rodriguez, an astrophysicist at sity. They can no longer simply whip up

Carnegie Mellon University who was not models to account for oddball events,

involved in the work. “With an individual but have to explain the entire set of IMAGE: LIGO/CALTECH/MIT/SONOMA STATE (AURORE SIMONNET)

event, there’s only so much you can do in observations. “When you have a whole

comparing to astrophysical models. But population things become a lot harder,”

with a catalog you can not only begin to Mandel says. “Your model not only has

constrain the theory, you can start to un- to reproduce the events that you do see,

derstand the landscape.” but also not predict events that you

For example, by analyzing the 47 black don’t see.”

hole mergers together researchers can The LIGO and Virgo teams owe their

probe how the black holes spin—a poten- bounty to their detectors’ ability to spot

tial clue to how the pairs came together. ever fainter, more distant events. And

If both black holes spin in the same sense they want to keep adding to it. “We’ve

that they orbit each other, they might answered a lot of questions we didn’t

have formed from a pair of stars born even know we had,” Fishbach says, “but

together in the same spinning cloud of Merging black holes might spin in different directions—a hint that we raised even more. This is just the be-

gas. If one or both black holes spins in they were born in separate star systems, then found each other. ginning of the science.” j

648 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 sciencemag.org SCIENCE

Published by AAAS

FEATURES

THE LONG SHOT
A little company chases its bigger competitors
in the race for a coronavirus vaccine

By Meredith Wadman, in Gaithersburg, Maryland

E ighteen months ago, a small vaccine- to invade human cells—Novavax’s vaccine
maker here called Novavax faced an outshone major competitors on key measures
existential threat: delisting by the in monkey and early human tests.
NASDAQ stock index. On the heels
of a second failed vaccine trial in The company is one of just seven vaccine-
less than 3 years, the firm’s shares makers to win funding so far from Opera-
had plunged to less than $1 for tion Warp Speed, the giant multiagency U.S.
30 straight days, triggering a warn- government effort aiming to quickly pro-
duce at least 300 million doses of COVID-19

ing by NASDAQ. Frantic to conserve vaccines. But most Warp Speed–backed

cash, the company sold its two Maryland companies are giant pharmaceutical firms,

manufacturing facilities, slicing its payroll and most have already launched late-stage

by more than 100 employees. By January, it clinical trials in the United States. Tiny No-

employed only 166 people. vavax is rushing to keep pace with its larger

“Good ideas. Bad management. … The rivals because companies that win the first

company will probably die soon,” a former approvals from regulators will have big

Novavax manager wrote on Glassdoor.com market advantages. Still, some observers

in October 2019. say Novavax’s technology gives it an edge.

What a difference a year—and a pandemic— “They are incredibly well positioned,”

ILLUSTRATION: A. KITTERMAN AND V. ALTOUNIAN/SCIENCE make. Today, Novavax is slated to receive up says Andrew Ward, a structural biologist

to $2 billion from the U.S. government and a at Scripps Research. Ward, who receives no

nonprofit organization to develop and manu- payments from the company but owns some

facture a coronavirus vaccine. The company’s stock, led a team that last month published

stock closed at $80.71 per share a paper in Science describing the

on 30 October, it has hired more structure of Novavax’s tailormade

than 300 new employees, and this Science’s spike protein, the heart of its vac-

Novavax’s vaccine is made of tiny month it plans to launch a piv- COVID-19 cine. He was impressed by its sta-
particles studded with the coronavirus otal clinical trial of its coronavirus reporting is bility and conformation, as well as
spike protein plus honeycomblike vaccine in the United States and supported by the the vigorous antibody responses
molecules, derived from plants, that Mexico. Made by moth cells har- Pulitzer Center it has elicited in humans and ani-
stimulate the immune system. nessed to crank out the virus’ spike mals. “They have the know-how,”
protein—which the pathogen uses and the he says. “And they obviously, as we
SCIENCE sciencemag.org Heising-Simons

Foundation.

6 NOVEMBER 2020 • VOL 370 ISSUE 6517 649

Published by AAAS

NEWS | FEATURES

Novavax scientist Nita Patel (left) examines a plate measuring antibodies in vaccinated monkeys; other staffers gauge how the vaccine’s protein binds to human cells.

confirmed, make a good product.” the end of a pivotal trial. The company had Developers of protein vaccines must PHOTOS: ALYSSA SCHUKAR
But other people are skeptical. They note also created protein subunit vaccines against develop their own version of the spike
two close cousins of the pandemic virus—the protein—one that closely mimics the natu-
that Novavax has focused on making vac- coronaviruses that cause severe acute respi- rally occurring spike and is stable enough
cines for more than 20 years but has never ratory syndrome and Middle East respiratory to retain its immunological punch during
brought one to market, and that its senior syndrome, using those viruses’ spike proteins. manufacturing, packaging, and distribu-
executives have sold tens of millions of dol- Those vaccines hadn’t made it to market, but tion. Most such vaccines include an addi-
lars of company stock since its share price Novavax had plenty of experience with the tional compound called an adjuvant to help
began to soar this summer. coronavirus family. Glenn believed it was his stimulate a strong, protective immune
company’s moment. response. Those extra steps make protein
Most significantly, the company has an vaccines slower to develop than those that
Achilles’ heel. Novavax must rely mostly on The gene for the spike protein was slow deliver genetic instructions.
contract manufacturers to meet its ambi- to arrive, however. Finally, at 6 a.m. on
tious goal for 2021: producing enough vac- 3 February, a vice president from the sup- But protein-based vaccines also have a
cine to give 1 billion people two shots each. plier hand-delivered a red-capped vial long track record of effectiveness, in con-
If manufacturing problems crop up—and bearing the gene to Novavax’s beige brick trast with the newer, largely unproven
the company last week said manufacturing building here. The virus still hadn’t been of- approaches. The successful hepatitis B vac-
delays had slowed launch of its late stage ficially named—the vial was labeled “Cov/ cine licensed in 1986 and recommended
North American trial—competing vaccines Wuhan”—but Novavax was now out of the for all U.S. babies in their first day of life
may surge ahead. “That’s concerning,” says gate and in the race to tame it. is a protein subunit vaccine. So are a flu
David Maris, a veteran drug industry ana- vaccine approved in 2013 and the human
lyst and managing director at Phalanx In- The company’s scientists started to work papillomavirus vaccines that have sent rates
vestment Partners. Where small companies “with frenetic pace,” Glenn says. Some of of cervical cancer plunging since the first
such as Novavax are concerned, he adds, their competitors were already a lap ahead, ones were licensed in the 2000s.
“people do want to believe in fairy tales.” working on their own vaccines. “There’s no
question [that we’re] behind” several compa- Perhaps because the technology is tried
ON 10 JANUARY, researchers in China pub- nies that also won Warp Speed funds, Glenn and true, scores of other companies are also
lished the genome sequence of the virus said on the morning of 24 September, the day racing to develop protein subunit vaccines.
ravaging the city of Wuhan. Three days Novavax launched its first phase III trial, of Novavax is the only one to have launched a
later, Gregory Glenn, president of R&D at 15,000 volunteers in the United Kingdom. phase III trial. Of the other firms, the huge
Novavax, asked his staff to order from a sup- vaccinemaker Sanofi Pasteur is likely No-
plier the gene for the virus’ spike protein. Most of Novavax’s key competitors— vavax’s biggest rival. It “is going to be formi-
Moderna, Pfizer, Johnson & Johnson sub- dable competition to the Novavax vaccine,”
Glenn and other Novavax scientists had sidiary Janssen, and AstraZeneca—had says Vijay Samant, a former head of vaccine
spent years developing “protein subunit” launched phase III trials by then. To make manufacturing at Merck and now a consul-
vaccines, so named because they employ a their vaccines, all four of those firms use tant to vaccine companies. (Novavax is not
protein (or part of one) from the targeted new technologies based on genetic material a client.) Sanofi Pasteur has deep pockets,
virus, plus an immune-boosting compound that directs protein production, rather than infrastructure, and experience, and markets
called an adjuvant, to provoke an immune delivering proteins directly. Those platforms vaccines against 19 infectious diseases.
response. The company hadn’t had a com- rely on DNA loaded in disabled viruses or on
mercial success—its vaccine against a seri- messenger RNA to carry genetic instructions But Novavax scientists say they’re ready
ous respiratory illness failed in clinical trials. for building the spike protein. Cells within for the competition. “We’ve been getting
But it had produced a promising flu vaccine a vaccinated person then churn out the pro- ready for this our whole lives,” says Gale
aimed at older adults, which was nearing tein, alerting the immune system. Smith, Novavax’s chief scientist.

650 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 sciencemag.org SCIENCE

Published by AAAS

ONCE THE PANDEMIC coronavirus gene 2000-liter bioreactors. The moth cells then A vital piece of good news came on
arrived in Gaithersburg, Maryland, on express the coronavirus spikes on their cell 24 March, boosting the company’s search
3 February, the company spent weeks mak- membranes. Scientists harvest the proteins for cash. The phase III clinical trial of
ing more than 20 versions of the spike and mix them with a delivery vehicle: syn- Novavax’s flu vaccine in older adults, also
protein, aiming for a product as immuno- thetic particles, on average 30 to 40 nano- made using the moth cell system, returned
logically potent as possible. The winner meters across. Each “nanoparticle” ends excellent results. For Novavax, which was
was the most stable antibody-inducing up studded with up to 14 spike proteins. now asking funders for major dollars for its
protein, one that mimicked the energy- The finished particles are only slightly pandemic coronavirus vaccine, the proof of
packed state of the spike just before it smaller than the coronavirus itself, help- its capabilities came at a fortuitous time.
fuses with the host cell membrane. ing the immune system “see” them as a
danger, Smith says. Then Novavax adds its Three days later, senior Novavax scien-
In March, a team led by Nita Patel, a adjuvant, based on saponin, a compound tists met with decision-makers from a key
senior director in the vaccine develop- found in soap bark trees that stimulates funder—the nonprofit, international Coali-
ment department (see sidebar, p. 652), the immune system (see graphic, below). tion for Epidemic Preparedness Innovations
confirmed in lab tests that the engineered (CEPI)—in a crucial Zoom call. Novavax scien-
protein bound tightly to its human cell-
surface receptor. The results strongly The heart of a new vaccine
suggested antibodies to Novavax’s protein
would interfere with the virus’ own spike To make their vaccine, Novavax scientists first used a baculovirus to insert the gene for the SARS-CoV-2
protein as it tried to fuse with cells. spike protein into moth cells, which produced the spikes on their cell membranes. Scientists then
harvested the spike proteins and mixed them with a synthetic soaplike particle in which the spikes embed.
Patel’s boss, Smith, next enlisted Ward A compound derived from trees serves as an immune-boosting adjuvant.
to verify the protein’s structure and stabil-
ity with electron microscopy. Other tests Moth 1 Baculovirus delivers spike protein DNA from coronavirus to fall armyworm moth cell.
showed the Novavax spike is stable for cell 2 Moth cell produces spike proteins.
many weeks at 2°C to 8°C—a key advan-
tage over the Moderna and Pfizer vaccines, Spike DNA
which need to be stored at –20°C and
–70°C, respectively, and once thawed, last 3 Spikes stud a synthetic particle.
only days in the refrigerator.
4 A saponin—a purified plant
Now, the challenge was to make the pro- compound—is added to boost
tein in the vast quantities that the world the immune response.
would need. Novavax had a system to do
that, co-invented by Smith decades earlier Saponin
and since used by the company to develop
its other vaccine candidates: moth cells. Antibody Coronavirus 5 Vaccination aims to trigger
production of antispike
As a 34-year-old graduate student at antibodies, blocking
Texas A&M University in 1983, Smith and SARS-CoV-2 infection.
colleagues had developed a system that
GRAPHIC: A. KITTERMAN AND V. ALTOUNIAN/SCIENCE could produce proteins in big quantities. To crank up production in the spring, tists were used to dealing with skeptics. “Most
The researchers started with an insect- Novavax had to cope with a harsh reality. people don’t think [our nanoparticles] work,”
infecting virus called a baculovirus, which “What we didn’t have—what we’d lost by Smith says. “We’ve been accused that [they]
had the virtue of a roomy genome that downsizing last year—is taking [the vac- aren’t even real, which is ridiculous.” Then
can accommodate large chunks of foreign cine] right over to a manufacturing facil- Ward’s new high-resolution images—show-
DNA. The researchers inserted a gene for ity,” Glenn says. “We could have been much ing tiny particles studded with spike proteins,
a human immune protein, interferon, into earlier had we had that strategic asset.” with honeycomblike saponins floating beside
the virus and then used it to infect cells Instead, the company “had to beg” he says, them—flashed on dozens of people’s screens.
from the caterpillar form of a pest called turning to Gaithersburg-based contract It was “one of those precious moments,” re-
the fall armyworm moth. The virus trans- manufacturer Emergent BioSolutions to calls Nick Jackson, CEPI’s head of vaccine
ferred the gene to the moth cells, which produce vaccine for the first human tri- programs. “The excitement was palpable.”
duly secreted human interferon. als. It was “not ideal,” Glenn says. “We’re
sprinters … [but] it’s hard to get someone Six weeks later, CEPI awarded Novavax
Back then, editors of major journals had else to sprint.” up to $384 million for trials and manufac-
little interest in the discovery and repeat- turing of its vaccine.
edly rejected Smith’s paper, which found a
home in an obscure new journal, Molecu-
lar and Cellular Biology. But today the sys-
tem is widely used in biotechnology. Now,
it is at work producing the Novavax vac-
cine at a plant owned by a contractor in
Morrisville, North Carolina, and soon, it’s
expected, at other plants owned or con-
tracted by Novavax in Europe, the United
States, and Asia.

In North Carolina, countless baculoviruses
loaded with the gene for the coronavirus
spike protein are invading moth cells in

SCIENCE sciencemag.org 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 651

Published by AAAS

NEWS | FEATURES

‘Nothing is impossible,’ says lab ace Nita Patel Ward’s work won over some scientific PHOTO: ALYSSA SCHUKAR
doubters. John Moore, an immunologist at
S tanding in front of reporters recently after showing Maryland Governor Larry Weill Cornell Medicine, had been skepti-
Hogan (R) through the company’s Gaithersburg, Maryland, labs, Novavax CEO cal of Novavax’s moth cell system because
Stanley Erck touted everything from the company’s manufacturing plans to the in the 1990s it had conspicuously failed
long hours its scientists are logging. But he praised only one staffer by name: Nita to produce an HIV spike protein with the
Patel, a diminutive 56-year-old wearing jeans and a black mask. “Nita,” Erck said right characteristics to make an AIDS vac-
to the governor, “has done all the work that you saw today.” cine. But in August, when Ward’s work
was posted as a preprint, “I looked at that
Patel is a senior director in the vaccine development program at Novavax, a small paper and was impressed,” Moore says. “It
firm among giant pharma companies racing to test a vaccine for the pandemic corona- changed my perception of the quality of
virus (see main story, p. 649). Her all-female crew is an essential part of Novavax’s lab the protein. The concerns I had were elimi-
team. Their sophisticated tests verified that the heart of the company’s vaccine—its nated by data, which is as it should be.”
version of the virus’ spike protein—performed as it should in cells and generated virus-
neutralizing antibodies in animals. “Nita is absolutely invaluable,” says her boss, chief By late May, Novavax had launched its
scientist Gale Smith. “She’s a genius.” first human safety trial in 131 volunteers in
Australia and used the CEPI funding to buy,
Patel has come a long way from her beginnings in Sojitra, a farming village in India’s for $167 million in cash, a state-of-the-art
Gujarat state. There, when she was 4 years old, her family fell into poverty after her vaccine manufacturing facility in the Czech
father nearly died from tuberculosis (TB). He never worked again and told Patel she Republic that the company said would de-
should become a doctor and find a cure. liver more than 1 billion doses in 2021. And
in early July, Operation Warp Speed granted
Patel set about doing that, wearing the same ragged dress to school day after day. the company up to $1.6 billion, with
She had no shoes. She begged bus fare $800 million available immediately, for a
from a neighbor—at whose house she also phase III clinical trial and for manufactur-
devoured the newspaper because her family ing 100 million doses of vaccine.
couldn’t afford a subscription.
Her academic excellence propelled her IN EARLY AUGUST, the big investors in the
through college on government scholar- tiny company won an initial vindication
ships. She later picked up two master’s when Novavax announced strong results
degrees, in India and the United States, in from the Australian trial. After two injec-
applied microbiology and biotechnology. tions, “the antibody responses in the No-
Her memory is photographic: When driving, vavax paper were markedly stronger than
she has to be careful not to look at license any of the other vaccines that have been re-
plate numbers, or she’ll memorize them. ported,” and participants had experienced
Patel married a U.S. biochemist and then no severe adverse events, says Moore, who
moved to Gaithersburg and started job recently published a Journal of Virology
hunting. One small company offered her review of the leading vaccine candidates.
less than others—but she would work on a Moore says he intends to volunteer for a
TB project. In 1990, Patel became the 16th Novavax trial if eligible. “I’m going, ‘Yes, I’ll
employee at MedImmune. One of her bosses have that [vaccine].’”
there, Herren Wu, now a senior vice presi-
dent at AstraZeneca, remembers her skill The government of the United Kingdom
with a difficult assay that bedeviled others. soon signed up to buy 60 million doses
“She was the one [whose data] I believed,” of Novavax’s vaccine, and the big drug-
he says. “She’s a very good bench scientist.” maker Takeda licensed it to manufacture
But Patel also understands setbacks: A at scale with funding from the Japanese
government. Other scientists noted strong
MedImmune Lyme disease vaccine failed in its first clinical trial, and another therapy, results in a dozen monkeys injected with
against respiratory syncytial virus (RSV), was rejected by the Food and Drug Adminis- various doses of Novavax’s vaccine and
tration. In 2015, attracted by Novavax’s RSV vaccine work, she jumped to the firm. then infected with live coronavirus. The
virus failed entirely to multiply in the ani-
After Novavax got the gene for the SARS-CoV-2 spike protein in February, Patel’s mals’ noses and replicated in the lungs of
team tested more than 20 engineered variants of the protein, identifying the version just one monkey that received the lowest
most likely to elicit a protective immune response. Now, she’s characterizing details of dose; that animal shut down the infection
that protein, identifying the precise locations where neutralizing antibodies vigorously after 4 days.
bind to it, and creating a test to ensure the spike is consistent from one manufacturing
plant to another. “It’s the only vaccine I’ve seen out of all
the candidates that are further down the
Since the pandemic arrived, she says, “my day just doesn’t end. And it’s the same pipeline that actually had no viral replica-
with everyone else here.” Yet Patel, who prays and meditates daily at a temple in her tion in the nasal swabs of vaccinated ani-
home, projects serenity and good cheer. “To me, nothing is impossible. So, having that mals,” says Angela Rasmussen, a virologist
mindset, nothing stresses me out, being honest.” at Columbia University. That’s important,
she says, because stopping viral replica-
Scientist Sonia Maciejewski, who works for Patel, agrees. “She has a very strong tion in the nose can reduce the spread of
work ethic … yet somehow doesn’t put that sort of pressure or stress on us.” infection among people who may be un-
aware they are sick. But she cautions that
Patel’s serenity gets a boost because she doesn’t see the firm as competing with
others. “We are [all] working towards, together, the world’s problem,” she says. —M.W. sciencemag.org SCIENCE

652 6 NOVEMBER 2020 • VOL 370 ISSUE 6517

Published by AAAS

monkeys are not people. “We can’t really transparency as to how the funding deci- Novavax and two board members had pock-

conclude that this vaccine is going to be bet- sions of Warp Speed were made.” (Journal- eted nearly $17 million in August alone.

ter in practice until we have some reliable ists and investors have tried unsuccessfully Maris notes that executives who are bull-

safety and efficacy data in people.” to obtain Novavax’s Warp Speed contract.) ish on their own companies tend to keep

That’s why researchers will be eager to “I would like to see the fundamental or deep their stock. “So it’s interesting that they de-

see results from Novavax’s phase III tri- analysis, if any, done prior to these fund- cided to sell.”

als. In the one in progress in the United ing decisions,” Maris says. “I’m not certain Novavax leaders continued their sales in

Kingdom, volunteers get either placebo or whether it exists.” September, with four senior managers sell-

vaccine in two injections, 21 days apart. Novavax says it will release the contract ing shares worth a combined $18.9 million.

Researchers will evaluate whether vacci- next week as part of its quarterly financial “Pretty much all my value I have is in Novavax,”

nated volunteers have fewer symptomatic reporting. says Glenn, who pocketed $6.2 million (be-

coronavirus infections than placebo recip- Other critics noted that since the pan- fore taxes) in August and sold shares worth

ients. They’ll also keep monitoring safety, demic began, Novavax top managers have $4.9 million in September. “A year ago it was

including any reactions to the adjuvant, made tens of millions of dollars by exercis- worth nothing.” CEO Stanley Erck, who sold

because this will be the first time huge ing options to buy their company’s stock at $4.5 million in stock in September, did not

numbers of younger people with vigor- earlier, lower prices and sell it at this year’s respond to requests for comment.

ous immune systems receive it. Even if Novavax’s phase III

Vaccine trials need volun- trials succeed, vaccine watch-

teers who are exposed to the Healthier prospects ers say the company’s biggest
virus, so skyrocketing infec- vulnerability will remain: the
tions in the United Kingdom In early 2019, Novavax’s share price fell so low that NASDAQ threatened to delist manufacturing process. “I think
are likely working in Novavax’s the company. Its candidate coronavirus vaccine has turned the small firm’s the vaccine is going to be effi-
favor. The company estimates fortunes around, although its stock lost value in the fall. cacious,” Samant says. “But you

there will be enough infections 160 put that 2 billion–dose task in

among participants to allow a 120 6 front of a small company, it’s a
first look at the data early in huge uphill task.”
2021—and says it expects the $ per share
7 Ward concurs. “It’s like

U.K. data will be enough to 80 58 trying to cook a really good
drive approval of its vaccine. 9 quiche. You can make one for

In the United States and Mex- 40 4 your family, but if you try to
ico, the company aims to enroll make 50 of them for a wed-
30,000 volunteers—about 90% ding, that’s actually very diffi-

CREDITS: (GRAPHIC) A. KITTERMAN/SCIENCE; (DATA) NASDAQ VIA YAHOO! FINANCE of them in the United States—in 01 23 2021 cult to do, to get them all the
a trial expected to launch this same and equivalent.”
month. Keeping volunteers in June 2019 2020 7 4 August
that trial may be challenging if Novavax delivers “The [moth cell system] is
other vaccine contenders win 1 27 June 2019 4 11 May positive data not like the flu vaccine and
U.S. marketing approval in com- Novavax sells Novavax wins up to from a phase I and eggs,” adds vaccine expert and
ing weeks (Science, 23 October, its two Maryland $384 million from the II trial of its FDA veteran Luciana Borio,
p. 389). But Glenn argues that manufacturing Coalition for Epidemic COVID-19 vaccine. an admirer of Novavax who is
this scenario is “not very realis- facilities. Preparedness Innovations. a vice president at In-Q-Tel, a
tic” given the time required for 8 24 September technology investment firm.
U.S. Food and Drug Adminis- 2 3 February 5 4 June Novavax launches “It’s untested.”
tration (FDA) action and wide- Novavax begins The U.S. Department of a phase III trial in
spread distribution of a vaccine. to develop its Defense pledges $60 million the United Kingdom. Novavax counters that the
COVID-19 vaccine. for U.S. manufacturing company’s manufacturing part-
Observers also note that more of Novavax’s vaccine. 9 30 October ners are deeply experienced in
than one vaccine will prob- 3 24 March Novavax delays making vaccines at scale. For in-
ably be needed to quell the Novavax’s flu 6 7 July launch of phase III stance, the Serum Institute of In-
pandemic. The first round of vaccine succeeds Novavax lands up trial in North America dia, a veteran vaccinemaker that
vaccine doses promised by Pfizer in a phase III to $1.6 billion in until November. is the world’s largest, is helping
trial in older adults. U.S. Operation Warp Novavax expand production at
Speed funding.

and Moderna combined would only cover high prices. Such options are a common the 14,000-square-meter Czech facility, plus

100 million people. Experts add that the first way to pay biotech executives, but against manufacturing an additional billion doses

vaccine approved won’t necessarily be the best. the background of a pandemic, the sales led itself, in India, for low- and middle-income

“Especially when we are talking about vacci- to an unwelcome spotlight on Capitol Hill countries. That brings the total doses the

nating millions of people, you have just got in September. At a hearing, the chair of the company now says it can manufacture in

to follow the science,” says Mayank Mamtani, House of Representatives Financial Services 2021 to 2 billion, the promised number.

a senior biotechnology analyst at B. Riley Subcommittee on Investor Protection, En- The fact that world-class manufacturers

Securities. In the long run, “being first to trepreneurship, and Capital Markets raised such as the Serum Institute “didn’t even

market is just not, in my opinion, important.” the examples of Novavax and other com- blink before wanting to work with them

panies by name. And in a stinging memo and helping them scale up” speaks highly of

SOME OBSERVERS RAISED their eyebrows that Democratic lawmakers issued under the company, Mamtani says.

when Novavax won Warp Speed funding, the heading “Corporate Integrity and Profi- “It’s going to be a dark horse,” he pre-

given that the firm was on life support last teering in the COVID-19 Pandemic,” they dicts. “A dark horse helping us to get out of

year. Maris bemoans the “complete lack of reported that three senior executives at this darkness.” j

SCIENCE sciencemag.org 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 653

Published by AAAS

INSIGHTS

PERSPECTIVES

Ballistic tongue representation
of Yaksha perettii is shown.

The albanerpetontid is dwelling in
the understory of the forest,

and is illustrated an instant before
being trapped by tree resin.

PA L E O N T O L O GY

A surprising fossil vertebrate

An ancient amphibian converged on a chameleon-like way of feeding

By David B. Wake Many had bizarre shapes, and they also var- troduce an unusual fossil of the obscure and ILLUSTRATION: STEPHANIE ABRAMOWICZ
ied greatly in size. Among them were the apparently extinct albanerpetontids.
T he invasion of land by vertebrates ancestors of the still-living salamanders,
initiated an explosion of new kinds frogs, and caecilians, collectively known as First detected in Late Cretaceous (100 to
of organisms—amphibians—whose lissamphibians. By the dawn of the Mesozoic 66 Ma) formations and recorded as sala-
diversity ballooned until the extinc- Era, which followed the Paleozoic, only liss- manders, albanerpetontids gradually be-
tion event that ended the Paleozoic amphibians and one other group (tremato- came recognized by paleontologists as a
Era 252 million years ago (Ma) nearly saurs) survived. The last trematosaurs dis- fourth kind of lissamphibian, albanerpeton-
wiped them out. Several early amphibians appeared in the late Mesozoic, 120 Ma. But
became specialized in morphology and life paleontologists had overlooked one clade. Museum of Vertebrate Zoology and Department of
history, even including forms that lost limbs. On page 687 of this issue, Daza et al. (1) in- Integrative Biology, University of California, Berkeley, CA
94720, USA. Email: [email protected]

654 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 sciencemag.org SCIENCE

Published by AAAS

tids (Order Allocaudata). With the discov- permanently aquatic forms with gills and a EVOLUTIONARY BIOLOGY
ery of several new taxa, albanerpetontids keratinous beak. Aggressively predaceous
(named for the Albian, a mid-Cretaceous amphiumas are large, very elongate aquatic The genetic law
age and stage, 100 to 113 Ma) became bet- forms lacking gills. They have ludicrously of the minimum
ter known. They were salamander-like, or small limbs and reduced digits—down to
maybe lizard-like, biologically, and per- one in one species. Asian giant salamanders The genetic code evolved
sisted for a very long time, first appearing reach 180 cm in length and weigh over 50 to reduce the impact
in the Triassic (252 to 201 Ma) and only dis- kg. By contrast, frogs, the most numerous of nutrient limitations
appearing “yesterday” (they were living in (88% of lissamphibians) and widespread liv-
Italy with other still-surviving amphibians ing amphibians, are tailless, short-bodied, By Martin F. Polz1 and Otto X. Cordero2
until the Early Pleistocene, about 2 Ma). usually large-headed, and have limbs of of-
With luck we might still have them some- ten very unequal length. Caecilians are vir- H ow organisms are optimized in the
where (hopefully, one will turn up in what tually blind, limbless, nearly tailless but very face of environmental challenges
remains of biological wilderness on this long-bodied burrowers, except for a bizarre remains one of the key unanswered
planet—but time is running out). There is clade of aquatic species in South American questions in biology. The optimiza-
now a much better idea of the kind of or- rivers and swamps. tion of enzymes for changing nutri-
ganism we seek, thanks to the report by ent concentrations in an organism’s
Daza et al. of their spectacular discovery of Now, enter the albanerpetontids. Super- environment is well known (1). However,
a new albanerpetontid, Yaksha perettii, en- ficially salamander-like in their prototypi- intricate genomics studies have revealed
cased in Myanmar amber (1). cal tetrapod habitus, albanerpetontids had that optimization might affect the ar-
features that seemed to suggest a burrow- chitecture of the entire genome (2). On
The Myanmar amber, in this case about ing way of life, with a strange, strengthened page 683 of this issue, Shenhav and Zeevi
99 million years old, preserves some spec- lower jaw with an interlocking articulation, (3) illuminate how selection driven by
tacular fossils. In 2016, Daza’s team (2) a strengthened skull with solid bones cov- resource scarcity can affect the evolution
reported amazingly well-preserved verte- ered with stout scales and elaborate bony of nucleotide and protein sequences in ma-
brates, including one thought to be the ear- sculpturing suggesting co-ossification of rine microbes.
liest chameleon. The basis for that identi- bone and skin, and with limbs bearing
fication was a long skeletal element in the claws on their digits (four front, five hind). In extremely nutrient-scarce regions of
head and throat, an entoglossal, found only But what about the tongue? And how could the ocean, microbial genomes are often
in chameleons and the key component in its these animals have been captured in amber small and streamlined, containing only
intricate ballistic tongue. The very elongated sap? Were they arboreal (see the figure)? the most essential genetic information
entoglossal plays a special role in tongue fir- The closest analogs may be the strange trop- (4). However, the essential selective factor
ing in chameleons. It is enveloped by spe- ical plethodontid salamanders of the genus often is not the absolute concentration of
cialized accelerator muscles, which wrap Oedipina, a group of highly specialized bur- a single nutrient but rather its ratio with
around it. At the anterior end is the massive rowers, which—such as O. alleni—occasion- other required nutrients (5). For example,
fleshy tongue pad. The entoglossal of cha- ally become arboreal. Their exquisitely spe- the sunlit ocean surface is typically lim-
meleons slightly tapers toward the front, so cialized ballistic tongue is as if designed in ited in nitrogen but not organic carbon,
when the accelerators squeeze down on it reverse to that of chameleons—the homolog because photosynthetic organisms require
the tongue pad is swiftly advanced and slips of the entoglossal (the basibranchial) is it- much of the former but produce copious
forward off its end, literally flung into space self, together with the tongue pad, projected amounts of the latter. When biomass from
(3). No other taxon was thought to have completely out of the mouth (4). this surface layer dies and sinks, it is de-
such an extreme entoglossal. Hence, the graded by heterotrophic bacteria, which,
initial identification seemed to make sense. The elongated entoglossal is a vivid exam- because of the stoichiometry of elements
Logical—but spectacularly wrong. Daza et ple of evolutionary convergence, which justi- in their food versus their cells, shift the
al. now show that not only are the bearers fiably continues to receive intense scientific balance toward carbon limitation (6, 7).
of the specialized tongue not chameleons, or scrutiny (5, 6), because it is common and
even squamates; they instead are members profoundly important. The expanded liss- Recent work has shown that this tran-
of the mysterious albanerpetontids. What amphibians display different levels of con- sition from nitrogen to carbon limitation
strange lissamphibians these albanerpe- vergence, including what might be termed provides an explanation for an abrupt shift
tontids are: They have claws, scales, and ar- complete convergence between Yaksha and in the guanine-cytosine (GC) content in the
mored skulls—and at least one had a tongue chameleons, which entails both structural genomes of marine microbes at the ocean
like a modern chameleon. and functional components, and incomplete surface versus those in the deep ocean (8,
convergence between Yaksha and plethod- 9). Organisms living under consistent ni-
How the lissamphibians are related to ontids like Oedipina, a convergence that is trogen limitation have a low GC content in
each other and to Paleozoic forms is closely functional but only partially structural. j their genomes, leading to a lower nitrogen
studied and contentious, but salamanders demand for DNA synthesis. These orga-
and frogs are likely sister taxa (Batrachia), REFERENCES AND NOTES
caecilians are mysterious but might be de- 1Centre for Microbiology and Environmental Systems
rived from stereospondyls, and albanerpe- 1. J. D. Daza et al., Science 370, 687 (2020). Science, University of Vienna, Vienna, Austria. 2Department
tontids seem likely to be basal derivatives. 2. J. D. Daza et al., Sci.Adv. 2, e1501080 (2016). of Civil and Environmental Engineering, Massachusetts
3. D. E. Moulton,T. Lessinnes, S. O’Keeffe, L. Dorfmann, Institute of Technology, Cambridge, MA 02139, USA. Email:
Although many salamanders are almost [email protected]; [email protected]
prototypical tetrapods, with four limbs of A. Goriely, Proc. R. Soc.A Math. Phys. Eng. Sci. 472,
roughly equivalent length, a generally long 20160030 (2016).
tail, and roughly proportional head and 4. S. M. Deban et al., Proc. Natl.Acad. Sci. U.S.A. 117, 10445
body, there are also some bizarre exceptions. (2020).
Sirens lack hind limbs and are very elongate, 5. D. B.Wake, M. H.Wake, C. D. Specht, Science 331, 1032
(2011).
6. J. B. Losos, Evolution 65, 1827 (2011).

10.1126/science.abe7826

SCIENCE sciencemag.org 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 655

Published by AAAS

INSIGHTS | PERSPECTIVES

nisms also use codons that favor Resource use is hardwired in the genome mutation. It would therefore be
a proteome with a comparatively illuminating to model the effects
low nitrogen and high carbon Optimal resource use has been a selective evolutionary force since before that such mutations might have
the last common ancestor (LCA) diversified into modern life (top). The

content (10, 11). genetic code evolved to afford marine microbes the ability to adaptively on cell physiology and long-term

Using a large set of metage- minimize nitrogen (N) or carbon (C) content in their biomass, depending on fitness. For example, scientists

nomic and single-cell genome the nutrient availability in the environment (bottom, ocean). could develop experimental

data from across the global ocean, models of competition experi-

Shenhav and Zeevi show that ments under nitrogen limitation

natural selection purged nucleo- Time to determine whether fitness

tide and amino acid changes that effects are actually measurable

increase the demand for limiting LCA (perhaps as a result of unantici-
resources. Selection was stronger N pated pleiotropy). Such experi-
at the protein versus DNA level, Ancient C ments could give researchers a
which is consistent with the high environment
better grasp of the magnitude

protein-to-DNA ratio in microbial Selection of the relative fitness advantage
cells. Highly expressed and se- experienced by the mutant or-

creted proteins showed the stron- High N DNA High C ganisms and the evolutionary
gest signal for resource-driven Low C proteome Low N dynamics that led to the patterns
selection because they place a optimization discovered by the authors.

high resource demand on the The study by Shenhav and

cell. Among the measured envi- Zeevi reveals a fundamental se-

ronmental variables, nitrate con- Depth Modern ocean Photic lective force that has affected all
centration—the prevailing form zone forms of cellular life dating back

of nitrogen at the ocean surface High C to their last common ancestor
(6)—was most strongly associated Low N and that seems to still be acting
with the selection of protein se- today on marine microbes. This

quences. Furthermore, mutations High N Aphotic work opens many new avenues
leading to lower nitrogen incorpo- Low C zone of inquiry—for example, whether
ration were inversely associated similar patterns of evolution are

with mutations leading to lower observed in other environments,

carbon demand. This finding re- such as soils or animal guts;

flects the inverse relationship of whether mutational patterns of

carbon and nitrogen limitation “amino acid choice” can be used

as a function of water-column to infer resource limitations from

depth. The new insight that carbon limi- the impact of random mutations on car- metagenomic data; and whether purifying

tation might also select for lower carbon bon and nitrogen demand. Thus, the code selection acts one amino acid at a time or

incorporation led the authors to link these seems to have evolved to minimize the po- whether other pleiotropic effects are re-

observations to the nature of the genetic tential damage of random mutations, both quired to explain the evolution of resource-

code, which appeared to be simultaneously in terms of mistranslations and inefficient driven codon selection in microbes. j

optimized for conservation of nitrogen and resource use. This new insight indicates REFERENCES AND NOTES
carbon. These findings strengthen the hy- that differential limitation by carbon and
pothesis that the microbial genome evolved nitrogen constrained the evolution of the 1. B.V.Adkar et al., Nat. Ecol. Evol. 1, 149 (2017).
to enable nutrient conservation in low-ni- most primordial forms of life when the 2. P. Baudouin-Cornu,Y. Surdin-Kerjan, P. Marlière, D.
trogen and low-carbon environments. universal genetic code evolved.
Thomas, Science 293, 297 (2001).
Although variations of the standard The findings of Shenhav and Zeevi point 3. L. Shenhav, D.Zeevi, Science 370, 683 (2020).
genetic code (for example, in mamma- to an incredible fine-tuning of genomes 4. S.J. Giovannoni,J. C.Thrash, B.Temperton, ISME J. 8,
lian mitochondria or mycoplasma) show toward nutrient availability where selec-
that the code itself can evolve, the vari- tion acts on individual codons. However, 1553 (2014).
5. K. R.Arrigo, Nature 437, 349 (2005).
6. C. E. Moore et al., Nat. Geosci. 6, 701 (2013).
7. E. R. M. Druffel, S. Griffin,A. I. Coppola, B. D.Walker,

ants are minor and derived from the stan- whereas single mutations that affect the Geophys. Res. Lett. 43, 5279 (2016).
dard code shared by all life-forms. Thus, performance or regulation of proteins can 8. J.J. Grzymski,A. M. Dussaq, ISME J. 6, 71 (2012).
the basic structure of the code, with its have large fitness effects, the fitness gain 9. D. R. Mende et al., Nat. Microbiol. 2, 1367 (2017).
characteristic amino acid assignments, is of an individual-codon mutation in a pro- 10. J. G. Bragg, C. L. Hyder, Proc. R. Soc. London Ser. B 271,

S374 (2004).

believed to be ancestral to all extant cel- tein that optimizes resource use must be 11. P. Baudouin-Cornu, K. Schuerer, P. Marlière, D.Thomas,
lular life-forms. Multiple (non–mutually vanishingly small. Using, as a reference, J. Biol. Chem. 279, 5421 (2004).
exclusive) theories have been proposed to the composition of Escherichia coli, a cell
explain how the code originated (12). One with a single nitrogen-saving codon muta- 12. E.V. Koonin,A. S. Novozhilov, IUBMB Life 61, 99 (2009).
13. C. R.Woese, Proc. Natl.Acad. Sci. U.S.A. 54, 1546 (1965).
14. R. Phillips, R. Milo, Proc. Natl.Acad. Sci. U.S.A. 106, 21465 GRAPHIC: KELLIE HOLOSKI/SCIENCE

of these—the adaptive theory—postulates tion in a highly expressed protein (present (2009).

that the genetic code evolved to maximize at 104 copies per cell), would experience a ACKNOWLEDGMENTS
mutational robustness (that is, to lower the change in nitrogen demand on the order
chance that random mutations lead to del- of only ~0.001%, assuming ~109 nitrogen M.F.P. is funded by the Simons Foundation (LIFE ID 572792)
eterious effects caused by translation er- atoms per cell (14). and the U.S. National Science Foundation Dimensions
rors) (13). The results of Shenhav and Zeevi Program (NSF 1831730). O.X.C. is funded by the Simons
add to this theory by showing that the code With these numbers in mind, it seems Collaboration on Principles of Microbial Ecosystems, award
hard to imagine a fitness advantage large number 542395.

is also robust in the sense that it minimizes enough to cause the spread of an adaptive 10.1126/science.abf2588

656 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 sciencemag.org SCIENCE

Published by AAAS

GENETICS

Regulation in common: Sponge to zebrafish

Developmental enhancers from a sponge regulate gene expression in zebrafish neurons

By Nathan Harmston1,2 are structured and evolve, and how gene parable in terms of their constituent TFBSs
regulatory networks are reused and co-opted. (8). Together, these examples highlight that
D uring the development of multicel- selection pressure on the output of some en-
lular animals, distal gene regulatory A large number of enhancers appear to be hancers drives the conservation of enhancer
sequences called enhancers are in- species-specific (5); however, there are a sub- sequence, whereas for other enhancers, se-
volved in determining when, where, set of enhancers that are conserved between quence conservation does not appear to mat-
and how much a gene is expressed (1). evolutionary distant species. Comparing ter, and despite major differences in their
Enhancers contain transcription fac- the genomes of different species within the organization, such enhancers are capable of
tor binding sites (TFBSs), and the combina- same phyla has identified elements that show generating the same output. Intriguingly, the
tion of TFs bound determines the activity of high noncoding conservation and which act set of enhancers identified by Wong et al.,
an enhancer. There is a lack of understand- as enhancers to regulate the expression of though not conserved at the sequence level,
ing about how an enhancer sequence inter- key developmental transcription factors (3). can drive expression of their corresponding
prets regulatory state (input) to drive target Mutations affecting these elements have been target gene in patterns similar to those of
gene expression (output), and how these found to have substantial effects on pheno-
sequences are constrained and/or modified
over time. On page 681 of this issue, Wong et Conserved enhancers
al. (2) identify a series of enhancers in a ma-
rine sponge (Amphimedon queenslandica) Injection of the entire Scaper-Islet locus of a marine sponge (Amphimedon queenslandica) into zebrafish
that respond to TFs expressed during zebra- (Danio rerio) embryos reveals that eISL (dark blue circle), a developmental enhancer located within an
fish (Danio rerio) development. Given the intron of Scaper, can drive Islet expression in zebrafish neurons. The eISL-driven gene expression patterns
large evolutionary distance between zebra- overlap with that of zebrafish orthologs of Islet.
fish and sponge (their common ancestor ex-
isted more than 700 million years ago), these eISL enhancer
enhancers lack detectable sequence homol-
ogy with vertebrate genomes, yet their ability Scaper exons Islet exons
to function as enhancers in zebrafish demon-
strates some kind of functional conservation A. queenslandica
without sequence conservation.
D. rerio
Throughout Metazoa, numerous pairs of
genes have been identified that are conserved A. queenslandica
together, a phenomenon known as micro-
synteny, thought to arise primarily from cis- D. rerio
regulatory constraints (3, 4). By investigating
gene pairs conserved across Metazoa, Wong D. rerio Islet enhancer Islet ortholog
et al. identified and tested a set of enhancers
GRAPHIC: A. KITTERMAN/SCIENCE present within the intron of one member of a types and in many cases are associated with their orthologs, but do not regulate expres-
pair (the bystander gene), whose function is developmental disorders (6). Therefore, small sion in comparable cell types.
to regulate the expression of the other gene changes in enhancer sequence can have large
(the target gene) in the pair. Insertion of the effects on function and phenotype. Multiple models have been proposed for
sponge Islet-Scaper gene pair into zebrafish how enhancers are structured in terms of
embryos revealed that eISL, an enhancer lo- However, between closely related the ordering and positioning of their TFBSs
cated in the intron of Scaper, drove the ex- Drosophila (fruitfly) species, the content, and the effect this has on the co-operative or
pression of Islet in neuronal cells, similar to ordering, and positioning of TFBSs (its cis- additive binding of TFs to them. These range
the expression patterns of the zebrafish para- regulatory grammar) within the eve stripe 2 from the enhanceosome model, which re-
logs of Islet. Intriguingly, eISL could drive enhancer are different, yet all of the configu- quires the precise positioning of TFBSs (9),
Islet expression in neurons, a cell type not rations lead to the same phenotype, indicat- to the billboard model, where the order and
present in sponges (see the figure). Therefore, ing functional conservation despite a lack of positioning of TFBSs are not important (10),
this enhancer is responding to the set of TFs sequence conservation (7). A brain enhancer with the TF collective model allowing for co-
expressed in zebrafish neurons and driving that is functionally conserved between chor- operativity between TFs despite the lack of
expression of Islet. These findings are impor- dates and hemichordates has been identified. a well-defined grammar (11). Each of these
tant for understanding both how enhancers This enhancer can regulate the expression models of enhancer organization implies dis-
of sonic hedgehog (Shh) or hedgehog (hh) tinct constraints on how enhancers evolve.
1Science Division, Yale-NUS College, 16 College Avenue genes during brain development in mouse Wong et al. used the set of TFBSs identified in
West #01-220, 138527, Singapore. 2Programme in Cancer and acorn worm, respectively. Despite be- eISL to search for similar sequences in other
and Stem Cell Biology, Duke-NUS Medical School, 169857, ing distinct at the level of their overall DNA genomes and identified sequences in human,
Singapore. Email: [email protected] sequence, these brain enhancers are com- mouse, zebrafish, and fruitfly that had a simi-

SCIENCE sciencemag.org 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 657

Published by AAAS

INSIGHTS | PERSPECTIVES

lar TFBS content and were active in neuronal SCIENCE AND LAW
cell types. Although there was no apparent
conservation between the entire sequences of Nudging people to court
eISL and these enhancers, short, conserved
blocks of TFBSs were identified between Behavioral interventions may improve court attendance,
them, indicative of a TF collective–like model but how to reform the system remains unclear
for this enhancer. This indicates the existence
of a common cis-regulatory grammar that is By Issa Kohler-Hausmann topics interesting, yet difficult, is that ob-
used across multiple lineages to regulate de-
velopmental gene expression in specific cell served behavioral propensities are usually
types, and furthermore suggests the presence
of a regulatory state that has been reused or N ew York City issues hundreds of compatible with multiple psychological ex-
co-opted throughout evolution. thousands of summonses and mis- planations [e.g., (6)].
demeanor arrests each year, highly
Together, these results indicate that there concentrated in the city’s poorer and Although the evidence that the “nudge”
is a complex relationship between the struc- minority communities (1, 2). On page treatments produce causal effects seems
ture and function of an enhancer and the fairly straightforward, the authors’ preferred
gene regulatory networks that it is a part
of, with each imposing constraints on the 682 of this issue, Fishbane et al. (3) explanation of the effect is less clear. What
other (12, 13). The mismatch between their
sequence and functional conservation raises report that about 40% of the summonses the authors present as opposing hypotheses
questions about how to define when two en-
hancers are identical. In cases where there is (issued usually for infractions or violations do not seem to be mutually exclusive. The
a clear evolutionary history and similar func-
tion, it seems obvious that these enhancers that are classified below misdemeanors) is- hypothesis the authors seem interested in
are the same. But what if parts or the whole
of an enhancer have turned over, resulting in sued in New York City in 2015 resulted in refuting—that the high FTA rate for sum-
a lack of observable sequence homology but
still having the same function–is this still the a failure to appear (“FTA”) in court, which monses is explained by defendants “deciding
same enhancer? Moreover, what techniques
can be used to identify and characterize (usually) results in an arrest warrant and to skip court”—might capture many mental
them? The eISL enhancer is not a true func-
tional equivalent of the zebrafish enhancer, a host of collateral consequences (4, 5). To states. One such mental state might be “To
yet it is capable of driving overlapping pat-
terns of gene expression. A critical question increase the likelihood that a person issued hell with criminal court,” where someone is
in understanding enhancer evolution is what
causes some enhancers to require high se- a summons shows up to the mandatory aware of the specifics of their court obliga-
quence conservation to ensure conserved ac-
tivity, whereas for others this does not matter court date, Fishbane et al. tions and would be intent on
(14)? Only through a combination of experi-
mental and computational techniques is it experimented with a num- “…they are not noncompliance irrespective
possible to begin to systematically dissect the ber of different behavioral excused on the of more information about
complex interplay of features affecting en- “nudges,” such as summons same terms many how to comply or the conse-
hancer evolution to begin to fully understand form redesign and texting quences of failure. Another
the cis-regulatory grammar (15). j different types of reminders might be “I can’t afford to go

REFERENCES AND NOTES to defendants. They found of us frequently to court today,” where some-
1. I. Miguel-Escalada et al., Curr. Opin. Genet. Dev. 33, 71 that all of these interven- one is aware of the specifics
(2015).
2. E.Wong et al., Science 370, eaax8137 (2020). tions decreased the FTA rate. invoke: We are of their court date, but does
3. P. G. Engström et al., Genome Res. 17, 1898 (2007). It would be a positive step if busy ...overtaxed not attend because they made
4. M. Irimia et al., Genome Res. 22, 2356 (2012). other jurisdictions adopted a rational calculation that the
5. D.Villar et al., Cell 160, 554 (2015).
6. L.A. Lettice et al., Hum. Mol. Genet. 12, 1725 (2003). these reforms. However, if ... emotionally benefits of nonappearance
7. E. E. Hare et al., PLOS Genet. 4, e1000106 (2008). the authors are correct that outweigh the costs (e.g., the
8. Y.Yao et al., Nat. Genet. 48, 575 (2016).
9. D. Panne, Curr. Opin. Struct. Biol. 18, 236 (2008). their study shows that FTAs overwhelmed.” opportunity costs of compet-
are not exclusively caused by ing obligations to work or
10. M. M. Kulkarni, D. N.Arnosti, Development 130, 6569
(2003). “choosing” not to appear in child care).

11. G.Junion et al., Cell 148, 473 (2012). court, what role will that have in efforts to But one can “choose” not to attend court
12. J. L. Royo et al., Proc. Natl.Acad. Sci. U.S.A. 108, 14186
reform our massive and punitive criminal even while being unaware of the specif-
(2011).
13. P. Khoueiry et al., eLife 6, e28440 (2017). legal system? ics of the obligation simply by “choosing”
14. N. Harmston et al., Philos.Trans. Royal Soc. B Biol. Sci.
Predicting behavior is distinct from un- not to look at the information. Versions of
368, 20130021 (2013).
15. T. Fuqua et al., Nature 10.1038/s41586-020-2816-5 derstanding motives. Fishbane et al. sug- this could include: “I realize this summons

(2020). gest that the research design can adjudicate means I am supposed to go to court at some

ACKNOWLEDGMENTS between two different motives for identical time, somewhere. But I feel hopeless and

Thanks to E. Chua for her constructive comments. behavior: contempt for one’s legal obliga- disillusioned from repeated injustice in the

10.1126/science.abe9317 tions versus lack of knowledge about one’s criminal legal system and I am tuned out,”

legal obligations. This may be a mere fram- or “I am overwhelmed and busy trying to

ing device for the authors’ true interest— manage so many life obligations with so few

perhaps simply establishing the existence resources, I never got around to this one.”

of a treatment effect and estimating its From my years studying and working in

magnitude. But behavioral economics infre- New York City’s criminal courts, these seem

quently so limits its explanatory ambitions. especially plausible. But these do not seem

Rather, it aspires to illuminate underlying conceptually exclusive of the authors’ pre-

causal mechanisms by reference to general ferred hypothesis: “insufficient awareness”

psychological principles. What makes such of legal obligations.

What I find more interesting, as a law-

Yale Law School, New Haven, CT 06511, USA, and yer, sociologist, and reform advocate, is
Department of Sociology, Yale University, New Haven, CT what these opposing theses say about how
06511, USA. Email: [email protected] we think we must approach the politics of

658 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 sciencemag.org SCIENCE

Published by AAAS

People wait to enter summons court on 346 Broadway in New York City, in 2011. most other domains, respondents rated

PHOTO: JASON EPPINK/WIKIMEDIA COMMONS CC BY criminal legal reform. The hypotheses re- three-quarters of summonses and half of court FTAs as less likely attributable to “for-
flect our cultural assumptions: Either the misdemeanor arrests resulted in some kind
people summonsed by the state—largely of dismissal, most of them “earned” because getting” and more likely to be “intentional.”
low-income Black and brown residents— defendants did community service, agreed
are deserving of compassion or leniency to a temporary marking on their record, or And respondents were least supportive of
because they are oblivious, or they are un- just appeared in court until the prosecution
deserving because they are obstinate. But was willing to dismiss charges (2, 7). Many “nudges” in the criminal justice domain.
they are not excused on the same terms New York City prosecutors hold “clean slate”
many of us frequently invoke: We are busy, events where anyone with an outstanding These findings might just be ascriptions of
our time and resources are overtaxed, and summons warrant can have it dismissed
we sometimes fail to discharge some of our without adjudication or paying a fine. The blameworthiness. When people are asked
obligations because we are just emotion- entire logic of low-level enforcement is less
ally overwhelmed. about showing up to court for the purpose how likely it is that a criminal defendant
of adjudicating the underlying accusation
Unfortunately, the largely low-income than it is about showing up to court for the “intentionally and deliberately decided
and minority communities where summons purpose of demonstrating that one has un-
enforcement is concentrated have had all dertaken a cost to perform a responsibility. to skip their appointment,” they might be
too many encounters with the state’s pe-
nal authority. Most recognize that the little I would respectfully disagree with the reporting how likely they think it is that
piece of paper the police officer hands them authors’ assertion that our nation’s punitive
represents another mandatory encounter penal policies are “built on an assumption this person is as culpable as “intention-
with the state’s coercive arm. The fact that it that people intentionally weigh the costs
is confusing or mentally taxing to pin down and benefits” of illegal conduct. I would say ally deciding” to skip, whether or not the
the logistical details of how exactly to com- they are built on the assumption that the
ply is distinct from the claim that one is not people targeted by such policies—largely person actually knew when and where the
“aware” that the state has issued a sanction- people of color and impoverished people—
backed demand to do so. To live in poverty are undeserving of full and equal member- appointment was or remembered its occa-
and in highly policed neighborhoods in ship in our political community absent a
America is to be constantly subjected to positive showing of worthiness. sion (8). Similarly, respondents’ expression
such demands—from police, courts, welfare
agencies, child services, landlords—and to Consider the evidence presented by of preferences for punitive measures over
hear a persistent message that one’s failure Fishbane et al. in which MTurk participants
to successfully perform is proof of one’s un- responded to information about hypotheti- “nudges” in response to court FTAs does not
fitness for concern and respect in our polity. cal “failures to take a required action,” such
as paying bills, turning in educational pa- necessarily mean they believe one is more
At the height of “Broken Windows” polic- perwork, and making a required criminal
ing in New York City around 2010, almost court appearance (i.e., FTA). Compared to efficacious than the other in the criminal

justice domain. It might well reflect their

political moral judgments that people who

miss court, irrespective of the reasons, de-

serve punishments and not nudges. This is

especially likely given evidence that when-

ever you ask someone about their attitudes

toward crime, they are often also expressing

their attitudes toward race (9, 10).

Although it would be positive if many

jurisdictions would adopt the practices de-

scribed by Fishbane et al., changing the ap-

proach to penal and welfare policy in our

country will require interventions that are

much more radical than cost-neutral behav-

ioral nudges that everyone can agree on. j

REFERENCES AND NOTES

1. New York City does not collect racial identification data
on the summons form. Data on misdemeanor arrests
show that about 80% of fingerprintable misdemeanor
arrests in recent years are of Black or Hispanic individu-
als. See (2).

2. I. Kohler-Hausmann, Misdemeanorland: Criminal Courts
and Social Control in an Age of Broken Windows Policing
(Princeton Univ. Press, 2018).

3. A. Fishbane et al., Science 370, eabb6591 (2020).
4. The FTA rate for misdemeanor arrests (including“desk

appearance ticket”arrests) is substantially lower than
40%, with about half of those returning voluntarily
within 30 days of the missed court date. See data from
(5).
5. New York City Criminal Justice Agency, CJAAnnual
Report of 2017 (pp. 19, 36–38); https://www.nycja.org/
publications/cja-annual-report-2017.
6. D. Gal, D. D. Rucker, J. Consum. Psychol. 28, 497 (2018).
7. P. Chauhan et al.,The Summons Report: Trends in the
Issuance and Disposition of Summonses in New York
City 2003–2013; www.jjay.cuny.edu/sites/default/files/
news/Summons_Report_DRAFT_4_24_2015_v8.pdf.
8. This elision is what is behind much of criminal law doc-
trine on“willful ignorance,”where courts and juries find
defendants guilty because they believe choosing not to
know under certain circumstances is just as culpable as
knowing.
9. R. C. Hetey,J. L. Eberhardt, Psychol. Sci. 25, 1949 (2014).
10. This is analogous to a situation where people respond-
ing to the question“Do workers who are late for work
because of childcare problems deserve to be fired?”
might also be expressing beliefs about women in the
workforce.

Published online 8 October 2020

10.1126/science.abc2495

SCIENCE sciencemag.org 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 659

Published by AAAS

INSIGHTS | PERSPECTIVES

The development of carpenter ants (Camponotus
floridanus) into different worker castes is regulated
by the metabolic-epigenetic axis.

EPIGENETICS morphology and behavior. For example, in ad-
dition to the distinction of the female repro-
Food for thought ductive queen from sterile workers, some ant
species have evolved multiple female worker
The nuclear metabolic-epigenetic axis bridges classes. These so-called castes specialize in
the environment and genes to modulate behavior either foraging or defense behaviors that are
vital for the survival of such complex societ-
By Gabor Egervari, Karl M. Glastad, epigenetic interactions are the nuclear re- ies. Recent findings indicate that epigenetic- PHOTO: RJ GRAHAM/BERGER LAB, UNIVERSITY OF PENNSYLVANIA
Shelley L. Berger ceptor superfamily, which bind circulating to-metabolic signaling pathways play a criti-
small molecules, such as steroid and thyroid cal role in caste determination in carpenter
T o drive behaviors essential for survival, hormones. The binding of their ligands un- ants (Camponotus floridanus). Juvenile
numerous pathways have evolved that leashes nuclear receptors to bind to DNA as hormone (JH) is pivotal to programming
translate environmental stimuli into transcription factors. They subsequently re- foraging, and repressive epigenetic pathways
gene expression. These include inter- cruit coactivators and corepressors involved expressed during brain development estab-
actions between metabolic and epigen- in chromatin modulation, resulting in the lish low expression of enzymes that degrade
etic regulation, which encompass both activation of new transcriptional programs. JH to preserve JH in the adult brain (4).
predictable indirect connections and unan- These mechanisms translate changes in cir- Transient experimental manipulation of the
ticipated direct contacts (1). Indirect path- culating hormones into specific physiological brain epigenome in early adulthood of the
ways involve metabolites generated from diet and behavioral outcomes (2). An intriguing defense caste promotes long-lasting behav-
and other sources that provide substrates alternative model proposes that circulating ioral reprogramming through stable epigen-
and cofactors for epigenetic enzymes to en- hormones regulate the activity of certain epi- etic repression of the JH-degrading enzymes,
sure seamless adaption to nutrient availabil- genetic enzymes and thereby alter gene ex- switching behavior to foraging (4). Thus, the
ity. In addition, epigenetic mechanisms regu- pression and behavior. Specifically, estradiol epigenome “encodes” metabolic information
late the expression of metabolic enzymes, can increase brain masculinization in mice either naturally expressed during develop-
which can in turn produce or deplete various and rats by reducing DNA methyltransfer- ment or transiently encountered during
metabolites. The direct metabolic-epigenetic ase activity, which prevents or reverses DNA vulnerable windows in early life, leading to
interface, however, represents a paradigm methylation. This results in de-repression of long-term ossification of adaptive behavioral
shift in our mechanistic understanding of en- masculinizing genes in sexually dimorphic states. Many social insects can drastically al-
vironmental impacts on gene expression and brain regions during neonatal development ter their behavioral repertoire over their life
behavior. Direct communication is mediated (3). Of note, pharmacologic or genetic inhi- span to satisfy colony demands. The precise
by metabolic enzymes—classically thought to bition of DNA methyltransferases recapitu- role of metabolic-epigenetic reprogramming
reside in mitochondria and cytoplasm—lo- lates the effect of gonadal steroids, resulting in the regulation of these phenomena later in
calizing within the nucleus and even binding in masculinized neuronal markers and male life is currently unknown.
to chromatin. This surprising relocation en- sexual behavior in female rats (3).
ables the generation of metabolite pools that Beyond hormonal regulation, intermediary
can fuel epigenetic enzymes directly. Conversely, epigenetic pathways can de- metabolism also influences epigenetic mech-
termine amounts of circulating hormones, anisms. Metabolites serve as substrates and
Classic examples of indirect metabolic- leading to persistent developmental and be- cofactors for epigenetic enzymes, and their
havioral changes. Relevant model organisms availability and concentration can alter gene
Epigenetics Institute, Perelman School of Medicine at the are ants and other social insects—bees, some expression (1). Furthermore, provocative re-
University of Pennsylvania, Philadelphia, PA, USA. Email: wasps, and termites—wherein closely related cent findings identified previously unknown
[email protected] individuals exhibit dramatic differences in histone modifications that can be driven by
metabolites. These include, for example, the
direct incorporation of lactate into chroma-
tin. Lactate covalently binds to several lysine
residues on core histone proteins, in a pro-
cess potentially regulated by histone acetyl-
transferases, such as p300 (5). Histone lacty-
lation is induced by hypoxia and by bacterial
infection in human and mouse cells, helping
to reestablish homeostatic gene expression
(5). Further examples include the deposition
of bioamine neurotransmitters serotonin (6)
and dopamine (7) as covalent modifications
of histones. Histone serotonylation potenti-
ates binding of transcription factor IID to
methylated histones (6). Serotonylation is en-
riched in the brain and gut (6), which are the
primary sites of serotonin production, raising
the intriguing possibility that incorporation
into chromatin is dependent on metabolic

660 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 sciencemag.org SCIENCE

Published by AAAS

availability in those tissues. Similarly, histone bolic enzymes that synthesize acetyl-CoA: Of particular interest is a nuclear meta-
dopaminylation occurs in dopamine-produc- acetyl-CoA synthetase (ACSS2) (8, 9) and bolic-epigenetic interface in neurons, where
ing neurons of the ventral tegmental area, a ATP-citrate lyase (ACLY) (10). By modulating metabolic regulation of histone acetylation
midbrain region involved in reward and mo- local acetyl-CoA pools, these nuclear meta- serves a key role in spatial learning and mem-
tivated behaviors. Dopaminylation accumu- bolic enzymes regulate histone acetylation. ory. Chromatin-bound ACSS2 is enriched at
lates during cocaine withdrawal, leading to Another example is chromatin-bound fuma- promoters of immediate early genes (IEGs), a
transcriptional changes in this brain region. rase, which affects histone methylation by set of rapidly induced genes (mostly encoding
Inhibiting histone dopaminylation rescues inhibiting 2-oxoglutarate–dependent lysine transcription factors) that drive activity-de-
cocaine withdrawal-associated phenotypes demethylases (11). pendent functional and structural changes in
and attenuates drug-seeking behavior in rats neurons and underlie synaptic plasticity and
(7). Building on these early findings, the ex- These paradigm-shifting mechanisms have learning. Reduction of ACSS2 in the hippo-
tent to which intermediary metabolites are profound relevance for health and disease. campus attenuates long-term spatial memory
directly incorporated as histone modifica- Direct metabolic-epigenetic interactions reg- formation and reconsolidation (8). Further,
tions and their precise role in cells and organ- ulate autophagy (9) and cell differentiation environmental metabolic fluctuations can in-
isms remain to be fully elucidated. (8, 10) and thus can alter the behavior and fluence this pathway. Circulating acetate de-
identity of specific cells. For example, ACLY rived from consumed alcohol is captured by
Recently, an unanticipated model has dynamically regulates histone acetylation in ACSS2 in neuronal nuclei and turned into a
arisen for direct interplay between meta- response to growth factor–induced nutrient local pool of acetyl-CoA. This is incorporated
bolic and epigenetic enzymes (see the figure). uptake, thus coordinating cell growth and into histone acetylation at IEGs, resulting
Contrary to prevailing dogma that places differentiation with metabolic state (10). in the activation of transcription programs
them exclusively in the mitochondria or cy- These changes, in turn, can also lead to im- that underlie associative spatial memory
toplasm, metabolic enzymes can translocate paired organismal function and disease. In formation (12). Through this pathway, direct
to the nucleus and be recruited to chromatin many cases, dysregulation of these pathways incorporation of alcohol metabolites into
to regulate local metabolite concentrations is linked to cancer. ACSS2-mediated histone brain histone acetylation may play a critical
in the nucleus or even at specific gene loci. acetylation is implicated in brain tumori- role in encoding drug-related environmental
These nuclear metabolic enzymes influence genesis, and ACSS2 concentrations in the stimuli, which contribute to craving, relapse,
gene expression programs through associa- nucleus correlate with grades of glioma ma- and development of substance use disorders.
tion with DNA-bound transcription factors, lignancy in humans (9). Chromatin-bound
chromatin remodelers, and histone modifi- fumarase promotes tumor growth under glu- Future research will expand our under-
ers. Prominent examples are nuclear meta- cose deficiency (11). standing of mechanisms that control this
metabolic-epigenetic axis. Precise regula-
The metabolic-epigenetic axis and behavior tion is required to restrict consequences of
natural hormonal and metabolic fluctuations
Through direct and indirect metabolic-epigenetic interactions, transient environmental perturbations can that would otherwise change the epigenome,
influence gene expression programs, leading to long-lasting functional and behavioral adaptations. For example, leading to stochastic alterations in transcrip-
chromatin-bound metabolic enzymes can facilitate the direct transfer of metabolites between histone tion. One key regulatory mechanism is the
residues and increase the local concentration of active metabolite pools in phase-separated chromatin domains. shuttling of metabolic enzymes between
the cytoplasm and nucleus. This is gated by
Environmental stimuli Precursor metabolites Indirect Active Transcriptional phosphorylation or other modifications (9,
infuence precursor metabolites changes drive 11), perhaps to regulate interaction with nu-
metabolite availibility (cytoplasm) behavioral clear import factors and epigenetic enzymes.
adaptations For example, a recent study demonstrates
Circulating Lactate, Cytoplasmic interactions between the folate pathway
ligands serotonin, and metabolic enzymes Epigenetic enzyme methylenetetrahydrofolate dehy-
dopamine mechanisms drogenase 1 (MTHFD1) and an acetyl-group
of nuclear regulate reader protein, bromodomain-containing 4
receptors metabolic (BRD4). This interaction drives recruitment
pathways of MTHFD1 to chromatin to regulate the
Direct nuclear concentration of one-carbon (methyl
Nuclear group) metabolites required for transcrip-
metabolic enzymes (nucleus) tion, thereby driving cancer cell proliferation
(13). Thus, there are likely to be numerous
mRNA mechanisms to fine-tune metabolic-epigen-
etic signaling in specific tissues—including
Chromatin Nuclear distinct neuronal circuits—in response to en-
remodelers membrane vironmental stimuli, which is critical for ef-
fective regulation of behavioral adaptations.
Chromatin- TF
bound An interesting functional implication of
metabolic nuclear and chromatin-bound metabolic en-
enzymes zymes is their availability to recycle posttrans-
lational modifications released from histones.
GRAPHIC: C. BICKEL/SCIENCE Phase 1 Phase 2 Nuclear R A This could accomplish dynamic and rapid
receptors gene activation. Intriguingly, under oxygen
A, activating histone modifcation; mRNA, Chromatin-bound and nutrient limitation, nuclear ACSS2 main-
messenger RNA; R, repressive histone metabolic enzymes tains histone acetylation and gene expression
modifcation; TF, transcription factor.

SCIENCE sciencemag.org 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 661

Published by AAAS

INSIGHTS | PERSPECTIVES

by converting acetate released by histone PA L E O C L I M AT E
deacetylases into acetyl-CoA, which is then
used by histone acetyltransferases (14). Local Steering iceberg armadas
recapturing of acetate and other metabolites
may be essential to maintain or activate new The Asian-Pacific tropics likely instigated millennial-scale
programs of gene expression in nutrient-poor climate changes
environments. Certain metabolites have pro-
foundly distinct effects on transcription, de- By John M. Jaeger1 and Amelia E. Shevenell2 The paradigm holds that the intensity of
pending on the histone residue. For example, North Atlantic Deep Water (NADW) pro-
methyl groups correlate with active [e.g., tri- S cience is theoretically objective, but duction controls the rate of the Atlantic
methylated histone H3 lysine 4 (H3K4me)] or biases and paradigms often originate Meridional Overturning Circulation
repressed (e.g., H3K27me) gene expression. A from something as fundamental as (AMOC), a central component of Earth’s
potential scenario emerges whereby chroma- field site accessibility, data density, climate system (3). A key supporting ob-
tin-bound metabolic enzymes associate with or publication date. Such biases may servation is the tenuous temporal link be-
epigenetic enzymes to enable direct transfer be at the heart of an enduring para- tween abrupt North Atlantic climate tran-
of molecules from repressive to activating digm in paleoceanography and paleoclima- sitions during the last glaciation, inferred
histone residues (or the reverse) to facilitate tology—that changes in cold dense water from Greenland ice cores, and melting of
rapid transcriptional changes required for production in the North Atlantic Ocean marine-terminating ice sheets encircling
cellular and behavioral adaptations. forced millennial-scale (<1000 year) global the North Atlantic (4). Marine sediments
climate changes during the past ~50,000 deposited in the glacial North Atlantic con-
Another possibility is that nuclear meta- years. These changes were first identified tain discrete layers of detrital carbonate-
bolic enzymes are required to maintain me- in Greenland ice cores >30 years ago (1). rich sands in muddy sediments (5). These
tabolite concentrations in phase-separated On page 716 of this issue, Walczak et al. coarse deposits, called Heinrich events,
chromatin domains (15). Free diffusion of me- (2) present compelling data from marine suggest melt-out from debris-rich icebergs
tabolites between liquid phases may be lim- sediments collected in the Northeast Pacific calved from North America’s Laurentide Ice
ited, and phase-separated chromatin modi- Ocean that add to evidence indicating that Sheet. Iceberg “armadas” and associated
fiers might thus be largely segregated from the engine of Earth’s climate system lies low-salinity glacial meltwater likely dis-
the nuclear and cytoplasmic pools of their outside the North Atlantic. rupted NADW production, thereby slowing
substrates. Further, chromatin phase sepa-
ration is regulated by posttranslational his- Unraveling a chain of regional climate events 50,000 years ago
tone modifications, for example, acetylation
(15), which is under metabolic control. It re- Paleoclimate records from places like the Hulu Cave in China record strong Asian monsoon periods preceding
mains to be seen whether metabolic enzymes Cordilleran melting events by a few millennia. Recurrent changes in iceberg discharges from the Cordilleran
phase-separate with epigenetic regulators Ice Sheet coincide with Sea of Okhotsk sinking water production and precede regional climate changes in
and whether colocalization to specific phases Greenland found in North Greenland Ice Core Project (NGRIP) ice cores and produced Heinrich event icebergs.
is required to maintain specific epigenetic U1419, Integrated Ocean Drilling Program (IODP) Site U1419.
signatures.
Heinrich event icebergs North Atlantic
The dialogue between metabolism and epi-
genetics within the nucleus presents a prom- Asian Pacifc tropospheric Atlantic Meridional
ising target for future therapeutic interven- moisture delivery Overturning Circulation
tions. Certain metabolic-epigenetic pathways
could be targeted to inhibit tumor formation Siku event icebergs Arctic Ocean NGRIP
and growth (9, 13) or to attenuate certain and meltwater
forms of unwanted memories (e.g., environ-
mental cues that trigger relapse in substance- Sea of Laurentide
use disorders or flashbacks in posttraumatic Okhotsk Ice Sheet
stress disorder) (12). Hence, continued in- Hulu
vestigation of the metabolic-epigenetic axis Cave
holds an exciting potential to launch future
therapies. j Bering Sea/ Cordilleran GRAPHIC: V. ALTOUNIAN/SCIENCE; (GLOBE) NOAA
Land Bridge Ice Sheet
REFERENCES AND NOTES
U1419
1. X. Li, G. Egervari,Y.Wang, S. L. Berger,Z. Lu, Nat. Rev.
Mol. Cell Biol. 19, 563 (2018). Vancouver Island
Santa Barbara Basin
2. R. M. Evans, D.J. Mangelsdorf, Cell 157, 255 (2014). Gulf of California
3. B. M. Nugent et al., Nat. Neurosci. 18, 690 (2015).
4. K. M. Glastad et al., Mol. Cell 77, 338 (2020).
5. D.Zhang et al., Nature 574, 575 (2019).
6. L.A. Farrelly et al., Nature 567, 535 (2019).
7. A. E. Lepack et al., Science 368, 197 (2020).
8. P. Mews et al., Nature 546, 381 (2017).
9. X. Li et al., Mol. Cell 66, 684 (2017).
10. K. E.Wellen et al., Science 324, 1076 (2009).
11. T.Wang et al., Nat. Cell Biol. 19, 833 (2017).
12. P. Mews et al., Nature 574, 717 (2019).
13. S. Sdelci et al., Nat. Genet. 51, 990 (2019).
14. V. Bulusu et al., Cell Rep. 18, 647 (2017).
15. B.A. Gibson et al., Cell 179, 470 (2019).

10.1126/science.abb4367

662 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 sciencemag.org SCIENCE

Published by AAAS

the AMOC and altering global ocean circu- changes by 1000 to 1500 years. This pattern CORONAVIRUS

lation (4). This cascade of events forms the of leads and lags supports the hypothesis Public health
during the
working hypothesis for abrupt (<decade) that the North Pacific is not a passive recipi- pandemic in
India
transitions between cold and warm climate ent of North Atlantic climate changes, but
Data from two Indian
states on millennial time scales during the rather is close to the source of millennial- states give detail about
variation in transmission
last glaciation (4, 5). Globally distributed scale climate perturbations. and disease outcomes

paleoclimate records reveal similar abrupt Millennial-scale climate changes at- By Jacob John1 and Gagandeep Kang2

transitions and millennial-scale events over tributed to Northern Hemisphere atmo- I n March 2020, with coronavirus disease
2019 (COVID-19) threatening to over-
the same period, and these signals are of- spheric teleconnections also are observed whelm India’s fragile health care ecosys-
tem, the country combined a stringent
ten linked to North Atlantic processes, even in the Santa Barbara basin (7), the Gulf of lockdown of its 1.37 billion population
with a program of surveillance and con-
though the root cause of the abrupt events California (8), and off Vancouver Island (9). tainment of varied effectiveness across states.
Testing and data management systems were
is debated (1, 3–10). However, these records lacked the resolution set up, but the paucity of publicly available
data, especially in the initial phase of the
Walczak et al. challenge this paradigm, or detailed independent chronologies to de- pandemic, limited understanding of disease
epidemiology and transmission dynamics as
presenting a high–temporal resolution ma- finitively determine the phasing of tropical, well as the effectiveness of control measures.
On page 691 of this issue, Laxminarayan et
rine sediment record from the Northeast North Pacific, and North Atlantic changes. al. (1) present findings from government-
implemented surveillance during the first 4
Pacific Ocean (see the figure). They use Walczak et al. have the necessary archival months of the pandemic in the two southern
states of Tamil Nadu and Andhra Pradesh
similar sedimentary archives and data from resolution and chronological control to con- in India. They use data from, and after, the
lockdown period to make important obser-
North Atlantic studies to document changes fidently assess this phasing. The authors’ vations on the dynamics of infection, trans-
mission, and risk factors. This collaboration
in regional Northeast Pacific data provide evidence that between the state governments of Tamil
Nadu and Andhra Pradesh and academic re-
climate. They suggest that globally recognized millen- searchers is a valuable template for federal
nial-scale climate changes government agencies.
“…climate signalssimilar armadas of icebergs,
The public health response to infectious
“Siku events,” calved epi- in the North Atlantic likely originated in the disease outbreaks is founded on the ability
sodically from the marine- consistently follow, tropical Asian-Pacific region. to mount a coordinated strategy that com-
terminating Cordilleran Ice Changes in heat and mois- bines measuring and tracking cases to assess
Sheet, when regional atmo- not lead,those ture transport via the west- the efficacy of interventions. For COVID-19,
spheric temperatures were erly Northern Hemisphere testing, tracing, treating and isolating cases,
quarantining contacts, as well as widespread
relatively warm. As in the observed in the jet stream likely explain mask wearing and social distancing were,
North Atlantic, these Siku synchronous rapid Northern and are, the tools for transmission control.
India’s population is second only to China’s
Northeast Pacific…”events were accompanied Hemisphere warming dur-
1Department of Community Health, Christian Medical
by fresh glacial meltwa- ing the last glaciation (10). College, Vellore TN, India. 2Division of Gastrointestinal
Sciences, Christian Medical College, Vellore TN, India.
ter that restricted vertical The atmospheric warming Email: [email protected]

ocean mixing, resulting in the apparent ag- melted the Cordilleran Ice Sheet, produc-

ing of intermediate-depth ocean waters (2). ing glacial meltwater that may have pro-

The record of Walczak et al. indicates that vided freshwater (via the Bering Sea and

climate signals in the North Atlantic con- Arctic Ocean) that slowed the AMOC (9,

sistently follow, not lead, those observed in 12). Additional evidence from the circum-

the Northeast Pacific, questioning whether Antarctic Southern Ocean indicates that

NADW perturbations initiate these global overturning driven by tropical atmospheric

events (3–6). perturbations regulated glacial-intergla-

Modern North Pacific climate is influ- cial CO concentrations, rather than the
2

enced by atmosphere-ocean coupling in the AMOC (13). Taken together, paleoclimate

tropical Indian and western Pacific Oceans and paleoceanographic records far from

(e.g., El-Niño Southern Oscillation, mon- the North Atlantic argue that it is time to

soons) (11). Walczak et al. propose that pro- revisit this paradigm central to paleocean-

cesses in the Asian tropics initiated glacial ography and paleoclimate studies since the

atmospheric perturbations, which affected first high-resolution ice core was drilled in

ocean circulation and CO cycling on mil- Greenland (1, 3). j
2
REFERENCES AND NOTES
lennial time scales. The authors link glacial 1. W. Dansgaard et al., Nature 364, 218 (1993).
Northeast Pacific atmospheric warming and 2. M. H.Walczak et al., Science 370, 716 (2020).
surface ocean freshening to times when the 3. A. Ganopolski, S. Rahmstorf, Nature 409, 153 (2001).
Asian monsoons were relatively strong, as 4. W. S. Broecker, Nature 372, 421 (1994).
indicated by independently dated Chinese

speleothem records. 5. G. C. Bond, R. Lotti, Nature 267, 1005 (1995).
Critically, the atmospheric and oceanic 6. N. Brown, E. D. Galbraith, Clim. Past 12, 1663 (2016).
7. I. L. Hendy,J. P. Kennett, Geology 27, 291 (1999).
changes triggering Siku events observed 8. T. Bhattacharya et al., Nat. Geosci. 11, 848 (2018).
in Walczak et al.’s independently dated 9. I. L. Hendy,T. Cosma, Paleoceanography 23, PA2101

Northeast Pacific record follow Asian mon- (2008).
soon changes by 1000 to 3000 years and 10. S. K. Praetorius,A. C. Mix, Science 345, 444 (2014).
precede North Atlantic Heinrich events 11. J. Emile-Geay, J. Geophys. Res. 108 (C6), 3178 (2003).
and Antarctic and global atmospheric CO 12. S. K. Praetorius et al., Sci.Adv. 6, eaay2915 (2020).
13. A. C. Mix et al., in Mechanisms of Global Climate Change
2
at Millennial Time Scales, P. U. Clark et al., Eds. (Geophys.

1Department of Geological Sciences, University of Florida, Monogr. Ser.,American Geophysical Union), vol. 112, pp.
Gainesville FL 32611-2120, USA. 2College of Marine Science, 127–148.
University of South Florida, St. Petersburg, FL 33701, USA.
Email: [email protected]; [email protected] 10.1126/science.abe8461

SCIENCE sciencemag.org 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 663

Published by AAAS

INSIGHTS | PERSPECTIVES

approximately 1.41 billion, in one-third of the data across the globe (5, 6). The determinants More than half the reported deaths in

land area, and so when severe acute respira- of superspreading are not well understood, these two states occurred within 6 days of

tory syndrome coronavirus 2 (SARS-CoV-2) but it is likely to be a function of social in- diagnosis compared with 16 days in China

began its relentless spread outside China, teraction patterns of the infectious host, the (12). There are several potential explanations.

there were concerns about the ability of low- environment, and biological characteristics During the lockdown and with concerns

and middle-income countries (LMICs) to de- of the infectious agent. Identifying the char- about transmission, individuals who were ill

ploy public health tools, given their limited acteristics of settings where superspreading may have come to health care facilities late

health care capacity. events are likely will help target control mea- in their illness. It is also possible that owing

Although there were limitations in track- sures and screening for those settings to max- to limited capacity, testing was reserved for

ing in many parts of the world, the data imize limitation of transmission. However, those who had more advanced symptoms

from hospitals and laboratories were widely focused control measures must be balanced and were potentially more likely to die. In

available, allowing modelers in academia against the potential for further stigmatiza- the early phase of the pandemic, the treat-

and public health systems to use data from tion of individuals with COVID-19 beyond ment facilities may have been inadequately

China and the industrialized world early in that already reported (7). prepared, equipped, and staffed. The 26%

the pandemic to build predictive improvement in mortality risk

models based on the government in recent months in these states

strategies that were developed Cases and deaths in two southern states of India (1) may partly be attributed to
(2). Although useful, these mod- improved access to testing, treat-
els are sensitive to underlying Trends in case detection (7-day moving average is shown) and coronavirus ment, and health care infrastruc-
assumptions about contact pat- disease 2019 (COVID-19) fatalities in Andhra Pradesh ( ) and Tamil Nadu ( ) ture over time.
terns and transmissibility of the highlight low case fatality and the eIects of early interventions.
The observation that traveling

infection, which are affected by 12,000 Lockdown in proximity to a case for a long
population density, occupation, duration was a risk factor for

and social structures. In India Daily cases10,000 Study period transmission merits special con-
and other LMICs, the lack of in- 8000 sideration for India, where most
formation sharing for analysis 6000 interstate transport is by train,
between government agencies bus, and truck. Studies in other

with access to the data and aca- 4000 parts of the world on air travel

demic groups with the skills to 2000 have also documented spread
perform these analyses resulted 0 (13). Most of these studies report
in control strategies being widely data before widespread mask

debated because the evidence Daily deaths 400 use, and experimental and real-
base for policy was unclear (3, 4). 200 world data obtained from using
different modes of transport with
Despite the perpetual un-

derinvestment in public health 0 well-described air circulation
in India, both Andhra Pradesh March April May June July August September must be used to inform travel

and Tamil Nadu have functional guidance (14). More studies from

public health departments. Laxminarayan The contact tracing data suggests two diverse settings at this stage of the pandemic,

et al. describe scaling of contact tracing to important findings regarding transmission. particularly including data from serosurveys,

reach more than 3 million exposed contacts First, there is an increased likelihood of are needed to better understand factors de-

and collect epidemiological and laboratory cases infecting contacts of similar ages, and termining transmission, plan interventions,

data from 575,051 contacts of cases in the second, that children under 14 are active and predict outcomes in LMICs. j

first 4 months of the pandemic, when such participants in transmission. These findings REFERENCES AND NOTES
extensive contact tracing was most likely to probably reflect prevalent social mixing pat-
be beneficial. The surveillance was not per- terns in India (8) but raise concerns about 1. R. Laxminarayan et al., Science 370, eabd7672 (2020).
fect. There were variations in the effective- the possibility of enhanced transmission 2. S. Flaxman et al., Imperial College COVID-19 Response

Team, Nature 584, 257 (2020).

ness of screening across districts, with most when poorly ventilated, crowded schools re- 3. The Lancet, Lancet 396, 867 (2020).
cases having an improbably low number of open (9). Children have been implicated in 4. Indian Public Health Association, Indian Association
exposed contacts. Testing strategies changed the transmission of other respiratory infec-
of Epidemiologists, Indian Association of Social and
Preventive Medicine,“3rd joint statement on covid-19

multiple times as the public health response tions to the elderly when intergenerational pandemic in India—Public health approach for covid-19
adapted to emerging challenges, complicat- contact is frequent (10). Careful monitoring control”(2020); https://bit.ly/2ITbky8.
ing analyses of infection rates and infection of transmission by children will be vital to 5. A. Endo, S.Abbott,A.J. Kucharski, S. Funk, Centre for the
fatality ratios. Despite these limitations and shield vulnerable older adults and those Mathematical Modelling of Infectious Diseases COVID-
the subsequent escalation in cases (see the with comorbidities. At the other end of the 19 Working Group, Wellcome Open Res. 5, 67 (2020).
figure), the authors have generated impor- age spectrum, the low mortality rate in the 6. M. S.Y. Lau et al., Proc. Natl.Acad. Sci. U.S.A. 117, 22430
(2020).
7. E. Cave, Asian Bioeth. Rev. 1 (2020). 10.1007/

tant insights. elderly as reported by Laxminarayan et al. s41649-020-00118-2 GRAPHIC: N. CARY/SCIENCE
The study highlights the importance of indicates the need to better understand the 8. S. Kumar et al., PLOS ONE 13, e0209039 (2018).
composition of older age groups by socio- 9. J. P. Majra,A. Gur, J. Glob. Infect. Dis. 2, 109 (2010).
“superspreaders” in fueling the pandemic. economic status and comorbidities to clar- 10. S. Cauchemez,A.J.Valleron, P.Y. Boëlle,A. Flahault, N. M.
Although there were limitations in contact ify the contribution of the survivor effect.
tracing, and hence in the evaluation of sec- The lower death rates may also reflect that Ferguson, Nature 452, 750 (2008).
ondary cases and of transmission chains, the those who live longer in LMICs are more 11. S.Afshar, P.J. Roderick, P. Kowal, B. D. Dimitrov,A. G. Hill,
finding that a minority of cases were associ-
BMC Public Health 15, 776 (2015).
12. T. Chen et al., BMJ 368, m1091 (2020).
13. J. Chen et al., Travel Med. Infect. Dis. 36, 101816 (2020).

ated with most transmission events (super- healthy than people of similar ages in high- 14. C.O.Buckee et al.,Science 368,145 (2020).

spreading) is consistent with the emerging income countries (11). 10.1126/science.abe9707

664 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 sciencemag.org SCIENCE

Published by AAAS

POLICY FORUM The 2017 decision to not protect the Pacific walrus
(shown) was based on projections to only 2060,
despite a 2012 decision to protect the Arctic ringed
seal that looked out to 2100.

C O N S E R VAT I O N “threatened,” which means likely to become
endangered in the “foreseeable future.” In
Species protection will take 2009, the Services first articulated their un-
more than rule reversal derstanding of the term “foreseeable future,”
declaring that it covers the time frame over
Key improvements are needed for implementation which predictions of the extent of threats and
of the Endangered Species Act their impact on species are “reliable” (6). The
new regulations provide that the foreseeable
PHOTO: MIKE KOROSTELEV/MINDEN PICTURES By Ya-Wei Li1, Joe Roman2, David S. Wilcove3, ardent among many environmentalists, sci- future “extends only so far into the future
Timothy Male1, Holly Doremus4 entists, and the public. Opposition to the ad- as the Services can reasonably determine
ministration’s changes, however, should not that both the future threats and the species’
S pecies are disappearing at an alarming overshadow the need for improvements to responses to those threats are likely.” The
rate, with global estimates of about a how the ESA is administered to make it more agencies’ explanation “clarifies” that “likely”
million species facing extinction (1). effective. Simply revoking recent changes will means “more likely than not.” Thus, whether
The Endangered Species Act (ESA), not solve these underlying problems. this new definition will change established
the primary—and often only—means practice turns on the difference, if any, be-
in the United States to prevent ex- Without deeper reforms to address under- tween whether predictions of the future are
tinctions, is justly celebrated as perhaps the lying problems, implementation of the ESA “reliable” or “likely.” The Services claim that
strongest model for endangered species pro- by the U.S. Fish and Wildlife Service (FWS) there is no difference, whereas many envi-
tection worldwide. Since its adoption, how- and the National Marine Fisheries Service ronmentalists see an intent to ignore climate
ever, the ESA has faced unabated controversy (NMFS) (“the Services”) will remain ad hoc change impacts on species (7).
because it can restrict economic activities and and insufficiently explained (5). This ambigu-
because its implementation often appears in- ity invites political intervention that under- Whatever the linguistic change means,
consistent. With the explicit goal of reducing cuts species protection and public confidence the underlying problem of inconsistent and
“unnecessary regulatory burdens,” the Trump in ESA decisions, triggers litigation that is inadequately explained treatment of the fore-
administration in 2019 finalized the most costly for all parties, and polarizes the law. seeable future remains. The Services have
comprehensive changes in more than two Finding solutions to these problems could applied notably different interpretations to
decades to the regulations that implement lead to broad bipartisan initiatives to stem species facing similar threats. When NMFS
the ESA (2). Some of the changes will make it biodiversity loss and to increase funding for listed the Arctic ringed seal (Phoca hispida
harder to protect species and their habitats; the ESA by reauthorizing the law. hispida) in 2012, for example, it estimated
none will directly further the Act’s goal of re- the threat of reduced sea ice and snow cover
covering species. For example, the changes DEFINING THE “FORESEEABLE FUTURE” out to the year 2100, stating that it was able
limit the government’s ability to protect One of the controversial revisions pertains to “reliably” forecast ~90 years into the fu-
habitat that species need to adapt to climate to how the Services determine the “foresee- ture on the basis of models of how global
change (3) and make it harder for the pub- able future,” which is used to decide whether greenhouse gas levels would affect the Arctic
lic to hold the federal government account- species merit listing as “threatened” under environment (8). But when FWS declined
able for activities that further imperil species the ESA. The law recognizes two levels of to list the Pacific walrus (Odobenus rosma-
(4). Opposition to the changes was swift and threat: Species may be “endangered”—that rus divergens) in 2017 in the face of similar
is, presently in danger of extinction—or threats, it limited its evaluation to 2060 be-
cause it considered any conclusions beyond
that date to be “based on speculation, rather
than reliable prediction” (9). The Services
did not articulate any difference in the natu-
ral histories of the seal or walrus that could
justify this difference. The state of Alaska has
petitioned NMFS to remove the Arctic ringed
seal from the endangered species list in part
on the basis of this discrepancy (10).

Courts and researchers also have ex-
pressed concerns about inconsistencies or
arbitrariness in how FWS has interpreted
the “foreseeable future” (11, 12). For example,
when a court rejected FWS’s listing of the

1Environmental Policy Innovation Center, Washington,
DC, USA.2Gund Institute for Environment, University of
Vermont, Burlington, VT, USA.3Princeton School of Public
and International Affairs and Department of Ecology and
Evolutionary Biology, Princeton University, Princeton, NJ,
USA.4School of Law, University of California, Berkeley,
Berkeley, CA, USA. Email: [email protected]

SCIENCE sciencemag.org 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 665

Published by AAAS

INSIGHTS | POLICY FORUM

northern long-eared bat (Myotis septentrio- equately explained their choices. Under the A new regulatory and funding package for
nalis) as threatened instead of endangered, ESA, the Services “may” offer threatened spe-
the agency did not dispute that its evaluation cies none, some, or all of the section 9 protec- working with private landowners to conserve
of threats, which extended only 8 to 13 years tions. In the context of agricultural activities,
into the future, was an irrational approach to for example, FWS offered the Gunnison sage- imperiled species, including dedicated staff-
interpreting the foreseeable future (13). The grouse (Centrocercus minimus) full protec-
new foreseeable future definition does not fix tions. By contrast, the 4(d) rule for the related ing for ESA voluntary conservation initiatives
these problems, but neither will restoring the lesser prairie chicken (Tympanuchus palli-
prior one. dicinctus) exempted all routine agriculture and tax benefits for easements and donations
on cropland maintained in cultivation (14).
What is required is consistency and trans- The agency may have had valid reasons for of private land for rare-species conserva-
parency. That will come only if the Services this discrepancy, but they have never publicly
issue guidance that will both hold them ac- explained those reasons. Exemptions in 4(d) tion, would unlock recovery opportunities
countable and explain the principles that rules thus often appear as ad hoc decisions
motivate their decisions. Such guidance influenced by political pressure to minimize for many species that rely on private lands.
should ensure, for example, that projections regulatory impacts of listing a species. This
about both the geophysical aspects of climate concern can trigger litigation from conserva- Conservation on federal lands could benefit
change and their effects on species are con- tion groups, resulting in further controversy
sistent across comparable situations. Once and expenditure on lawsuits. from legal incentives for federal agencies to
NMFS concluded that the extent of sea ice loss
was reliably foreseeable to 2100, any conflict- The Services should develop policy that re- carry out actions that go beyond the mini-
ing decisions should explain why that conclu- solves key issues pertaining to protection of
sion was wrong or why it merits revision in threatened species through 4(d) rules. That mum required by the ESA, such as rewarding
light of new data. Given that 2100 is embed- policy should directly address the question
ded in many of the global climate projections that they have long ducked: What protections agencies with greater management flexibility
constructed by the Intergovernmental Panel meet the ESA’s standard of being “necessary
on Climate Change, we suggest this date as a and advisable” to conserve threatened spe- when they help a species exceed its recovery
conservative starting point for assessing spe- cies? Having a policy that states the relevant
cies vulnerable to climate change. Although principles would limit the Services’ tendency milestones. A new wildlife data and technol-
climate change could affect individual spe- to bow to political pressures, creating an ad
cies differently, the Services should clearly ex- hoc patchwork of protections. It could also ogy initiative could bring ESA implementa-
plain the evidence for these varied effects and help assure landowners that voluntary ef-
the justification for differential treatment. forts at conservation will not bring a heavy tion into the 21st century by taking advan-
regulatory crackdown. At a minimum, activi-
EXPLAINING DISCRETION ties that would undercut a species’ recovery tage of open and machine-readable data,
The key protections of section 9 of the ESA should be regulated through 4(d) rules, and
apply only to endangered species, not threat- activities that promote recovery should be remote sensing data, and other technologi-
ened species. Protections include restrictions strongly considered for exemption. An exam-
on importing endangered species into the ple is the recent 4(d) rule for the Louisiana cal innovations to help monitor species and
United States, trafficking in them or their pine snake (Pituophis ruthveni), which ex-
parts, and harming or harassing endangered empts forestry activities that improve the their habitats. Such advances offer some of
animal species by other means, including snake’s habitat but regulates intensive me-
habitat destruction. For threatened species, chanical forestry practices that can degrade the best opportunities to understand how cli-
Congress gave the Services the authority to that habitat (15). Second, the Services should
decide on a species-by-species basis which commit to finalizing the protections that a mate change will affect the nearly 2400 spe-
protections to apply. FWS has long extended threatened species needs when it is listed,
by default the full protections of section 9 to unless there is substantial uncertainty about cies protected by the ESA.
all threatened species while retaining discre- whether the protections will benefit the spe-
tion to modify those protections on a species- cies. By addressing these and other basic is- To keep pace with our biodiversity crisis,
by-species basis through a special rule issued sues, the agencies can help ensure that pro-
under section 4(d) of the ESA. The recent tections for threatened species are adequate the ESA will need to go well beyond the sta-
regulatory revisions withdrew those default and predictable.
protections for future listings, requiring tus quo. Let the current controversy over
FWS to issue a 4(d) rule whenever it seeks NEW APPROACHES
to extend any protection to those species and The improvements above focus on issues that the revised regulations serve as the starting
aligning the agency’s approach with that of are addressed in the recent rulemaking and
NMFS, which has never extended default that can be addressed without legislation, point to finding meaningful solutions and
protection to all threatened species. Despite but other reforms also deserve priority. For
this reversal in FWS policy, the agency is still example, in 2016 FWS developed a plan to having deeper discussions of what must be
able to offer threatened species as many or address its backlog of decisions on whether
as few protections as it deems necessary for to list hundreds of species under the ESA. done to conserve imperiled species in the
conservation—as has always been the case. FWS will need to diligently implement the
plan to reduce litigation over delayed listing United States and elsewhere. The passage of
The problem is that the Services have decisions—something it has so far failed to
never issued clear guidance on how they will do, partly because of political intervention. the Great American Outdoors Act reminds us
exercise this discretion, nor have they ad-
that conservation can still be a bipartisan is-

sue. The reforms we suggest could help bring

us closer to consensus on the ESA. j

REFERENCES AND NOTES

1. Intergovernmental Science-Policy Platform on
Biodiversity and Ecosystem Services,“Global assess-
ment report on biodiversity and ecosystem services”
(2019).

2. FWS, NMFS,“Trump administration improves
the implementing regulations of the Endangered
Species Act”(2019); www.fws.gov/news/ShowNews.
cfm?ref=trump-administration-improves-the-imple-
menting-regulations-of-the-&_ID=36443.

3. FWS, NMFS, 84 Fed. Regist. 84, 45020 (2019) [to be
codified at 50 Code of Federal Regulations (C.F.R.) §
424.12] (2019).

4. FWS NMFS, Fed. Regist. 84, 44976 (2019).
5. H. Doremus, Wash. Univ. Law Q. 75, 1029 (1997).
6. U.S. Department of the Interior,“The Meaning of

‘Foreseeable Future’in Section 3(20) of the Endangered
Species Act,”memorandum M-37021 (2009).
7. R. Beitsch, The Hill, 12 August 2019; https://thehill.com/
policy/energy-environment/457086-trump-adminis-
tration-rolls-back-endangered-species-protections.
8. NMFS, Fed. Regist. 77, 76706 (2012).
9. FWS, Fed. Regist. 82, 46618 (2017).
10. State of Alaska et al.,“Petition to Delist the Arctic
Subspecies of Ringed Seal (Phoca Hispida Hispida)
Under the Endangered Species Act”(2019).
11. Defenders of Wildlife v. Jewell, 176 F. Supp. 3d 975 (D.
Mont. 2016).
12. J. D’Elia, S. McCarthy, Bioscience 60, 751 (2010).
13. Center for Biological Diversity v. Everson, no. 15-CV-477,
2020 WL 437289 (D.D.C. 28 January 2020).
14. FWS, Fed. Regist. 79, 20074 (2014).
15. FWS, Fed. Regist. 85, 11297 (2020).

ACKNOWLEDGMENTS

We thank M. Bean for feedback on a draft of this manuscript.

10.1126/science.abb3806

666 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 sciencemag.org SCIENCE

Published by AAAS

Surpassing the expectations of its early critics,
Wikipedia is now the world’s leading encyclopedia.

dia has more than 31,000 active contributors,

yet only 11 language editions have more than

a thousand active contributors, and more

than half of the editions have fewer than 10.

Moreover, a recent Wikimedia Foundation

survey revealed that about 91% of Wikipedia

editors are male and 77% are white. As of late

2019, only 18% of biographies on Wikipedia

were about women. Far fewer were about

nonwhites. A number of nonmale and non-

white contributors to the book describe their

own, often unavailing, efforts to improve

these statistics.

There is also the tricky issue of determin-

ing the appropriate relationship that should

exist between Wikipedia’s language editions.

Each is written independently of the other

284 editions, although “a contributor may

consult an existing article in another lan-

guage edition when writing a new article,

or they might even use the content transla-

INFORMATION SCIENCE tion tool to help with translating one article

The ascent of Wikipedia to another language, but there is nothing to
ensure that articles in different language edi-
tions are aligned or kept consistent with each

Scholars reflect on 20 years of crowdsourced knowledge other,” notes Denny Vrandecˇic´, founder of
both Wikidata and the Croatian Wikipedia.

“This is often regarded as a contribution to

knowledge diversity since it allows every lan-

By Andrew Robinson The book’s 22 essays are wide-ranging, guage edition to grow independently of all

often intellectually engaging, and, in parts, other language editions,” he adds, begging

I n 2005—not long after the founding of stylishly written. Its 34 contributors include, the question: “Would creating a system that
Wikipedia by Jimmy Wales and Larry fittingly, academics and nonacademics based aligns the contents more closely with each
Sanger in early 2001—academic experts in many countries, although predominantly other sacrifice that diversity?”
commissioned to compare 42 articles in the United States. Its U.S.-based editors,
published in Encyclopaedia Britannica Joseph Reagle and Jackie Koerner, are (re- Ironically, one weakness of the book—com-
mon in edited collections—is the infrequency

and Wikipedia relating to science found spectively) a professor of communication of cross-referencing between articles. An-

an average of three errors in the Britannica studies and a qualitative research analyst other is the sweeping summary conclusion

entries and four in Wikipedia, suggesting a for online communities who also acts as the by Katherine Maher, executive director of the

comparable level of accuracy (1). Yet in 2007, community health consultant for Wikimedia Foundation, that “Wi-

Michael Gorman, former president of the the Wikimedia community. kimedia reminds us that the great-

American Library Association, argued scorn- Wales neither contributes an es- est thing we will ever build is the

fully that “A professor who encourages the say nor makes much of an appear- thing which we build with others.”

use of Wikipedia is the intellectual equivalent ance in the book, although he does This surely underestimates the ad-

of a dietician who recommends a steady diet provide a pithy blurb saluting the vances in human knowledge that

of Big Macs with everything” (2). Gorman’s “hard-won wisdom of its con- have come from solitary think-

article reflected the widespread skepticism at tributors, the novel reflections of ers (many of them specialists)—a

PHOTO: JOHN MACDOUGALL/AFP/GETTY IMAGES the time about the reliability of an encyclope- scholars, and the necessary provo- Wikipedia @ 20 universally popular part of Wiki-
dia that anyone can edit. cations of those working to shape Joseph Reagle and pedia’s entries—rather than from
[Wikipedia’s] next twenty years.” Jackie Koerner, editors collaborative groups. That said,
Today, Wikipedia is the world’s leading en- These provocations are examined MIT Press, 2020. 376 pp. anyone interested in the history,
cyclopedia. Every month, 1.5 billion unique

devices worldwide access it 15 billion times, in detail and range from what to current constitution, and possible

with more than 6000 page views per second. do about microaggressive community edit- future development of a singular contempo-

Meanwhile, Encyclopaedia Britannica—last ing of novice Wikipedia contributors to how rary global phenomenon will be stimulated

printed in 2010—is now “all but dead” online, Wikimedia, the nonprofit organization that by this anniversary collection. j

according to scholar Heather Ford in her es- hosts Wikipedia, might address the lack of REFERENCES AND NOTES
say in Wikipedia @ 20. reliable internet access experienced by four
billion people worldwide. 1. J. Giles, Nature 438, 900 (2005).
The reviewer is the author of The Last Man Who Knew 2. M. Gorman,“Jabberwiki: The Educational
Everything (Oneworld Publications, 2007) and Genius: Perhaps the most important internal con-
A Very Short Introduction (Oxford Univ. Press, 2011). troversy discussed is the bias of Wikipedia’s Response, Part II,”Encyclopaedia Britannica Blog
Email: [email protected] contributors and entries. The English Wikipe- (2007); http://blogs.britannica.com/2007/06/
jabberwiki-the-educational-response-part-ii/.

10.1126/science.abf2433

SCIENCE sciencemag.org 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 667

Published by AAAS

INSIGHTS | BOOKS

SCIENCE LIVES Rebels, Scholars, Explorers:
Women in Vertebrate
Recognizing the work of women Paleontology
Annalisa Berta and
Despite several stumbles, a new volume about women in Susan Turner
paleontology will likely prove valuable to future scholars Johns Hopkins University
Press, 2020. 344 pp.

By Jess Miller-Camp ralist Roy Chapman Andrews to ask if girls observations and advice from women such
as Margery Coombs, Catherine Badgley, and
could be paleontologists—and how she kept Romala Govender, as well as from male pa-
leontologists who have mentored women.
T he history of vertebrate paleontol- his encouraging reply as a treasured token. However, some interviewees aim for equal-
ogy, like that of other scientific dis- The inclusion of a chapter on modern in- ity rather than equity. Reading such pas-
ciplines, has traditionally been told sages was frustrating, but their inclusion
and shaped through a masculine fil- dividuals whose careers are not primarily in accurately reflects the prevalence of mis-
ter. Annalisa Berta and Susan Turner original research is refreshing, given aca- guided efforts at allyship. (This section of
demia’s general habit of ignoring such con- the book is presented without commentary
and is bound to spark some very good dis-
aim to rectify this bias, and their tributors. Included here are women such cussions in paleo reading groups.)

new book, Rebels, Scholars, Explorers, is a as Akiko Shinya, the chief vertebrate fossil As a book about the history of a field
whose infancy lies in the West, Rebels,
stepping stone along that path, synthesiz- preparator at the Field Museum, and Tsiory Scholars, Explorers has a largely Occi-
dental focus. Discussion of women in
ing observations about the past, present, Andrianavalona, who leads an outreach other theaters picks up, albeit inconsis-
tently, as the book proceeds forward in
and future of women’s contributions in the center in Madagascar called ExplorerHome time. The authors thoroughly cover the
scientific efforts of mid-20th-century
field. The book is the first major effort Chinese women, for example, but only
a single woman from and living in In-
to bring the work of several centuries’ dia—Sanjukta Chakravorti, a recent
graduate—is included.
worth of silenced people to light. Any
The book’s final chapter begins to ad-
such endeavor will inevitably have dress intersectionality by discussing the
additional challenges faced by women
gaps, but it will also serve as a refer- paleontologists who are also ethnic
minorities. Here, Anusuya Chinsamy-
ence for future projects—particularly Turan’s account of the restrictions placed
on her during South Africa’s apartheid
with regard to premodern individuals, was particularly poignant. However,
the authors’ handling of transgender
details about whom are often much issues, another intersectional identity,
is disappointing.
harder to track down.
Although they rightly include at least
Rebels, Scholars, Explorers can per- one trans woman in their account, they
also include James Robinson, who, prior
haps best be thought of as a three-part to his transition, studied plesiosaur
anatomy and behavior. One wonders
work. In the first section, the authors how he would feel about being referred
to by his pretransition name—a practice
offer a broad overview of the often known as deadnaming, which most who
transition consider to be disrespectful—
hostile climate within which women in and, more generally, about his inclusion in
a book about women. It is vital that anyone
vertebrate paleontology have long oper- studying or writing about gender seek out
noncisgendered perspectives, lest errors be
ated. In the second, they present short introduced and individuals harmed.
Despite these shortcomings, Rebels,
biographical sketches of a sampling of Scholars, and Explorers is a strong back-
bone upon which future scholarly work can
women throughout the field’s history. build. I look forward to seeing the rest of
the skeleton uncovered. j
In the third, they provide an assess-
10.1126/science.abe5779
ment of where things currently stand

and where we might go from here.

The book includes the contributions

of many early modern women I had

never heard of. Among them is Maria

Pavlova, who, although she was an emi-

nent Russian paleontologist and pro-

fessor in 1919, could do nothing when

a close colleague rejected her highly Avian paleontologist Hildegarde Howard examines bird bones

qualified student (a woman) for a pro- at the Natural History Museum of Los Angeles County. PHOTO: © NATURAL HISTORY MUSEUM OF LOS ANGELES COUNTY

fessional position. In her memoir, Pav-

lova wrote of the incident, “I’m feeling as if that seeks to inspire scientific curiosity in

I returned from a very hard funeral.” Malagasy students.

A number of the biographical sketches It was incredible and heartening to see,

also contain anecdotal gems. Taphonomist throughout the book, so many citation-

Kay Behrensmeyer’s, for example, references rich sections exclusively referencing works

her nonchalance about a venomous green led by women. The authors’ account of

mamba at her field site in Cameroon. And vertebrate paleontology in the Soviet

Elizabeth (Betsy) Nicholls’s entry notes how, Union, for example, discusses the work of

at the age of 12, she wrote to renowned natu- a host of women studying Paleozoic fishes.

Such passages make stark the extent to

The reviewer is at the Department of Earth and Atmospheric which the contributions of women are
Sciences, Indiana University Bloomington, Bloomington, often overlooked.
IN 47405, USA. Email: [email protected]
The book’s interviews contain insightful

668 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 sciencemag.org SCIENCE

Published by AAAS

LETTERS

The Oriental stork (Ciconia boyciana) is threatened by human activities in its migratory stopover points in China.

PHOTO: MARTIN HALE/FLPA/SCIENCE SOURCE Edited by Jennifer Sills and prevents them from finding enough REFERENCES AND NOTES
food (4). As a result, the storks relocate
Aquaculture jeopardizes to private fishponds, where they face an 1. CITES,“Appendices”(2020); https://cites.org/eng/
increased risk of poisoning and poaching. In app/appendices.php.
migrating Oriental storks 2019, 19 storks were poisoned in the Qilihai
and Caofeidian wetlands (8). 2. BirdLife International,“Ciconia boyciana”(IUCN Red List
The Oriental stork (Ciconia boyciana), of Threatened Species, 2018).
once the most common bird of the Far The Oriental stork has been catego-
East, is now listed in Appendix I of the rized as a terrestrial species under state 3. Y.Yamada et al., Ecol. Res. 34, 277 (2019).
Convention on International Trade in protection (with a beneficial, economic, 4. IUCN Commission on Environmental, Economic,
Endangered Species of Wild Fauna and or scientific value) since 2000 (9), but
Flora (CITES) and classified as Endangered the species’ extremely limited population and Social Policy,“A reflection on protected areas in
on the International Union for Conservation size indicates that this designation is not serving wildlife migration: Endangered Oriental storks”
of Nature’s (IUCN’s) Red List (1, 2). Over enough. To better protect the Oriental (2019).
the past few decades, illegal poaching, stork, the Chinese government is cur- 5. W. Peng et al., Int.J. Ecol. 9, 108 (2020) [in Chinese].
habitat loss, and environmental pollution rently updating the special state protection 6. Z.J.Zhao, Avifauna of China (Jilin Science and
have caused a decline in the Oriental stork list and changing the protection of this Technology Press, vol. 1, 2001) [in Chinese].
population in its Northeast Asian breeding bird to the highest first-class level (10). 7. “Ninety percent of Caofeidian wetland was outsourced
grounds (3). Fewer than 3000 individu- In addition, immediate habitat restora- and turned into fishponds”[China Biodiversity
als remained worldwide by 2018 (2). The tion is required. Fishponds in protected Conservation and Green Development Foundation
Oriental stork now faces a severe survival areas must be restored to natural wet- (CBCGDF), 2019].
threat at migratory stopover sites in China’s lands to create favorable living conditions 8. “In-depth analysis of‘murder’on the journey: What’s
Bohai coastal region, where human distur- and reverse population decline. Local behind the continuous death of Oriental white stork? Is
bances drive habitat degradation (4). governments should rapidly formulate it a‘gang’crime?”(CBCGDF, 2019); www.cbcgdf.org/
eco-compensation measures and publicize NewsShow/4854/10817.html [in Chinese].
The Qilihai and Caofeidian wetland wildlife protection to mediate human-bird 9. National Forestry and Grassland Administration,
reserves, located north of the Bohai Bay, are conflicts. Only by taking action to protect Government of China,“Lists of terrestrial wildlife under
the most important stopover sites for the this species and its habitat can we prevent state protection, which are beneficial or of important
Oriental stork (5). More than 2000 individu- its looming extinction. economic or scientific value”(2000); www.forestry.gov.
als refuel in these wetlands during their cn/main/3954/content-959027.html [in Chinese].
fall migration (6). However, large areas of Yanfeng Sun1,2, Liqiang Du3, Yuan Yin2, 10. National Forestry and Grassland Administration,
these reserves (including about 80 to 90% Yuefeng Wu2, Aijun Cai3, Dongming Li2* Government of China,“List of wildlife under special
of the Caofeidian wetland) have been leased 1Ocean College, Hebei Agricultural University, state protection (draft)”(2020); www.forestry.gov.cn/
to aquacultural farmers to create fishponds Qinhuangdao 066000, China. 2Key Laboratory of main/153/20200619/092731170435586.html
(7). The farmers dislike foraging storks and Animal Physiology, Biochemistry and Molecular [in Chinese].
often try to scare them away with fire- Biology of Hebei Province, College of Life
crackers (4). For aquaculture, wetlands are Sciences, Hebei Normal University, Shijiazhuang 10.1126/science.abf2089
maintained at a relatively high water level, 050024, China. 3College of Marine Resources &
which makes foraging difficult for storks Environment, Hebei Normal University of Science Indigenous rights to
& Technology, Qinhuangdao 066600, China.
*Corresponding author. Patagonia’s Guafo island
Email: [email protected]
In September, private investors put

20,000-ha Guafo island up for sale for

US $20 million (1). The island, located in

northern Chilean Patagonia, is a strong-

hold of unique biodiversity (2, 3) and a

biocultural heritage site for Patagonia

Indigenous groups and the country (4).

The owners bought the island a decade

SCIENCE sciencemag.org 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 669

Published by AAAS

INSIGHTS | LETTERS

ago with plans to conduct coal mining by Indigenous communities from nearby economic security for hundreds of mil-
operations (1), but after Chile made a lions of people (2). Historical marsh
climate change commitment to become Chiloé island (12), the “Wafo Wapi ances- losses coupled with increasing pressures
carbon neutral by 2050 (5), the difficulty from coastal development and climate
obtaining mining permits made them tral land for conservation.” The Chilean change place these intertidal ecosystems
rethink their investment. The Chilean and surrounding uplands under growing
government should protect these valuable government should support this claim. threat (3). Preventing further losses of salt
ecosystems by deeding the island to the marshes and associated fisheries produc-
Indigenous people who claim it. Pablo A. Marquet1,2*, Juan Carlos Castilla1, tion will require greater public awareness
Aurora Gaxiola1,2, Rodrigo Hucke-Gaete3, and difficult choices in coastal policy and
The challenges facing Guafo island are Alfredo Pena-Vega4 management, underpinned by greater
emblematic of environmental problems 1Departamento de Ecología, Facultad de Ciencias understanding of marsh function.
throughout Patagonia. A growing exotic Biológicas, Pontificia Universidad Católica de
salmon aquaculture industry has brought Chile, CP 8331150, Santiago, Chile. 2Instituto Quantifying the value of salt marsh habi-
about environmental degradation (6). de Ecología y Biodiversidad (IEB), Santiago, tat to fisheries production is challenging.
Climate change–induced drought has Chile. 3Programa Austral Patagonia, Instituto de Many fisheries species feed and shelter in
led to harmful algal blooms (6, 7) that Ciencias Marinas y Limnológicas, Universidad the salt marsh only as juveniles, and it is dif-
may have contributed to the stranding Austral de Chile, Campus Isla Teja, Valdivia, Chile. ficult to assess the marsh’s effect once they
of hundreds of endangered Sei whales 4Ecole des Hautes Etudes en Sciences Sociales/ have moved to a new location (1). It is also
(8). Terrestrial ecosystems face increas- Centre National de la Recherche Scientifique unclear how marsh landscape fragmentation
ing tensions from tourist developments, Institut Interdisciplinaire d’Anthropologie du under sea level rise will affect fisheries; it
a growing human population, peat bog Contemporain, Paris, France. may boost fishery production, at least tem-
degradation, exotic species invasion, and *Corresponding author. Email: [email protected] porarily (4), but it could also disrupt food
climate change (6), which threatens gla- web processes that support fisheries (5).
cial freshwater reserves (9) and increases REFERENCES AND NOTES
the likelihood of fires (6). Projections of marsh expansion offer hope
1. D. Collyns,“Activists outraged that sacred Chilean island (6) but are largely dependent on changes
Disrespecting Indigenous peoples’ heri- is listed for sale for $20m,”The Guardian (2020). in coastal watershed management. For
tage in Patagonia threatens the region’s instance, human development may prevent
biodiversity. Degrading the capacity of car- 2. R. Hucke-Gaete, L. P. Osman, C.A. Moreno, K. P. Findlay, marshes from migrating upland with sea
bon sequestration in forest soils, peatbogs, D. K. Ljungblad, Proc. R. Soc. London Ser. B. 271, level rise and thus lead to marsh drowning
and kelp forests (6) and disrupting the S170 (2004). (7). Adequate sediment supply is also essen-
carbon sequestration processes fostered tial for marsh resilience, but many coastal
by large whales and other marine verte- 3. R. Reyes-Arriagada, P. Campos-Ellwanger, R. P. Schlatter, areas in the world are sediment-starved
brates (10) will initiate a perfect storm of C. Baduini, Biodivers Conserv. 16, 913 (2007). (8). Much effort has been made to restore
increasing warming and ecosystem deg- natural riverine flow and other sources of
radation with global consequences. It is 4. R.Álvarez, M. Navarro, in Conservando el Mar de Chiloé, sediment delivery into marshes, although
incumbent upon the Chilean government Palena, y Guaitecas, R. Hucke-Gaete, P. Lo Moro,J. Ruiz, such efforts may have negative impacts on
to set an example for Patagonian policy by Eds. (Universidad Austral de Chile, 2010), pp. 65–123 the very fisheries these marshes support (9).
protecting Guafo island and its surround- [in Spanish].
ing seascapes, requiring that the salmon To design effective policies for salt
industry withdraw operations from 5. Climate Action Tracker, Chile, Pledges and Targets marsh restoration and conservation that
protected waters, and giving Indigenous (2020); https://climateactiontracker.org/countries/ protect fisheries production, we need to
people the rights to their ancestral lands. chile/pledges-and-targets/. better understand the role of salt marshes.
In 2008, Chile passed the Mapuche- Researchers should continue to explore the
Lafkenche Marine and Coastal Areas for 6. P.A. Marquet et al., Eds.,“Biodiversidad y cambio fundamental linkages between salt marshes
Indigenous Peoples (MCAIP) law (11). climático en Chile: Evidencia científica para la toma de and fisheries (10), the marsh habitat value
The legislation enables the allocation and decisiones”(Comité Científico COP25; Ministerio de within the context of the interconnected
administration of coastal marine areas to Ciencia,Tecnología, Conocimiento e Innovación, 2019) and increasingly urbanized mosaic of
Indigenous communities, who can ensure [in Spanish]. coastal ecosystems, and the value of salt
the sustainability and conservation of marshes created by upland transgression
marine resources and ecosystems. There is 7. J. León-Muñoz, M.A. Urbina, R. Garreaud,J. L. Iriarte, and active engineering. Restoration and
already an MCAIP claim for Guafo island Sci. Rep. 8, 1330 (2018). conservation planning must take a long-
term view that specifically recognizes sea
8. V. Häussermann et al., PeerJ. 5, e3123 (2017). level rise and its interaction with other
9. M. Rodell et al., Nature 557, 651 (2018). anthropogenic stressors.
10. S. Lutz, R. Barnes,T. Kurvitis,“Fish carbon: Exploring
Ronald Baker1*, Matthew D. Taylor2, Kenneth W.
marine vertebrate carbon services”(GRID-Arendal, Able3, Michael W. Beck4, Just Cebrian5, Denise D.
Arendal, Norway, 2014), p. 36. Colombano6, Rod M. Connolly7, Carolyn Currin8,
11. L. Hiriart-Bertrand,J. Silva, S. Gelcich, Ocean Coast. Linda A. Deegan9, Ilka C. Feller10, Ben L. Gilby11,
Manag. 193, 105233 (2020). Matthew E. Kimball12, Thomas J. Minello13,
12. F.Araos et al., Coast. Manag. 48, 289 (2020). Lawrence P. Rozas14, Charles Simenstad15, R.
Eugene Turner16, Nathan J. Waltham17, Michael
10.1126/science.abf1962 P. Weinstein18, Shelby L. Ziegler19, Philine S.E. zu
Ermgassen20, Caitlin Alcott21, Scott B. Alford22,
Fisheries rely on Myriam A. Barbeau23, Sarah C. Crosby24, Kate
Dodds25, Alyssa Frank1, Janelle Goeke26, Lucy
threatened salt marshes

Salt marsh ecosystems and the seascapes

in which they are embedded serve as

critical habitats for species harvested

by fisheries (1), which provide food and

NEXTGEN VOICES: SUBMIT NOW

Defining events of 2020

Add your voice to Science! Our new NextGen Voices survey is now open:
What new word or phrase would you add to the dictionary to help scientists explain the events of
2020 to future generations?

To submit, go to www.sciencemag.org/nextgen-voices
Deadline for submissions is 20 November. A selection of the best responses will be published in
the 1 January 2021 issue of Science. Anonymous submissions will not be considered.

670 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 sciencemag.org SCIENCE

Published by AAAS

A. Goodridge Gaines11, Felicity E. Hardcastle11, Marine Field Laboratory, University of South Allison University, Sackville, NB E4L 1E4, Canada.
Carolina, Georgetown, SC 29442, USA. 13NOAA 31Louisiana Coastal Protection and Restoration
Christopher J. Henderson11, W. Ryan James27, Fisheries, Southeast Fisheries Science Center, Authority, Baton Rouge, LA 70802, USA. 32Institute
Galveston, TX 77551, USA. 14NOAA Fisheries, of Environment, Florida International University,
Matthew D. Kenworthy28, Justin Lesser27, Debbrota Estuarine Habitats and Coastal Fisheries Center, Miami, FL 33199, USA. 33NOAA Fisheries,
Lafayette, LA 70506, USA. 15School of Aquatic Restoration Center, Silver Spring, MD 20910,
Mallick1, Charles W. Martin22, Ashley E. McDonald26, and Fishery Sciences, University of Washington, USA. 34Department of Earth and Environment,
Seattle, WA 98195–5020, USA. 16Department of Institute of Environment, Florida International
Catherine McLuckie29, Blair H. Morrison1, James Oceanography and Coastal Sciences, Louisiana University, Miami, FL 33199, USA. 35University of
State University, Baton Rouge, LA 70803, USA. Georgia Marine Extension and Georgia Sea Grant,
A. Nelson27, Gregory S. Norris23, Jeff Ollerhead30, 17Centre for Tropical Water and Aquatic Ecosystem Athens, GA 30602, USA. 36U.S. Fish and Wildlife
Research, and Marine Data Technologies Hub, Service, Galloway, NJ, 08205, USA. 37Coastal
James W. Pahl31, Sarah Ramsden1, Jennifer S. College of Science and Engineering, James Research and Extension Center, Mississippi State
Cook University, Townsville, QLD, 4811, Australia. University, Biloxi, MS 39532, USA. 38Mississippi
Rehage32, James F. Reinhardt33, Ryan J. Rezek34, 18New Jersey Marine Sciences Consortium, Alabama Sea Grant Consortium, Ocean Springs,
Fort Hancock, Sandy Hook, NJ 07043, USA. MS 39564, USA. 39University of Maryland Center
L. Mark Risse35, Joseph A.M. Smith36, Eric L. 19Moss Landing Marine Laboratories, Moss for Environmental Science, Horn Point Laboratory,
Landing, CA 95039, USA. 20Changing Oceans Cambridge, MD 21617, USA.
Sparks37,38, Lorie W. Staver39 Group, School of Geosciences, Grant Institute, *Corresponding author. Email: [email protected]
1Department of Marine Sciences, University University of Edinburgh, EH9 3FE, UK. 21Inter-
of South Alabama, Dauphin Island Sea Lab, fluve, Hood River, OR 97031 USA. 22University REFERENCES AND NOTES
Dauphin Island, AL 36528 USA. 2Port Stephens of Florida, Institute of Food and Agricultural
Fisheries Institute, New South Wales Department Sciences, Nature Coast Biological Station, 1. M.W. Beck et al., Bioscience 51, 633 (2001).
of Primary Industries, Nelson Bay, NSW 2315, University of Florida, Cedar Key, FL 32625 USA. 2. J. C. Rice, S. M. Garcia, ICES J. Mar. Sci. 68, 1343 (2011).
Australia. 3Department of Marine and Coastal 23Department of Biology, University of New 3. K. B. Gedan, B. R. Silliman, M. D. Bertness, Annu. Rev.
Sciences, Rutgers, State University of New Brunswick, Fredericton, NB E3B 5A3, Canada.
Jersey, New Brunswick, NJ 08901, USA. 4Institute 24Harbor Watch, Earthplace, Inc., Westport, Mar. Sci. 1, 117 (2009).
of Marine Sciences, University of California, CT 06880, USA. 25Department of Biological 4. E.J. Chesney, D. M. Baltz, R. G.Thomas, Ecol.Appl. 10,
Santa Cruz, CA 95062, USA. 5Northern Gulf Sciences, Macquarie University, Sydney, NSW
Institute, Mississippi State University, Stennis 2109, Australia. 26Department of Marine Biology, 350 (2000).
Space Center, MS 39529, USA. 6Department of Texas A&M University at Galveston, Galveston, TX 5. G.A. Hyndes et al., Biol. Rev. 89, 232 (2014).
Environmental Science, Policy, and Management, 77554, USA. 27Department of Biology, University 6. M. Schuerch et al., Nature 561, 231 (2018).
University of California, Berkeley, Berkeley, CA of Louisiana at Lafayette, Lafayette, LA 70504, 7. J. Fitzsimons, M.W. Beck, L. Hale, K. Leo, C. Gillies, Ocean
94720, USA. 7Australian Rivers Institute–Coast USA. 28Department of Marine and Environmental
& Estuaries, School of Environment and Science, Sciences, Savannah State University, Savannah, Coast. Manag. 175, 180 (2019).
Griffith University, Gold Coast, QLD 4222, GA 31404, USA. 29Department of Environmental 8. M.L.Kirwan et al.,Geophys.Res.Lett.37,L23401 (2010).
Australia. 8National Oceanic and Atmospheric Science and Management, University of 9. T.J. Mozdzer, E. B.Watson,W. H. Orem, C. Swarzenski, R.
Administration (NOAA) National Centers for Newcastle, Ourimbah, NSW 2258, Australia.
Coastal Ocean Science, Beaufort, NC 28516, 30Geography and Environment Department, Mount E.Turner, Sci.Tot. Environ. 743, 140420 (2020).
USA. 9Woodwell Climate Research Center, 10. J. S. Lefcheck et al., Conserv. Lett. 12, e12645, (2019).
Falmouth, MA 02540, USA. 10Smithsonian
Environmental Research Center, Edgewater, 10.1126/science.abe9332
MD 21037, USA. 11School of Science and
Engineering, University of the Sunshine Coast,
Maroochydore, QLD 4558, Australia. 12Baruch

ScienceSignaling.org

PUT YOUR
RESEARCH
OUT IN FRONT

Submit your research: cts.ScienceMag.org

Twitter: @SciSignal
Facebook: @ScienceSignaling

Published by AAAS

SPECIAL SECTION

SAMPLING THE EARLY

SOLAR SYSTEM
SCIENCE RESEARCH ARTICLES
Variations in color and refectance on the surface of asteroid (101955) Bennu p. 674
Widespread carbon-bearing materials on near-Earth asteroid (101955) Bennu p. 675
Bright carbonate veins on asteroid (101955) Bennu: Implications for aqueous alteration history p. 676

SCIENCE ADVANCES RESEARCH ARTICLES
Heterogeneous mass distribution of the rubble-pile asteroid (101955) Bennu 10.1126/sciadv.abc3350
Hemispherical diferences in the shape and topography of asteroid (101955) Bennu 10.1126/sciadv.abd3649
Asteroid (101955) Bennu’s weak boulders and thermally anomalous equator 10.1126/sciadv.abc3699

By Keith T. Smith1 and Kip V. Hodges2

O ur knowledge of the Solar System has Earth in December 2020. Meanwhile, on 31 Decem- PHOTO: NASA/GODDARD/UNIVERSITY OF ARIZONA
been greatly advanced by exploration ber 2018, the OSIRIS-REx (Origins, Spectral Inter-
with robotic spacecraft, but there are pretation, Resource Identification, and Security–
many limitations on the instruments Regolith Explorer) spacecraft arrived at another
those can carry. More detailed infor- primitive asteroid, (101955) Bennu, with plans to
mation can be extracted by analyzing return at least 60 grams of material.
samples of Solar System bodies in Earth
laboratories. Meteorites provide some Writing in Science and Science Advances, mem-
natural samples, but the body they came bers of the OSIRIS-REx team present results from
from is often unknown, and they may not repre- the survey and reconnaissance phases of the mis-
sent typical material. Recent years have seen in- sion. Detailed maps of surface properties were
creased interest in directly retrieving samples from used to identify promising sites for sample col-
other worlds and bringing them back to Earth, a lection and provide the necessary scientific con-
process known as sample return. text. These data provide information on Bennu’s
composition, constrain its formation process, and
The most primitive carbonaceous asteroids pre- show how its surface evolved. They show that
serve information about the formation and early Bennu’s surface material has been modified by
evolution of the Solar System and thus have been exposure to space weathering, contains abundant
a high priority for sample return. The Hayabusa organic material, and has evidence of past altera-
mission collected 1500 dust particles from aster- tion by liquid water. OSIRIS-REx successfully col-
oid (25143) Itokawa and returned them to Earth lected its sample of Bennu on 20 October 2020; it
in 2010. A successor mission, Hayabusa2, visited is due to arrive on Earth in 2023.
asteroid (162173) Ryugu with the goal of obtaining
a larger mass of sample, which is due to arrive on 1Senior Editor, Science. 2Deputy Editor, Science Advances.

672 6 NOVEMBER 2020 • VOL 370 ISSUE 6517 sciencemag.org SCIENCE

Published by AAAS

SCIENCE sciencemag.org The sample site on Bennu, nicknamed
Nightingale. OSIRIS-REx collected

material from within the blue circle.

6 NOVEMBER 2020 • VOL 370 ISSUE 6517 673

Published by AAAS

SURVEYING BENNU

◥ heterogeneity and fall into distinct popula-
tions on the basis of reflectance. Dark boulders
RESEARCH ARTICLE SUMMARY

(reflectance of 0.034 to 0.049, encompassing

ASTEROIDS Bennu’s average reflectance of 0.044) tend

Variations in color and reflectance on the surface of to be rougher and rounder, whereas bright
boulders (0.049 to 0.074) are smoother and

asteroid (101955) Bennu more angular. Variation in color within indi-
vidual boulders is also apparent; for example,

boulder faces that appear to be more recently

D. N. DellaGiustina*, K. N. Burke, K. J. Walsh, P. H. Smith, D. R. Golish, E. B. Bierhaus, R.-L. Ballouz, exposed owing to fracturing are bluer than

T. L. Becker, H. Campins, E. Tatsumi, K. Yumoto, S. Sugita, J. D. Prasanna Deshapriya, E. A. Cloutis, putatively older faces. Conversely, small red-

B. E. Clark, A. R. Hendrix, A. Sen, M. M. Al Asad, M. G. Daly, D. M. Applin, C. Avdellidou, M. A. Barucci, dish craters are observed to overlie blue cra-

K. J. Becker, C. A. Bennett, W. F. Bottke, J. I. Brodbeck, H. C. Connolly Jr., M. Delbo, J. de Leon, ters, indicating that the former are younger

C. Y. Drouet d’Aubigny, K. L. Edmundson, S. Fornasier, V. E. Hamilton, P. H. Hasselmann, (more recently exposed material). Bennu’s

C. W. Hergenrother, E. S. Howell, E. R. Jawin, H. H. Kaplan, L. Le Corre, L. F. Lim, J. Y. Li, P. Michel, smallest craters have a size distribution that

J. L. Molaro, M. C. Nolan, J. Nolau, M. Pajola, A. Parkinson, M. Popescu, N. A. Porter, B. Rizk, indicates that they are also the youngest,

J. L. Rizos, A. J. Ryan, B. Rozitis, N. K. Shultz, A. A. Simon, D. Trang, R. B. Van Auken, and they are redder than the average sur-

C. W. V. Wolner, D. S. Lauretta face. Many of the larger (older) craters have

colors indistinguishable from Bennu’s av-

erage. Crater spectral slopes indi-

INTRODUCTION: The color and reflec- cate that terrains with intermediate

tance of asteroids can be used to infer N ages have the bluest near-ultraviolet
their compositions and histories. Var- spectral slopes.
iations in these spectrophotometric

properties are driven by differences CONCLUSION: The differences in re-

in lithology and/or exposure to pro- flectance and texture among boul-

cesses collectively known as space ders indicate that Bennu may have

weathering (bombardment by mete- inherited distinct lithologies formed

oroids and solar wind ions). On an- at different depths in its larger pro-

hydrous bodies, such as the Moon genitor asteroid, as well as debris

and S-type asteroids, space weath- from impactors. The color variations

ering darkens and reddens spectral within boulders and among craters

slopes (where “redder” indicates a suggest that space weathering on

more positive slope relative to the Bennu does not drive a unidirectional

solar spectrum) in the visible wave- progression from red to blue (or vice

lengths. However, on primitive C- versa). Rather, freshly exposed redder

complex asteroids—bodies that may surfaces, as exemplified by the small

have delivered water and organics reddish craters, initially brighten in

to early Earth—the spectral changes the near-ultraviolet region (i.e., be-

that result from space weathering are come blue at shorter wavelengths),

not well understood. Evidence from 20 m as exemplified by blue crater rims and
meteorites thought to be analogous fractured boulder faces. Brighten-

to C-complex asteroids suggests that ing in the visible to near-infrared

either reddening or bluing is pos- False-color image mosaic of rubble on asteroid Bennu, as observed wavelengths follows, ultimately lead-

sible. Deciphering such changes is with the MapCam multispectral imager. Color and reflectance vary ing to more moderately blue spec-

necessary to understand the origin between and within boulders, resulting from different exposure ages and tral slopes, consistent with Bennu’s

and relative exposure age of sur- innate compositions. Red is the x/v band ratio (indicating redder spectral average. The time scale associated

face units on primitive Solar Sys- slopes), green represents relative change in the w band (an indication with space weathering–induced color

tem objects. of composition), and blue is the b′/v band ratio (indicating bluer spectral changes (~105 years) is compatible

slopes in the near-ultraviolet region). with previous findings only if Bennu’s

RATIONALE: The MapCam imager on small reddish craters formed under

the OSIRIS-REx (Origins, Spectral Inter- tance at a pixel scale of ~25 cm. In combina- conditions in which gravity, rather than the

pretation, Resource Identification, and tion with higher-resolution (~5 cm per pixel) strength of the impacted surface, is the dom-

Security–Regolith Explorer) spacecraft panchromatic PolyCam images, we assessed inant influence. This finding offers an indica-

acquired global multispectral images of relationships between MapCam spectra and ▪tion of cratering physics on small rubble-pile
the C-complex asteroid (101955) Bennu in morphologic features on Bennu’s surface, aim-
four bands: b′ (0.44 to 0.50 mm), v (0.52 to ing to understand sources of variation from asteroids.

0.58 mm), w (0.67 to 0.73 mm), and x (0.82 to the average and determine the relative timing

0.89 mm). Bennu is a rubble pile, made up of associated with color differences. The list of author affiliations is available in the full article online.
the reaccumulated fragments of a larger C- *Corresponding author. Email: [email protected]
complex progenitor that was blown apart by RESULTS: The surface of Bennu has unexpect- Cite this article as D. N. DellaGiustina et al., Science 370,
a catastrophic impact. edly heterogeneous colors distributed on a mod- eabc3660 (2020). DOI: 10.1126/science.abc3660

Using band ratios and principal components erately blue (gently negatively sloped) global READ THE FULL ARTICLE AT

analysis, we mapped Bennu’s color and reflec- surface. Boulders are the dominant source of https://doi.org/10.1126/science.abc3660

DellaGiustina et al., Science 370, 674 (2020) 6 November 2020 1 of 1

SURVEYING BENNU

◥ Although the initial composition of an as-
teroid influences its global colors, physical prop-
RESEARCH ARTICLE erties such as particle size, surface roughness,
and porosity can also influence these spectral
ASTEROIDS characteristics, as can duration of exposure to
the space environment. The surface colors of
Variations in color and reflectance on the surface of airless bodies are expected to be heavily al-
asteroid (101955) Bennu tered by space weathering processes (12, 13),
including bombardment by solar wind partic-
D. N. DellaGiustina1,2*, K. N. Burke1, K. J. Walsh3, P. H. Smith1, D. R. Golish1, E. B. Bierhaus4, les and meteoroids. On anhydrous planetary
R.-L. Ballouz1, T. L. Becker1, H. Campins5, E. Tatsumi6,7, K. Yumoto7, S. Sugita7, surfaces, such as the Moon and stony (S-type)
J. D. Prasanna Deshapriya8, E. A. Cloutis9, B. E. Clark10, A. R. Hendrix11, A. Sen10, M. M. Al Asad12, asteroids, space weathering darkens and red-
M. G. Daly13, D. M. Applin9, C. Avdellidou14, M. A. Barucci8, K. J. Becker1, C. A. Bennett1, W. F. Bottke3, dens spectral slopes in the visible and near-
J. I. Brodbeck1, H. C. Connolly Jr.15, M. Delbo14, J. de Leon6, C. Y. Drouet d’Aubigny1, K. L. Edmundson1, infrared region (12, 14). However, on primitive
S. Fornasier8,16, V. E. Hamilton3, P. H. Hasselmann8, C. W. Hergenrother1, E. S. Howell1, E. R. Jawin17, carbonaceous asteroids such as Bennu, and
H. H. Kaplan18, L. Le Corre11, L. F. Lim17, J. Y. Li11, P. Michel14, J. L. Molaro11, M. C. Nolan1, J. Nolau4, their meteorite analogs, space weathering ef-
M. Pajola19, A. Parkinson9, M. Popescu20,6, N. A. Porter1, B. Rizk1, J. L. Rizos6, A. J. Ryan1, B. Rozitis21, fects are not well understood. Measured colors
N. K. Shultz1, A. A. Simon18, D. Trang22, R. B. Van Auken1, C. W. V. Wolner1, D. S. Lauretta1 of primitive asteroids do not show consistent
spectral relationships with surface exposure
Visible-wavelength color and reflectance provide information about the geologic history of planetary age (13, 15–17), nor do laboratory experiments
surfaces. Here we present multispectral images (0.44 to 0.89 micrometers) of near-Earth asteroid of simulated space weathering on analogous
(101955) Bennu. The surface has variable colors overlain on a moderately blue global terrain. Two meteorite and phyllosilicate samples: Some
primary boulder types are distinguishable by their reflectance and texture. Space weathering of studies indicate that space weathering leads
Bennu surface materials does not simply progress from red to blue (or vice versa). Instead, freshly to bluing (13, 18–22), but others find that it
exposed, redder surfaces initially brighten in the near-ultraviolet region (i.e., become bluer at shorter leads to reddening (16, 20, 23, 24). This is likely
wavelengths), then brighten in the visible to near-infrared region, leading to Bennu’s moderately because the initial composition and the phys-
blue average color. Craters indicate that the time scale of these color changes is ~105 years. We ical structure of the materials play a role in the
attribute the reflectance and color variation to a combination of primordial heterogeneity and varying spectral changes observed (16, 20). To deter-
exposure ages. mine how space weathering affects low-albedo
carbonaceous asteroids, we searched for a cor-
T he near-Earth asteroid (101955) Bennu telescopic observations of Bennu had identi- relation between Bennu’s colors and the age of
is the target of the OSIRIS-REx (Origins, fied it as a low-albedo object—potentially in- its surface features determined from morphol-
dicating a carbon-rich composition—with a ogy. The spatial distribution and geologic set-
Spectral Interpretation, Resource Identi- featureless, gently blue spectrum (blue sig- ting of varying colors on Bennu may also aid
nifies a negative spectral slope with respect our understanding of the composition and
fication, and Security–Regolith Explorer) evolution of the asteroid’s surface.
sample-return spacecraft (1). Before launch, to the solar spectrum, whereas red signifies a
positive slope). This resulted in its classifica- Color observations of Bennu
1Lunar and Planetary Laboratory, University of Arizona, tion as a blue (B-type) asteroid (2), a subclass
Tucson, AZ, USA. 2Department of Geosciences, University of of the broader carbonaceous (C-complex) group OSIRIS-REx obtained color observations of
Arizona, Tucson, AZ, USA. 3Southwest Research Institute, Bennu during two hyperbolic flybys on 14 March
Boulder, CO, USA. 4Lockheed Martin Space, Littleton, CO, of small bodies. Bennu is a rubble-pile asteroid and 26 September 2019, as part of the Baseball
USA. 5Department of Physics, University of Central Florida, (3–6), accumulated from fragments of a larger Diamond campaign of the mission’s Detailed Sur-
Orlando, FL, USA. 6Instituto de Astrofísica de Canarias and parent body that was shattered by a catastro- vey (25). The OSIRIS-REx Camera Suite (OCAMS)
Departamento de Astrofísica, Universidad de La Laguna, phic impact in the inner main asteroid belt ~1 (26) acquired color images using the multi-
Tenerife, Spain. 7Department of Earth and Planetary Science, billion years ago (3). Bennu eventually mig- spectral MapCam imager, which has four bands
University of Tokyo, Tokyo, 113-0033, Japan. 8LESIA rated from the main belt into its current orbit in the visible (VIS; 0.40 to 0.70 mm) and near-
(Laboratoire d’Etudes Spatiales et d’Instrumentation en in near-Earth space (3). infrared (NIR; 0.70 to 2.5 mm) wavelengths. The
Astrophysique), Observatoire de Paris, Université PSL (Paris MapCam bands—b′ (0.44 to 0.50 mm), v (0.52 to
Sciences & Lettres), CNRS (Centre National de la Recherche OSIRIS-REx measurements acquired during 0.58 mm), w (0.67 to 0.73 mm), and x (0.82 to
Scientifique), Université de Paris, Sorbonne Université, 92195 0.89 mm)—are similar to those used by tele-
Meudon, France. 9Department of Geography, University of the initial phases of the mission showed that scopic surveys (27) to infer asteroid com-
Winnipeg, Winnipeg, MB R3B 2E9, Canada. 10Department of Bennu is dominated by hydrated clay-bearing position and classify their spectra (28). Most
Physics and Astronomy, Ithaca College, Ithaca, NY, USA. minerals (phyllosilicates) and magnetite (7), asteroid observations have been limited to
11Planetary Science Institute, Tucson, AZ, USA. 12Department indicating that water was present on and al- unresolved disk-integrated (globally averaged)
of Earth, Ocean and Atmospheric Sciences, University of tered the composition of Bennu’s parent body spectra. We used spatially resolved MapCam
British Columbia, Vancouver, BC, Canada. 13The Centre for (aqueous alteration). Organic compounds and color images (pixel scale ~25 cm) to investigate
Research in Earth and Space Science, York University, reflectance and color across Bennu’s surface.
Toronto, ON, Canada. 14Université Côte d’Azur, Observatoire carbonates have been discovered across the To establish relationships between color and
de la Côte d’Azur, CNRS, Laboratoire Lagrange, Nice, France. asteroid’s surface, supporting the hypothesis surface morphology, we paired these color ob-
15Department of Geology, Rowan University, Glassboro, NJ, that B-type asteroids are carbon rich (8, 9). servations with higher-resolution OCAMS PolyCam
USA. 16Institut Universitaire de France (IUF), 1 rue Descartes, Carbon-bearing species are optically opaque panchromatic images (2 to 5 cm per pixel) of
75231 Paris CEDEX 05, France. 17Smithsonian Institution the same locations.
National Museum of Natural History, Washington, DC, USA. (as is magnetite) and thus could be respon-
18NASA Goddard Space Flight Center, Greenbelt, MD, USA. sible for Bennu’s low global normal albedo of We radiometrically calibrated the MapCam
19Istituto Nazionale di Astrofisica (INAF), Osservatorio 0.044 (4, 10). These findings suggest that and PolyCam images to units of reflectance (also
Astronomico di Padova, Padua, Italy. 20Astronomical Institute Bennu’s composition may be representative of
of the Romanian Academy, Bucharest, Romania. 21The the primitive bodies that delivered water and
School of Physical Sciences, The Open University, Milton organic molecules to early Earth (11).
Keynes, UK. 22University of Hawai‘i at Mānoa, Hawai‘i
Institute of Geophysics and Planetology, Honolulu, HI, USA.

*Corresponding author. Email: [email protected]

DellaGiustina et al., Science 370, eabc3660 (2020) 6 November 2020 1 of 12

RESEARCH | SURVEYING BENNU

known as radiance factor or I/F) (29). MapCam assess albedo differences across the surface principal components analysis (PCA) were used
images were corrected to normal viewing con- (30, 31). We subsequently map-projected and to identify variations in multispectral images
ditions (0° solar incidence, 0° solar phase, and mosaicked the MapCam images using carto- and distinguish regions with distinct spectral
0° observer emission angles) by using a Robotic graphic techniques developed for irregular properties (29). To establish statistically mean-
Lunar Observatory photometric function to planetary bodies (23, 31, 32). Band ratios and ingful relationships between color, reflectance,

Fig. 1. Color composite, reflectance,
and band ratio maps of Bennu. (A) False-
color red-green-blue (RGB) color model
composite overlaid on a 0.55-mm (v band)
normal reflectance map of Bennu. Color
channels are: red, x/v (0.85/0.55 mm,
mid-VIS to NIR spectral slope); green, w band
strength (depth at 0.70 mm, composition,
fig. S5); and blue, b′/v (0.47/0.55 mm,
near-UV slope). (B) Normal reflectance.
(C) The x/v band ratio, a proxy for
the mid-VIS to NIR spectral slope,
where warmer values correspond to
redder spectral slopes; values >1 are
redder than the global average, and
values <1 are less red than the global
average. (D) The b′/v band ratio,
a proxy for the near-UV slope, where
higher values correspond to bluer spectral
slopes; values >1 are bluer than the
global average, and values <1 are less
blue than the global average. All
maps range from 65°N to 65°S latitude
(positive and negative values on the
y axes respectively correspond to north
and south), 0° to 360°E longitude.
The white area near 50°S, 128.5°E
represents no data.

DellaGiustina et al., Science 370, eabc3660 (2020) 6 November 2020 2 of 12

SURVEYING BENNU

and morphological features, we mapped ~1600 features using centimeter-scale 3D digital terr- resolution using the OSIRIS-REx Visible and
boulders and ~700 craters, then extracted ain models produced with data from the
their median spectra using established meth- OSIRIS-REx Laser Altimeter (OLA) (34–36). We InfraRed Spectrometer (OVIRS) (37).
ods (4, 31, 33). We assessed spectral variations also compared our findings with near-infrared Bennu’s global photometric spectrum is mod-
that were bounded by irregular morphological hyperspectral data acquired at lower spatial
erately blue (b′ to x spectral slope of –0.1701 mm–1)
in MapCam data (0.44 to 0.89 mm), but spectral

AB

CD

Fig. 2. Variation of boulder color and reflectance on Bennu. (A) Reflectance versus the b′ to x spectral slope. Dark boulders tend to have a steeper near-UV
distribution of boulders (>5 m) on Bennu. The distribution is multimodal with slope relative to the global average (>1), whereas bright boulders are more often
more than one Gaussian component (31). Shading and colors indicate different spectrally flat or show a downturn in the near-UV (from the b′ to v bands). (D) The
classifications of boulders, as indicated in the legend. (B) Normal reflectance versus relative band depth at 0.7 mm (w band) versus the b′ to x spectral slope. Some
absolute spectral slope of the same boulder populations; some individual boulders boulders show an absorption feature at 0.7 mm (relative w band depth >0), indicative
are indicated in the legend. Dark boulders tend to be redder, and their reflectance of Fe-bearing phyllosilicates. The boulders named Roc (23.6°S, 25.3°E; Fig. 3C)
monotonically decreases with increasing (redder) spectral slopes, whereas bright and BenBen (46.8°S, 127.5°E) are two of the largest on Bennu; both are dark. The blue
boulders are bluer and more scattered (31). (C) The near-UV index (b′/v band ratio) rock (39.80°S, 263.02°E) is shown in Fig. 3E.

DellaGiustina et al., Science 370, eabc3660 (2020) 6 November 2020 3 of 12

RESEARCH | SURVEYING BENNU

slopes vary from blue (negative, –0.25 mm–1) to Table 1. Adopted color units on Bennu and their distinguishing properties.
red (positive, 0.05 mm–1) at spatial scales of as
small as 2 m (Fig. 1). Bennu’s surface exhibits Color unit Distinguishing properties
widespread heterogeneity in reflectance (Figs.
1 and 2). PCA shows that the first principal Bright boulders Normal reflectance ranges from 0.049 to 0.074.
component (PC1) corresponds to albedo, whereas
the second principal component (PC2) corre- Bluish spectral slopes are slightly steeper than
sponds to changes in the overall spectral slope
(from b′ to x), and PC3 indicates variation in the global average in the mid-VIS to NIR
the near-ultraviolet (near-UV) region (from b′
to v) (figs. S1 to S3). wavelengths (0.52 to 0.96 mm) but are often

Bennu’s globally blue surface is dominated spectrally flat or show a downturn in the
by a coarse layer of decimeter- to meter-scale
rocks with some centimeter-scale particles near-UV wavelengths (0.44 to 0.50 mm;
(regolith), which we refer to as average terrain.
The spectral variability is associated with dis- . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .M. . . .a. .p. . .C. . .a. .m. . . . . .b. .′. . .b. . .a. .n. . .d. . ). ... . .D. . .i.a. . .m. . . .e. .t. .e. .r. .s. . . .a. .r. .e. . . .<. . .1. .0. . . . .m. . . ... . . . . . . . . . . . . . . . . .
tinct geologic features, including boulders,
craters, and areas of mass wasting (rock move- Dark boulders Normal reflectance ranges from 0.034 to 0.049,
ment down geopotential slopes), which we
used to distinguish color units on the asteroid overlapping with the average reflectance of
(Table 1 and fig. S4, A and B). These units pro-
vide a framework for classifying commonly Bennu (0.044). Slopes tend to be redder in the
observed features on the surface.
mid-VIS to NIR wavelengths (0.52 to 0.96 mm) and
Boulders on Bennu
often show an upturn in the near-UV wavelengths,
Boulders are the primary source of heteroge-
neity on Bennu. Some individual boulders have consistent with the global average. Diameters
VIS-NIR absorption features at 0.55 mm [as pre-
viously observed (5)], 0.7 mm (Fig. 2D), and near range from decimeters to ~95 m.
1 mm [as previously observed (38)]. There are
also outliers among the boulder population that .....................................................................................................................................................................................................................
do not correspond with a specific color unit.
Fe-bearing phyllosilicate boulders An absorption feature is present at 0.70 mm
Boulders have a wide range of normal re-
flectance values [0.032 to at least 0.26 (38)] (determined from a relative band depth >1%
that are multimodally distributed with two
prominent peaks (Fig. 2A). The reflectance of in the MapCam w band). Reflectance spans
boulders is not normally distributed and is
most consistent with four Gaussians (31), or a wide range, most often overlapping with
perhaps two or more non-Gaussian compo-
nents. We refer to boulders as bright or dark that of dark boulders.
based on whether they are brighter or darker
than the median reflectance of 0.049, which .....................................................................................................................................................................................................................
lies between the two prominent peaks of the
reflectance distribution. Pyroxene-bearing boulders An absorption feature is present beyond

Bright boulders have smooth surfaces, typ- 0.89 mm (determined from a downturn in the
ically angular shapes (Fig. 3, A and B), and blue
spectral slopes in the mid-VIS to NIR (MapCam MapCam x band relative to the w band) due to pyroxene
v to x bands). However, unlike the average
terrain, ~80% of the bright boulders are dark (36). Reflectance may reach up to 0.26 (36). These units
in the near-UV region (b′/v < 1; Fig. 2 and fig.
S4, A and B). The bright boulders appear can occur as discrete boulders or pyroxene-bearing
to have similar sizes (are well sorted) with
diameters <10 m. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .c. .l. a. . .s. .t. .s. . . .i.n. . . .a. . . .d. . .a. .r. .k. . . .b. . .o. .u. . .l.d. . e. . .r. .–. . l. .i.k. .e. . . .m. . . .a. . .t.r. .i.x. . ... . . . . . . . . . . . . . . . . . . . . . .

Dark boulders (reflectance ≤0.049) span a Blue units These boulders and craters show an upturn in the
range of visible spectral slopes but are gener-
ally redder than the bright boulders in the near-UV wavelengths that exceeds that of the
mid-VIS to NIR wavelengths (Figs. 1 and 2, A
and B). The dark boulders are less angular than global average photometric spectrum, possibly
bright boulders and commonly have rougher,
more undulating surface textures (Fig. 3, C . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .r. .e. .s. .u. . .l.t. .i.n. .g. . . . f. .r. .o. .m. . . . . .a. .n. . . . .a. .b. . .s. .o. . .r.p. . .t. .i.o. .n. . . . a. . .t. . .0. . ...5. . .5. . . .m. . .m. . . ... . . . . . . . . . . . . . . . . .
and D). They encompass a wide range of sizes
(from decimeters to ~95 m) and include all Reddish craters These small (<25-m diameter) craters are ≥0.5s
large ð≳20 mÞ boulders on the asteroid. Al-
though the average terrain lies between the redder than Bennu’s global average (median)

and contain material that is not resolved

at ~2 cm per pixel.

.....................................................................................................................................................................................................................

Breccias These medium (~5 m) to large (>10 m) boulders

have embedded clasts (tens of centimeters)

whose spectrophotometric properties are

distinct from those of the host matrix, which

resembles the dark boulders.

.....................................................................................................................................................................................................................

Average terrain These areas are absent of large boulders

ð≳20 mÞ and have a photometric spectrum

similar to the global average (median).

.....................................................................................................................................................................................................................

bright and dark populations, dark boulders H) and occur in textures akin to weathering
and smaller dark particles (presumably formed rinds—exterior crusts that appear discolored
by boulder breakdown) appear to be the dom- compared with faces that are potentially more
inant material; this is illustrated by the close recently exposed (Fig. 3, C and G). We also
correspondence between Bennu’s average re- observed boulders that appear to be breccias—
flectance (0.0439 ± 0.002) and the reflectance that is, objects composed of rock fragments
peak of the dark boulder population (0.0450 ± cemented together as a result of large impacts
0.002) (Fig. 2A, gray dashed line). on Bennu’s parent body (33, 38). In these bould-
ers, spectrophotometrically distinguishable frag-
Color variation is also evident within indi- ments (clasts) are embedded in a host matrix
vidual boulders (Figs. 1 and 3). Sometimes this that has similar texture, reflectance, and color
occurs between faces of an individual rock, to the dark boulders (Fig. 3, E and F).
usually a large dark boulder (Fig. 3, C to H).
These examples of intraboulder color varia- A small population of boulders with very
tion are associated with apparent exfoliation high reflectance [up to 0.26 (38)] shows evidence
and fracturing of the rock (39) (Fig. 3, G and of an absorption feature at 1 mm (downturn in

DellaGiustina et al., Science 370, eabc3660 (2020) 6 November 2020 4 of 12

SURVEYING BENNU

Fig. 3. Examples of boulder color and morphology. All RGB color composite (E) A dark boulder with resolvable clasts that appear distinct from the host
images are shown on the same color scale as in Fig. 1A. (A and B) Bright matrix (4.62°S, 248.95°E). (F) Digital terrain model of the same boulder. The
boulders near 17.76°S, 74.74°E in (A) MapCam (25 cm per pixel) and (B) three arrows highlight the same clast in (E) and (F). (G) A rock at 39.80°S,
PolyCam (5.25 cm per pixel) images. The higher-resolution panchromatic 263.02°E. The darker and bluer portion corresponds to a lower-relief fractured
PolyCam image (B) shows the angular morphology of bright boulders. (C and face in the digital terrain model (H). (I) A boulder that appears to contain clasts
D) Dark boulders near (C) 23.6°S, 25.3°E and (D) 3.92°N, 178.98°E, some of and be brecciated; the bright clasts with a greenish color signature are indicative
which display intraboulder color variation. This includes Roc (C), which is the of pyroxene in this false-color scale. (J) A higher-resolution PolyCam image
largest boulder observed on Bennu at 95 m in the longest observable dimension. (5.25 cm per pixel) of the same boulder. A wider context image is shown in fig. S15.

the x band). OVIRS data indicate that these in some clay-bearing phyllosilicates (41). Bould- (fig. S4C). The bluer, recessed eastern face may
boulders contain pyroxene (38). Pyroxene- ers with the deepest absorptions at this wave- be a fresher surface, more recently exposed to
bearing material appears in distinct clasts em- length span a wide range of reflectance (0.036 the space environment by thermal fracturing
bedded within larger host rocks whose color to 0.081); however, most (~60%) dark boulders or exfoliation—ongoing surface processes on
and reflectance are similar to those of the dark tend to have a shallow (~1%) 0.7-mm absorp- Bennu (39, 42). Similar patterns are observed
boulders (Fig. 3, I and J) (38); it also appears in tion. Although this is at the limit of the 1% rel- on other boulders that appear to have been
smaller (meter-scale), isolated boulders that ative precision of OCAMS data (29), it is spatially recently exfoliated (as indicated by layers with
do not look brecciated. Pyroxene was probably coherent with individual boulders, giving us different relief). We also observe bluer-than-
inherited from Bennu’s parent body, where it confidence that the feature is real (fig. S5). average near-UV slopes on the high-elevation
was implanted by an impactor that may have rims (10 to 20 m higher than surrounding
originated from a fragment of (4) Vesta (38), Color and surface processes terrains) of equatorial craters that show recent
the differentiated (not primitive) inner–main- indications of mass wasting (Fig. 4, A and B) (43).
belt asteroid visited by the Dawn mission (40). Some areas of the surface are brighter in the
Although their reflectance overlaps with that near-UV region (i.e., show an upturn in the The correspondence between blue units and
of the bright boulders and their texture is like near-UV b′ band; b′/v > 1.01, or 1% greater than potentially less weathered surfaces suggests
that of the breccias, we separated pyroxene- average); we refer to these areas as blue units. that enhanced near-UV reflectance is related
bearing boulders into their own category (Table One of the bluest contiguous surfaces on Bennu to younger exposure ages on Bennu. The blue
1) based on their distinct spectral shape in the is the eastern side of the boulder shown in Fig. units are correlated with the relative band
VIS to NIR (v to x; Fig. 2, B and C). 3G. Digital terrain models show that this rock depth at 0.55 mm (fig. S6), indicating that
face is recessed relative to the western face of the upturn observed in the near-UV index
Some boulders have an absorption feature the boulder (Fig. 3H), and color data indicate may be the result of an absorption feature
at 0.7 mm (absorption depth of 2 to 10%). Sim- that the recessed face has a steeper blue spec- at 0.55 mm. This absorption feature on Bennu
ilar absorption features have been observed in tral slope. Conversely, the western face of the has previously been attributed to magnetite
spectra of primitive asteroids and carbonaceous boulder is brighter and has a more neutral (5), which is also detected in thermal emis-
meteorites, where they were attributed to iron spectral slope, similar to the global average sivity spectra from the OSIRIS-REx Thermal

DellaGiustina et al., Science 370, eabc3660 (2020) 6 November 2020 5 of 12

RESEARCH | SURVEYING BENNU

Emission Spectrometer (OTES) (7). However, The size-frequency distribution of reddish as the primary OSIRIS-REx sample collection
this absorption feature could also result from craters implies that they are one of the young- site, Nightingale (56°N, 42°E).
graphitized carbon (44), and both magnet- est components of the global crater population
ite and graphite are associated with space (Fig. 5C). If so, we expect that reddish craters Evidence of freshly exposed material on Bennu
weathering (discussed further below). are among the youngest surface features on
Bennu. The absolute spectral slopes of the Reddish craters and blue units on Bennu both
The color of the largest craters (>100 m) on reddish craters appear to correspond with correspond to apparently young exposure ages
Bennu is indistinguishable from that of the crater size (Fig. 5, A and B), and these craters (Figs. 3, G and H, and 4, C and D). To resolve
average terrain. However, many small craters are also darker than the global average (Fig. this apparent contradiction, we considered
(≤25 m) are redder than Bennu’s average by 5D). In PolyCam images, the reddish craters crater production rates and size-scaling laws,
≥0.5s in the near-UV to NIR, where s is the display a texture distinct from that of the bulk stratigraphic relationships, and potential con-
full-width at half maximum of the global dis- of Bennu’s surface: unresolved at the pixel scale tributors to spectral slopes other than expo-
tribution of b′ to x spectral slopes (Figs. 4, C (i.e., <5 cm), indicating fine-particulate material sure age.
and D, and 5, A and B). We refer to these as (fig. S7). The largest examples of reddish
small reddish craters. By contrast, we identified craters exist at mid- to high latitudes (pole- The size-frequency distribution of the red-
no craters bluer than Bennu’s global average ward of ±20°), including the crater selected dish craters has a power-law index of –2.1 ± 0.4
spectral slope by ≤0.5s (Fig. 5A). (31). The power-law index of the reddest
subset of these craters (b′ to x spectral slopes
Fig. 4. Examples of crater color. (A) The b′/v band ratio map of equatorial craters at 3.05°S, 128.79°E ≥1s from the global median value, i.e., ≥
(black dashed circle) and 1.06°S, 152.75°E (red dashed circle), which have a relatively high near-UV index and –0.0698 mm–1) is –2.3 ± 0.6 (31). These values
are considered blue units. (B) An elevation map of the same equatorial craters in (A). These blue units are close to that of the expected production of
correspond with areas that show recent indications of mass movement away from regionally high elevations, craters in the present-day main asteroid belt
such as from crater rims. Black arrows correspond to locations of previously mapped mass movement and near-Earth space over the past 100,000 years
(43). (C and D) RGB color composite images of small craters (indicated by white arrows), shown on the same (predicted power-law index between –2.6 and
color scale as in Fig. 1A. As indicated by their color, these craters are consistently redder than Bennu’s –2.7; Fig. 5C) (45–48). The global crater popula-
average terrain, with positive to slightly blue b′ to x spectral slopes. The blue crater indicated by the dashed tion has a different power-law index of –1.1 ±
black circle in (A), (B), and (D) has been overprinted by several smaller reddish craters. 0.1 (31). At small diameters, the distribution
of the reddish craters does not deviate from
that of the expected crater production (Fig.
5C), unlike the global population of craters
on Bennu (33) and nearly all other closely
studied small bodies (49). A mismatch at
small diameters between observed crater
populations and the expected crater produc-
tion has been attributed to erasure processes
(49), which efficiently erode and diminish small
craters. The correspondence between the
expected production of the redder craters on
Bennu and their actual distribution supports a
young age: Unlike the global crater distribu-
tion, they have not yet experienced substan-
tial erasure.

We estimated the time required to produce
the craters on Bennu using a crater produc-
tion rate and a scaling law for crater size from
impactor size (31). Assuming that the redder
craters have formed since Bennu’s arrival in the
inner Solar System, we adopted the established
crater production rate from the near-Earth
object population (47, 48). Crater scaling rela-
tionships, however, are less certain owing to
unknown material properties and the structure
of rubble-pile asteroids. The Small Carry-on
Impactor (SCI) experiment performed on asteroid
(162173) Ryugu by the Hayabusa2 mission (50)
showed that small impactors (~30 cm) can
produce craters consistent with scaling laws
that depend on gravity; craters formed in this
gravity regime can be many times larger than
the sizes expected from scaling laws governed
by target material strength. The sizes of the
reddish craters on Bennu are smaller than or
similar to the diameter of the SCI crater (~18 m)
(50). If gravity dominates the cratering process
for small craters on Bennu (51), the reddest
subset of these craters is less than 105 years old

DellaGiustina et al., Science 370, eabc3660 (2020) 6 November 2020 6 of 12

SURVEYING BENNU

Fig. 5. Color, reflectance, and size distribution of Bennu’s craters. (A) The b′ the reddish craters (purple circles) is more consistent with the black line at
to x spectral slope distribution of craters on Bennu, which are not normally small diameters than that of the global crater population (gray circles).
distributed. (B) Crater diameter as a function of the crater’s median b′ to x spectral The reddest subset of craters (red circles) falls below the black line and
slope. Craters have more negative spectral slopes at higher size and frequency; appears to have formed more recently than 100,000 years ago. (D) The
this suggests that redder (more positively sloped) craters are younger. (C) The normal reflectance of craters on Bennu as a function of b′ to x spectral
crater size frequency distribution on Bennu for craters classified on the basis of slope. Like that of dark boulders, the reflectance of craters monotonically
their b′ to x spectral slopes. The black line shows the expected crater production decreases with increasing (redder) spectral slopes (31). Supporting
for 100,000 years in near-Earth space (cumulative power-law index of –2.7), information for the relationship between spectral slope and crater size
assuming cratering in the gravity regime (51). The size-frequency distribution of and frequency is shown in fig. S16.

DellaGiustina et al., Science 370, eabc3660 (2020) 6 November 2020 7 of 12

RESEARCH | SURVEYING BENNU

(Fig. 5C). This is consistent with the expected the emission of its own thermal radiation with large color variation (b′ to x slope differ-
time scale of space weathering on near-Earth (10, 55), consequences of the Yarkovsky-O’Keefe- ence of >0.05 mm–1 between the two regions)
asteroids (~105 years) based on returned sam- Radzievskii-Paddack (YORP) effect. The lo- as a function of the azimuthal angle of the
ples of asteroid Itokawa (52) and laboratory ex- cations of two of the bluest craters (1.06°S, blue-to-red direction (31). Bluer faces are pre-
periments on primitive meteorites (20). Thus, 152.75°E and 3.05°S, 128.79°E) correspond to ferentially oriented toward the equator (fig. S12).
it is plausible that the reddish craters are the an isolated equatorial region that experienced This may relate to solar exposure (e.g., heating
most recent areas of surface exposure and re- increased surface accelerations as Bennu’s spin or irradiation) and/or meteoroid bombard-
present the least weathered material on Bennu. period decreased from 5 hours to the present- ment, all processes that would preferentially
day 4.3 hours (fig. S10) (10, 55), suggesting that affect equatorial latitudes (42, 56). We ob-
Although recent surface exposure may ex- this area has experienced surface mass move- served this intracolor variation only on dark
plain the reddish craters on Bennu, in carbo- ment at some point in the past 200,000 years boulders, perhaps owing to their larger sizes
naceous meteorites, redder spectral slopes in (43). Thus, we infer that that the exposure age compared with other boulder types, or a dif-
the VIS-NIR can also arise from fine particle of blue units is ~200,000 years. ferent initial composition.
sizes (<100 mm) (53). The smooth and unre-
solved appearance of the reddish craters on Blue unit craters have also been overprinted Mechanisms for space weathering on Bennu
Bennu suggests that they possess finer-scale by small reddish craters (Fig. 4D); we there-
regolith (fines) than elsewhere on the surface fore presume that they are composed of the Dark, optically opaque minerals, such as nano-
(fig. S7). However, small craters on boulders same underlying material and that the blue phase iron, graphitized carbon, sulfides, and
also appear redder than the global average unit craters are older than the reddish craters. magnetite, are commonly produced by space
photometric spectrum, indicating that parti- This color trend of bluing with exposure time weathering of primitive materials (19, 23, 44, 57).
cle size is not the only factor (fig. S8). When the is consistent with some spectral studies of Laboratory studies have shown that phyllosi-
electrostatic forces acting on particles exceed space weathering of carbonaceous meteorites licates intimately mixed with certain carbon
that of gravity and cohesion—as is often the (18–22) but not previous surface-resolved ob- species (including graphite) and magnetite
case for micrometer-sized grains on asteroids— servations of asteroids. can lead to bluer and darker spectral slopes
lofting occurs and preferentially removes fines in the visible wavelengths (44) (fig. S4, C and
(54). Simulations of electrostatic lofting show We suggest that nonlinear space weathering D). The link between bluing opaque minerals
that detachment and escape of submillimeter occurs on Bennu’s surface. In this scenario, and space weathering implies that blue spec-
particles is feasible on Bennu and likely occurs freshly exposed material is initially redder tral slopes are the result of a mature, weath-
shortly after the formation of such fines (54). than the bulk of Bennu in the near-UV to NIR ered regolith on primitive B-type asteroids,
Although particle sizes <100 mm could con- wavelengths (b′ to x) (first stage). During early although they cannot fully explain the bright-
tribute to reddening on Bennu, we anticipate space weathering, these surfaces brighten more ening in the near-UV to NIR observed on Bennu.
that the loss of fines takes place on shorter time rapidly in the near-UV (b′) than in the mid-VIS
scales than the age of the reddish craters. How- to NIR (v to x), thereby increasing the b′/v band As discussed above, studies of primitive as-
ever, if micrometer-scale particles are closely ratio (middle stage). This near-UV bluing may teroids and meteorites have contradictorily
associated with freshly exposed materials, they result from the deepening of an absorption near predicted both bluing and reddening with
could also produce the observed reddening. 0.55 mm, implying that magnetite or graphite increased space weathering (13–24). Ion and
abundance increases during the early stages of meteoroid bombardment lead to darkening
Longer infrared wavelengths also indicate space weathering. Eventually, however, these and reddening of anhydrous silicate plane-
younger exposure ages for reddish craters. The color differences neutralize as the surface is tary surfaces; this has previously been attrib-
shape of the 2.7-mm hydration feature, which is brightened across the wavelengths observed uted to the accumulation of nanophase and
ubiquitous on Bennu (7), is sharper and shifts by MapCam, and the downturn at 0.55 mm larger metallic iron particles, which form in
to shorter wavelengths within reddish craters, (v band) diminishes, leading to the gently response to the space environment (58). How-
including the Nightingale sample site (fig. S9A). blue spectral slope that characterizes Bennu’s ever, contrary to the bluing and darkening pre-
This is consistent with laboratory space weather- global photometric spectrum and the oldest dicted from the production of graphitized
ing experiments performed on carbonaceous craters (final stage). carbon and magnetite, the formation of nano-
meteorites (20), which show that the minimum phase iron in low-albedo asteroids such as
of the hydration feature at ~2.7 mm moves This space weathering progression is dem- Bennu may have a reddening and brightening
toward longer wavelengths with prolonged ex- onstrated by craters that have been categorized effect, owing to the higher reflectance of nano-
posure to space weathering processes. Thus, on the basis of their spectral slope (Fig. 6). phase iron than that of the primitive materials
sharper band features with shorter minimum The first and middle stages are illustrated by found in carbonaceous meteorites (59).
wavelengths within craters may signify more the small reddish craters overprinted on blue
recent exposure. The blue equatorial crater at equatorial craters (Fig. 4D). The middle and Space weathering trends observed on Bennu
1.06°N, 152.75°E (Fig. 4, A and B) appears to final stages may also be illustrated by the corroborate earlier studies (13, 44) that found
have a sharper absorption feature but a band boulder in Fig. 3G, whose higher-relief, pre- that primitive asteroids, though dark relative to
minimum similar to the global average (fig. sumably older western face is brighter and has the asteroid population, are brighter in the UV
S9B), indicating that it may have an interme- a more neutral spectral slope than the more than their primitive meteorite counterparts—
diate exposure age. Unlike the spectral slope, recently exposed, bluer face. The final stage is that is, they are spectrally bluer at shorter
the shape of this spectral signature is not ex- illustrated by Bennu’s average terrain. wavelengths. Ion bombardment of primitive
pected to be influenced by particle size (20). low-albedo meteorites in the laboratory leads
The orientation of intraboulder color varia- to spectral bluing and brightening (20). These
The exposure age is less clear for the bluer- tion provides further evidence of space weather- spectral changes are attributed to the process
than-average, apparently broken boulder face ing on Bennu. We examined 220 boulders of carbonization, whereby hydrogen is lost and
in Fig. 3, G and H. We can set some constraints with sizes ≳5 m in the equatorial region (20°S crystalline carbon structures, such as graphite,
from the blue units associated with equatorial to 20°N), where MapCam images have the are formed (57). Irradiation experiments on
craters. Since its time in near-Earth space, most consistent viewing conditions, and cal- complex hydrocarbons have shown that car-
Bennu’s rotation rate has accelerated in re- culated the azimuthal angle that maximizes bonization can induce metal-like optical prop-
sponse to surface scattering of sunlight and blue-to-red color variation across each boulder erties in carbonaceous material, which leads
(31). Figure S11 shows the latitude of boulders

DellaGiustina et al., Science 370, eabc3660 (2020) 6 November 2020 8 of 12

SURVEYING BENNU

A Bennu average global spectrum ( ) B
Bluer than average craters ( > b -x slope)
0.048 Redder than average to reddish craters ( +0.5 > b -x slope > ) 1.03
0.046 Reddish to reddest craters ( +1 > b -x slope > +0.5 ) 1.02
0.044 1.01
0.042 Reddest craters (b -x slope > +1 ) 1.00
Normal reflectance (I/F) 0.99
0.04 Reflectance (I/F) normalized at 0.55 m 0.98
0.038 0.97
0.036 0.96
0.95
0.94

0.5 0.6 0.7 0.8 0.5 0.6 0.7 0.8

Wavelength ( m) Wavelength ( m)

Fig. 6. Evolution of crater colors from MapCam data. Older craters have bluer normalized at 0.55 mm. The progression from the mid-VIS to NIR (v to x bands)
overall spectra from b′ to x (Fig. 5); here we show variations in each filter dominates the evolution of crater spectra, which mature toward more negative
separately. (A) The average absolute reflectance spectra of all craters within slopes. In the near-UV, spectra with intermediate b′ to x slopes steepen in a
a given b′ to x slope range (see Fig. 5A). The light gray box encompasses the subtle but statistically significant way (31). This may result from more rapid
range of absolute radiometric uncertainty (29), whereas error bars show the brightening in the near-UV relative to longer wavelengths, a deepening of
relative precision of OCAMS measurements (26). Craters become brighter absorption feature at 0.55 mm (v band), or both. As a result, crater spectra
as their spectral slopes steepen. (B) The same reflectance spectra shown in (A), show a non-unidirectional change near the b′ band as they age.

to bluing and brightening (17, 57). We propose erties for boulders on Bennu (60). The dark phyllosilicates than other boulders and implies
that space weathering–induced carbonization boulders have lower thermal inertia, which is that they represent a population of material
or magnetite formation may have influenced attributed to higher porosity (60), consistent from Bennu’s parent body that has experienced
the surface colors on Bennu, especially in dark with their rougher and more crumbly (friable) less aqueous alteration. A correlation between
materials that become bluer (from the v to appearance (Fig. 3, C and D). Conversely, the lower reflectance and a 0.7-mm absorption band
x bands) and brighter (across all bands) with apparently smoother, more consolidated and is consistent with moderately altered CM car-
increased exposure age. angular bright boulders (Fig. 3, A and B) tend bonaceous chondrites, which are among the
to have higher thermal inertias, attributed to darkest primitive meteorites with a nearly ubi-
Evidence for parent body heterogeneity lower porosity (60). Distinct texture and poro- quitous 0.7-mm absorption feature (64).
sity can follow from differing mineralogy, levels
Although space weathering may influence the of compaction, or heating and aqueous alter- Some bright boulders contain veins of
spectral slopes on Bennu, the disparate boul- ation histories. brighter material, which may be composed of
der populations that we identify—which differ carbonates (9). This implies a level of aqueous
in terms of their reflectance, texture, and size— The average blue spectrum of Bennu is con- alteration that should also lead to the forma-
suggest that some of Bennu’s heterogeneity was sistent with serpentine or magnetite and ser- tion of magnetite (65). The lack of a near-UV
inherited from its parent body. Dark boulders pentine, with some carbon (fig. S4, C and D). upturn in carbonate-bearing boulders could
show a monotonic relationship of decreasing This composition is similar to that of Bennu’s signify that other phases influence their spec-
reflectance with increasing (redder) spectral presumed meteorite analogs, the CM and CI tral characteristics. For example, bright boul-
slope, which is distinguishable from that of groups of carbonaceous chondrites, which are ders may be dominated by a hydrated mineral
their bright counterparts (Fig. 2B) (31). Be- dominated by Fe- and Mg-bearing phyllosi- that is more absorbing at the longer wave-
cause space weathering is likely controlled by licates, respectively. In the most intensely lengths (so the reflectance is bluer).
initial texture and composition, the difference aqueously altered CI chondrites, the Fe is con-
in spectral slope trends between dark and tained in oxides, sulfides, carbonates, and other We expect vein-bearing boulders to con-
bright boulders could result from the matura- minor species (61–63). tain less organic material if their reduced
tion of geologically distinct materials. Likewise, carbon was oxidized by fluids to form the
the less varied spectrophotometric properties The tendency of dark boulders to be slightly observed carbonates (66). Thus, if both low
of the bright boulders suggest that they are less redder and brighter in the near-UV region albedo and near-UV bluing are caused by
susceptible to modification from space weather- (Fig. 2, A to C) may indicate that they have a the carbonization of organics via space weath-
ing or change on a different time scale (Fig. 2). higher overall abundance of organic molecules ering, we expect those spectrophotometric ef-
compared with their bright counterparts. This fects to be weaker in the vein-bearing rocks—as
Heterogeneity in boulder reflectance on Bennu composition manifests as lower reflectance and is observed (Fig. 2, A and C). Although graph-
may be the result of distinct rock types that redder slopes in more freshly exposed surfaces, itized carbon could explain the bluing ob-
fragment differently, leading to an observed which develop into steeper blue slopes during served in the more recently exposed faces of
difference in their size-frequency distributions the early stages of space weathering. This, dark boulders, a UV upturn is also consistent
(4). Different compositions of the dark versus along with the weak 0.7-mm absorption some- with increasing abundances of magnetite,
bright boulders may account for the corre- times present in dark boulders (Fig. 2D), is in- which has a blue spectral slope shortward
lation between reflectance and thermal prop- dicative of a higher proportion of Fe-bearing of 0.5 mm (65).

DellaGiustina et al., Science 370, eabc3660 (2020) 6 November 2020 9 of 12

RESEARCH | SURVEYING BENNU

The presence of potential carbonate veins thought to have come from primitive asteroid during the spin-down of Ryugu (68). A lati-
(9) in bright boulders signifies a greater degree families in the inner main belt (67), Ryugu, un- tudinal color trend is also observed on Bennu,
of aqueous alteration than in their dark coun- like Bennu, appears to have experienced par- but the difference is small compared with its
terparts, suggesting an origin within the in- tial dehydration (68). The multiband cameras overall color variation [>99% confidence with
terior of Bennu’s parent body. In dark boulders, onboard the two spacecraft use similar photo- mean difference of 0.21s (31)]. Bennu’s slightly
we do not find a clear spectral signature in- metric filters in the visible wavelengths and bluer equatorial region may indicate the pres-
dicative of their provenance; however, their thus allow a direct comparison of the spectra ence of more mature material, which is con-
textures may provide clues. Brecciated boulders from each (26, 31, 68). Figure S13 shows the sistent with its increasing rotation rate and
typically have a host matrix similar in texture areal distribution of the reflectance and near- the associated global patterns of mass move-
to the dark boulders, including examples with UV to NIR spectral slope of each asteroid. The ment across the asteroid (43).
clasts of exogenic pyroxene; this implies variation in reflectance on Bennu is 1.7 times
that these rocks formed near the surface of that on Ryugu, and Bennu exhibits a bluer Unlike Ryugu, color variation on Bennu ap-
Bennu’s parent body (38). Boulders on Bennu overall color. Though the standard deviations pears to be dominated by heterogeneity at the
thus may have originated from different zones of the spectral slope distributions are similar meter scale, likely driven by boulders. This
within the parent body. The multimodal dis- (s = 0.039 and 0.034 mm–1 for Ryugu and suggests that the extent of recent large-scale
tribution of the boulder populations implies Bennu, respectively), the distribution of color mass wasting on Bennu may not have been
that different processes (or extents of processes), differs spatially. Ryugu shows large-scale lati- as widespread as the effect of regolith mix-
such as aqueous alteration and heating, led to tudinal color differences: The latitudinal dif- ing. Episodes of particle ejection have been
their distinct spectrophotometric properties. ference is ~0.5 the standard deviation of the observed from Bennu’s surface (42), redistrib-
global color variation [>99% confidence with uting its surface material over shorter time
Comparison with Ryugu mean difference of 0.52s between the redder scales than those expected for mass wasting
mid-latitudinal and the bluer equatorial regions (69). Large-scale latitudinal spatial patterns
Asteroid Ryugu, visited by the Hayabusa2 (27)], which has been attributed to regolith may have been obliterated by particle ejection
spacecraft, is also a low-albedo, carbonaceous migration from the equator to mid-latitudes events, which overturn ~104 g of surface mate-
near-Earth asteroid. Although both asteroids are rial per orbit (437 days) (69). Of the material

Surface processes

Fig. 7. Proposed model of color and reflectance diversity. We propose that formation and subsequent transit to near-Earth space, it has been altered by
distinct rock types formed at different depths on Bennu’s parent body. After exposure to the space environment, which ultimately results in its moderately
the parent body was catastrophically disrupted by a giant impactor, Bennu blue global color. Small near-Earth impactors also continually refresh the surface,
accumulated from its debris (4–6) and inherited these distinct materials, leading creating craters of comparatively fresh, reddish material, which weather
to the observed heterogeneity among boulders on Bennu. Since Bennu’s toward bluer colors on a time scale of ~105 years.

DellaGiustina et al., Science 370, eabc3660 (2020) 6 November 2020 10 of 12