Science 30.10.2020

CONTENTS INSIGHTS

30 OCTOBER 2020 • VOLUME 370 • ISSUE 6516 PERSPECTIVES

522 & 557 522 Of dogs and men
Ancient genomes reveal the common history
Dogs, including this endangered dingo, were the first domesticated animal. Researchers have examined of human and dog By P. Pavlidis and M. Somel
ancient dog genomes to identify the complex way in which man’s best friend evolved.
RESEARCH ARTICLE p. 557
NEWS 514 How an immunologist pivoted PHOTO: GARY MEREDITH
to tackle COVID-19 523 The quiet spring of 2020
IN BRIEF For Akiko Iwasaki, the pandemic has Anthropogenic noise has no legacy effects
brought new research priorities—and on bird song By W. Halfwerk
508 News at a glance new urgency By J. Couzin-Frankel
REPORT p. 575
IN DEPTH 515 Edit reviews without permission?
Some journal editors say it’s OK 525 Speeding protons with metal
511 U.S. funds new fleet of probes to Deleting offensive language is common, vacancies
explore ocean biogeochemistry but some editors alter reviewers’ overall Membranes made from nanosheets derived
Drifting Argo floats will track oxygen loss from recommendation By C. O’Grady from CdPS3 have high proton conductivity
global warming and the oceans’ ability to
soak up carbon By P. Voosen 516 Efforts to control monkey brains By F. Wang and J. He
get a boost
512 Denisovan DNA found in cave on With open data project, primate REPORT p. 596
Tibetan Plateau optogenetics confronts stumbling blocks
“Molecular caving” shows archaic humans 526 Should I stay or should I go?
visited high-altitude cave over long period By K. Servick Pinpointing genetic alleles that influence
the timing of salmon migration might aid
By A. Gibbons F E AT U R E S restoration efforts By G. McKinney

REPORTS pp. 579 & 584 518 Power to the people REPORT p. 609
Nations are turning to citizen
513 Herd immunity? India still has a long assemblies to weigh up climate 527 Will SARS-CoV-2 become endemic?
way to go, scientists say policies By C. O’Grady Reinfection, seasonality, and viral
Cases are dropping, but critics question competition will shape endemic transmission
optimistic forecast By V. Chandrashekhar PODCAST patterns By J. Shaman and M. Galanti

500 30 OCTOBER 2020 • VOL 370 ISSUE 6516 530 Charles H. Turner, pioneer in animal
cognition
An African American scientist’s early
discoveries are forgotten for all the wrong
reasons By H. S. Galpayage Dona and L. Chittka

PODCAST

532 Paolo Sassone-Corsi (1956–2020)
Groundbreaking molecular biologist
and epigeneticist By E. Verdin

POLICY FORUM

533 Political sectarianism in America
A poisonous cocktail of othering, aversion,
and moralization poses a threat to
democracy By E. J. Finkel et al.

BOOKS ET AL.

537 The vibrant lives of Neanderthals
A nuanced portrait of our evolutionary
cousins encourages empathy and
understanding By E. Pomeroy

538 A profound plan to save the seas
Rejecting piecemeal strategies,
a conservationist encourages total
ocean protection By M. E. Hannibal

LETTERS

539 Ban unsustainable mink production
By C. Xia et al.

sciencemag.org SCIENCE

Published by AAAS

512, 579, 592 Quantum systems
& 584 Parallel single-shot measurement and
coherent control of solid-state spins below
Excavation in Baishiya Karst Cave identified Denisovan mitochondrial DNA dating to 100,000 years ago. the diffraction limit S. Chen et al.

PHOTO: YUANYUAN HAN, DONGJU ZHANG, LANZHOU UNIVERSITY 539 Support U.S. research during 550 Plant science 596 Proton membranes
COVID-19 Receptor kinase module targets CdPS3 nanosheets-based membrane
By M. M. Crow et al. PIN-dependent auxin transport during with high proton conductivity enabled
canalization J. Hajný et al. by Cd vacancies X. Qian et al.
540 Hainan peacock-pheasant needs
focused protection 557 Ancient dog genomics PERSPECTIVE p. 525
By S. Guan et al. Origins and genetic legacy of
prehistoric dogs A. Bergström et al. 600 Topological systems
RESEARCH Generation of helical topological
PERSPECTIVE p. 522 exciton-polaritons W. Liu et al.
IN BRIEF
564 Coronavirus 605 Geophysics
543 From Science and other journals The emergence of SARS-CoV-2 in Europe Surface deformation associated with
and North America M. Worobey et al. fractures near the 2019 Ridgecrest
REVIEW earthquake sequence X. Xu et al.
REPORT p. 571
546 Cancer 609 Migration
Physical traits of cancer H. T. Nia et al. REPORTS A complex phenotype in salmon
controlled by a simple change in
REVIEW SUMMARY; FOR FULL TEXT: 571 Coronavirus migratory timing N. F. Thompson et al.
DX.DOI.ORG/10.1126/SCIENCE.AAZ0868 Cryptic transmission of SARS-CoV-2
in Washington state T. Bedford et al. PERSPECTIVE p. 526
RESEARCH ARTICLES
RESEARCH ARTICLE p. 564 D E PA R T M E N T S
547 Structural biology
The coupling mechanism of 575 Pandemic pause 502 Editorial
mammalian respiratory complex I Singing in a silent spring: Birds respond to Untapped computer scientists
a half-century soundscape reversion during
D. Kampjut and L. A. Sazanov the COVID-19 shutdown E. P. Derryberry et al. By Henry T. Frierson et al.

RESEARCH ARTICLE SUMMARY; FOR FULL TEXT: PERSPECTIVE p. 523 503 Editorial
DX.DOI.ORG/10.1126/SCIENCE.ABC4209 It’s just louder this time By H. Holden Thorp
579 Human evolution
548 Hybrid perovskites Denisovan ancestry and population history 630 Working Life
Atomic-scale microstructure of metal halide of early East Asians D. Massilani et al. The things I wish I could say By Anonymous
perovskite M. U. Rothmann et al.
NEWS STORY p. 512; REPORT p. 584 ON THE COVER
RESEARCH ARTICLE SUMMARY; FOR FULL TEXT:
DX.DOI.ORG/10.1126/SCIENCE.ABB5940 584 Paleogenomics Chinook salmon swimming in the Rogue River,
Denisovan DNA in Late Pleistocene Oregon. Genome sequencing and analysis
549 Microbiota sediments from Baishiya Karst Cave of tribal fishery catch in the Klamath River,
Multi-omics analyses of radiation survivors on the Tibetan Plateau D. Zhang et al. California, show that salmon ecotypes in diverse
identify radioprotective microbes and populations result from a simple Mendelian
metabolites H. Guo et al. NEWS STORY p. 512; REPORT p. 579 polymorphism that affects seasonality
of spawning migration. Physiological and
RESEARCH ARTICLE SUMMARY; FOR FULL TEXT: 587 Magnetism
DX.DOI.ORG/10.1126/SCIENCE.AAY9097 Metal-organic magnets with large coercivity reproductive differences
and ordering temperatures up to 242°C long thought to distinguish
P. Perlepe et al. ecotypes appear as a
result of environmental
effects from summer
residence in different
ecosystems. See pages
526 and 609. Photo: Mark
Conlin/Alamy Stock Photo

AAAS News & Notes.................................. 541
Science Careers ......................................... 614

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SCIENCE sciencemag.org 30 OCTOBER 2020 • VOL 370 ISSUE 6516 501

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EDITORIAL

Untapped computer scientists

Henry T. Frierson U nderrepresented U.S. women of color (UWOC)— neering (CISE) enrolled 19 UWOC; thus far, eight have
is the associate vice Black Americans, Latina Americans, Native graduated with a Ph.D. degree. Of these eight women,
president and dean Americans, and Indigenous Pacific Island- six were Black Americans, one was Latina, and one was
of the Graduate ers—have long been underrepresented among Native American. Among the remaining 11, three are
School, University of Ph.D. recipients in computer science. The num- currently doctoral candidates. Only two have left CISE
Florida, Gainesville, ber of computer science Ph.D. degrees annu- without a Ph.D. degree. Compared to the national 0.43%
FL, USA. hfrierson@
ufl.edu ally awarded to UWOC is miniscule. Moreover, UWOC (U.S. citizens) who graduated with a computer

Juan E. Gilbert even when compared with white women, the discrep- science Ph.D., the graduation trend at CISE is encourag-
is the the Banks
Family Preeminence ancies are overwhelming. The Computer Research As- ing and is an example of what can be achieved.
Endowed Professor
and Department sociation’s Taulbee Survey revealed that in 2019, only To promote retention and graduation of UWOC, CISE
Chair, Department
of Computer seven UWOC (U.S. citizens) received Ph.D. degrees places students with faculty who foster research cultures
Information Science
Engineering, in computer science—a mere 0.43% of all computer and provide holistic advising that enhance success. Fur-
Wertheimer College
of Engineering, science doctorates attained that year and only 2.1% of ther, students receive funding to attend conferences on
University of Florida,
Gainesville, FL, USA. the doctorates awarded to all women. research and community building,
[email protected]
A sincere will to increase the number such as the Grace Hopper Celebration
Jeremy A. M.
Waisome of UWOC in computer science graduate “Although of Women in Computing Conference,
is a lecturer in programs may be effective in getting the Association for Computing Machin-
the Department
of Engineering more undergraduate UWOC to enroll. strides ery Conference, and the Richard Tapia
Education, Herbert A start would be to encourage under- Celebration of Diversity in Computing
Wertheim College
of Engineering, The graduate UWOC to engage in computer have been Conference. Students and faculty at-
University of Florida, science research and then to pursue tend these conferences to network and
Gainesville, FL, USA.
jwaisome@eng. a computer science graduate degree. made...more broaden the participation of underrep-
ufl.edu Another tactic is to establish commu- favorable resented students in computing. CISE
nication with other computer science outcomes are Ph.D. students are encouraged to guide
departments to identify UWOC who welcomed.” undergraduate students in research
are Ph.D. prospects and recruit them to and to connect with other graduate stu-
graduate programs. Once enrolled, they dents and faculty across departments.
must be provided financial support, They also engage in organizations that
effective mentoring, and a supportive provide professional development op-
environment. To reduce the sense of iso- portunities, such as the Black Graduate

lation, faculty leaders should avoid put- Student Association and the Society of

ting UWOC in situations where they are Hispanic Professional Engineers. En-

the only underrepresented persons of color. In addition, rolled students receive sufficient funding to relieve them

faculty and students should ensure that their UWOC col- from financial pressures and are placed in established

leagues engage with and build relational networks within student communities that provide ongoing peer sup-

the computer science academic and professional com- port. Students thrive in CISE’s culture of diversity. The

munities. This will require institutions and departments department has worked to strategically infuse culturally

to understand the existing systems in which UWOC are relevant pedagogy into the curriculum. The department

minoritized and marginalized, and a commitment to dis- faculty currently has four Black American women, two

mantling them. Black American men, and one Hispanic American man.

Many computer science departments express the de- These faculty members provide underrepresented stu-

sire to increase diversity by enrolling more U.S. citizens dents of color with role models who come from similar

of color in their doctoral programs. Although strides cultures, which encourages success and mitigates feelings

have been made at universities such as Clemson, Au- of isolation.

burn, and the University of Florida (UF), more favorable The UF CISE department has recognized an existing

outcomes are welcomed. Computer science departments pool of potential computer scientists among UWOC and

at Auburn, Clemson, and UF share similar features, such has shown the willingness to draw from a source proven

as established connections with historically black col- to be fruitful. With sincere will, other institutions are en-

leges and universities and the recruitment of faculty of couraged to do the same.

color. For example, from 2014 to 2020, the UF Depart- –Henry T. Frierson, Juan E. Gilbert,

ment of Computer and Information Science and Engi- Jeremy A. M. Waisome

10.1126/science.abf3892

502 30 OCTOBER 2020 • VOL 370 ISSUE 6516 sciencemag.org SCIENCE

Published by AAAS

It’s just louder this time

A s if there were any doubt that U.S. President sils, which enhanced our understanding of how human
Donald Trump has no respect for scientists, he life unfolded on Earth, as evidence that evolution was
now refers to public health scholars as “Fauci invalid because scientists were always changing theo-
and all these idiots.” That’s how he’s describ- ries when new data were obtained. He was criticizing
ing experts in virology, immunology, epidemi- scientists for doing science, as my colleague Jon Cohen
ology, and infectious disease. Never mind that recently tweeted. If Pence thinks we can’t change our un-

after recovering from coronavirus disease 2019 derstanding with new data, then we’d have to go back to

(COVID-19), Trump suddenly became excited about fu- breathing phlogiston and being orbited by the Sun. H. Holden Thorp
Editor-in-Chief,
ture vaccines and “Regeneron,” which is what he calls The paradox has played out for years. Many Republi- Science journals.
[email protected];
monoclonal antibodies in general. (Regeneron Phar- cans in Congress have been strong advocates for science @hholdenthor

maceuticals, Inc. is probably thrilled to have achieved funding, especially for the National Institutes of Health,

the product-brand status of Xerox and Kleenex, but Eli although some simultaneously espouse antiscience

Lilly also has developed promising monoclonals, and views and embrace creationism. Biology is the study of

more are in clinical trials.) Apparently, no one told the evolution, and biomedicine is applied evolution. Why

president that scientists from these same fields—many would creationists spend money to study and apply

of whom live in “Democrat-run cit- this heresy? Because they want their

ies” or college towns and are immi- new medicines. They want to tell

grants who wouldn’t be here under “This paradox their constituents that they are fight-
his policies—created these drugs ing diseases that are harming their

and carried out the decades of sci- of loving the families. Arguing for science funding
ence that made them possible. This by promising new cures has been a

paradox of loving the drug but hat- drug but hating winning political strategy for the 75
ing the science is nothing new. It’s the science is years that the United States has had
just louder this time. nothing new.” federally funded science.

Republican presidents were not A recent survey from the Pew Re-
always rhetorically hostile to sci- search Center found that only 20%
ence. As described earlier this year of the political right has “a lot” of
on this page, on the 50th anniver- confidence in scientists. Yet when

sary of Earth Day, James Morton folks at this end of the political

Turner and Andrew Isenberg care- spectrum get sick, they want the

fully traced how the United States got to this point. best treatments that secular academic medicine can

In the 1970s, President Richard Nixon worked hard to provide. The consequences of this are profound and

pass important pieces of public health and environ- especially apparent in the COVID-19 crisis. The same

mental legislation that were approved with large bi- politicians who are criticizing public health guidance

partisan majorities in Congress. Then, when Ronald are praising vaccines and antibodies without acknowl-

Reagan arrived as a candidate in the 1980 election, he edging that they come from the same principles and

advocated teaching creationism in public schools and researchers as masks and social distancing.

mocked environmental science and regulation. In his When the presidential election is over, science will

brand of conservatism, the free market and American face an important choice. Should the scientific com-

exceptionalism could not coexist with a shared respon- munity try to get the missing 80% of the ideological

sibility for caring for the planet or its inhabitants. right to understand its people and its methods? Or

Vice President Mike Pence is carrying on Reagan’s should science write it off as a lost cause and continue

tradition. In a widely viewed speech on the House floor to take the funding while providing the outstanding

when he was a member of Congress, Pence extolled “in- new medicines?

telligent design.” He cited a then-recent study of new fos- –H. Holden Thorp

PHOTO: CAMERON DAVIDSON 10.1126/science.abf4012
30 OCTOBER 2020 • VOL 370 ISSUE 6516 503
SCIENCE sciencemag.org

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NEWS

IN BRIEF
Edited by Jeffrey Brainard

PUBLIC HEALTH

Europe starts shutdowns
amid COVID-19’s second wave

A second wave of coronavirus infections is prompting re- first wave in the spring, Belgium had one of Europe’s highest
newed restrictions across Europe, with countries from rates of cases and deaths, but the Czech Republic was largely
Ireland to Italy imposing nightly curfews and limiting spared. France, Italy, Spain, and the United Kingdom, also
the number of people allowed to gather. The hardest hit hard-hit then, are now reporting tens of thousands of cases
countries, Belgium and the Czech Republic, are report- per day. Authorities in many countries are attempting to use
ing roughly 800 new cases per 100,000 residents per targeted shutdowns to slow the spread of the virus in hot
week. In Prague, the Czech army last week set up a 500-bed spots, leading to empty streets in front of Rome’s Colosseum
field hospital to treat COVID-19 patients, and experts said the (above) and other locations. Ireland has imposed the strictest
Belgian health system was nearing collapse as large numbers restrictions, with most nonessential shops closed nationwide
of health care workers were infected. During the pandemic’s through 1 December.

Extra pandemic deaths hit young resulting for example from lack of access FDA allows first COVID-19 drug PHOTO: RICCARDO DE LUCA/ANADOLU AGENCY VIA GETTY IMAGES
to care for other conditions. The findings
COVID-19 | The United States recorded in CDC’s Morbidity and Mortality Weekly T H E RA P EU T I CS | The U.S. Food and Drug
some 299,000 more deaths than expected Report are a comprehensive analysis of Administration (FDA) last week approved
between late January and early October, U.S. excess deaths, defined as those from the first drug to treat COVID-19, Gilead’s
with big increases among people 25 to all causes beyond what would be expected antiviral remdesivir, despite a lack of
44 years old and nonwhite people, espe- from historical trends, in this case average evidence of efficacy from the world’s larg-
cially Latinos, the U.S. Centers for Disease numbers from 2015 to 2019. The authors est trial of it. The drug is now licensed to
Control and Prevention (CDC) reported reported that deaths among 25- to treat people as young as 12 years old who
last week. Roughly two-thirds of the excess 44-year-olds increased 27%, more than in are hospitalized with COVID-19. Since the
deaths were directly attributable to COVID- any other age group. Deaths rose 54% pandemic’s early days, researchers have
19, the authors estimated; others may for Latinos; from 29% to 37% for other non- viewed remdesivir as one of the most
have been indirectly related to the disease, white groups; and 12% for white people. promising drugs that might be repurposed

508 30 OCTOBER 2020 • VOL 370 ISSUE 6516 Published by AAAS sciencemag.org SCIENCE

against COVID-19. In May, FDA granted an Promises not always kept authors at the Brookings Institution. Some
emergency use authorization for remdesivir 45 cities have adopted targets; their levels
after a U.S. trial found it reduced the median Greensboro, North Carolina, and a few other are generally in line with the goals of the
time to recovery in hospitalized COVID-19 cities are beating their goals for lowering carbon 2015 Paris climate accord and, if achieved,
patients from 15 days to 10. The drug has not emissions, but many are not. Percentages show the would be equal to removing 79 million cars
been shown to reduce deaths among such difference between the actual and target level from U.S. roads. But these “bottom-up”
patients, however. And recently published in the year most recently inventoried. approaches have been buffeted by stiff eco-
data from the World Health Organization’s nomic and political head winds, the report
large Solidarity trial showed no clear mortal- Chicago 52% notes. Many cities lack plans for achieving
ity benefit or reduction of time to discharge the targets, and what plans do exist don’t
from the hospital. FDA did not mention the Tucson, Arizona 47 account for how population growth and
trial in its decision to grant full approval. economic development could boost green-
Madison, Wisconsin 41 house gas emissions.
Japan aims for carbon neutrality
Durham, North Carolina –14 Shortened treatment for TB
C L I M AT E SC I E N C E | Japan this week joined
the growing list of countries that have set Washington, D.C. –15 I N F ECT I O U S D I S E AS E S | A novel com-
target dates to achieve carbon neutrality, bination of existing antibiotics can cure
pledging to reduce greenhouse gas emissions Greensboro –22 tuberculosis (TB) in 4 months instead of
to zero by 2050. Prime Minister Yoshihide six, a study has found. TB specialists say
Suga told the nation’s parliament that Japan m the shorter regimen promises to be one of
plans to meet that target by bolstering con- the most important changes to standard
servation, increasing renewable and nuclear U.S. cities labor to cut emissions treatment since the 1960s. The cocktail
energy generation, and making a “drastic includes four antibiotics, including one,
change” in the use of coal. Environmental C L I M AT E SC I E N C E | Two-thirds of the moxifloxacin, previously reserved for
organizations welcomed the announce- 100 largest U.S. cities that have adopted multidrug-resistant TB, and a high dose
ment but are urging Japan to dramatically targets for reducing carbon emissions are of rifapentine, one of the most commonly
reduce emissions sooner, by 2030, to help falling short of meeting them, according
keep global warming to within the 2015 to a study released last week. Setting those
Paris accord’s preferred target of 1.5°C. They targets is still a worthwhile exercise given
suggest the country ramp up renewable the lack of consensus at the federal level
capacity, drop nuclear power, and phase for how to combat climate change, say the
out coal. Japan, which has the world’s third
largest economy, has been building new coal The OSIRIS-REx
plants to replace electricity from nuclear probe’s sampling arm
reactors idled since the 2011 Fukushima touched its target
Daiichi nuclear disaster. on an asteroid 321 million
kilometers from Earth.

CREDITS: (GRAPHIC) A. CUADRA/SCIENCE; (DATA) BROOKINGS INSTITUTION; (IMAGE) NASA/GODDARD/UNIVERSITY OF ARIZONA Judges nix altering census count PLANETARY SCIENCE

D E M O G RA P H I CS | A panel of U.S. judges NASA grabs its first asteroid sample
last week blocked President Donald Trump’s
plan to leave out undocumented residents in NASA’s OSIRIS-REx probe last week took a bite of the asteroid Bennu and came away
deciding how many seats each state gets in stuffed. The $800 million spacecraft captured a sample of asteroid grit and will ferry
the 435-member House of Representatives. it back to Earth—the agency’s first ever collection of this kind. When OSIRIS-REx
The three judges ruled that subtracting touched its target for 6 seconds with its robotic collector arm, Bennu’s surface proved
undocumented residents from the final surprisingly soft, and the collector penetrated as deep as 50 centimeters. Photos
tally for the 2020 census, which the Census indicate the mission collected far more than the 60-gram minimum required by NASA:
Bureau hopes to deliver by the end of the The collector was overstuffed to the point that a mylar flap wouldn’t close, allowing
year, would violate the U.S. Constitution’s dust to slowly leak out. To prevent further losses, NASA planned to command the
mandate to count every resident, as well as spacecraft to seal the sample in its return capsule this week. Next year, when Bennu’s
federal law on how to carry out apportion- orbit is aligned favorably with Earth’s, the spacecraft will depart, ultimately sending its
ment. The judges didn’t prohibit Census cargo to a parachute landing in the Utah desert in 2023.
officials from following a presidential order
to calculate the number of undocumented 30 OCTOBER 2020 • VOL 370 ISSUE 6516 509
residents in each state, which demographers
say is a nearly impossible task. But the infor-
mation “won’t have any legal weight and
Congress can ignore it,” says Justin Levitt, a
constitutional law scholar. The Department
of Justice has appealed the ruling, by a court
in Northern California, and on 30 November
the Supreme Court will hear arguments in a
similar case from New York.

SCIENCE sciencemag.org

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NEWS | IN BRIEF

used drugs against TB. The combination has learned. They include the Global fund established by a donor to fund eugen-
proved safe and well tolerated in a Biodiversity Information Facility, the Ibero- ics research. UC Berkeley apologized for
randomized, controlled study involving American Federation of Physical Societies, its School of Public Health’s Genealogical
2500 patients. Presented last week the International Science Council, the Eugenics Institute Fund, which in recent
at the 51st Union World Conference on International Union of Pure and Applied years had provided $70,000 annually for
Lung Health, the study took place in Physics, and the Third World Academy of faculty and student research expenses
13 countries. It was run by the Tuberculosis Sciences. Finding the money elsewhere unrelated to eugenics. UC Berkeley froze
Trials Consortium in collaboration with may be a tall order as some membership the $2 million fund in 2018 after faculty
the AIDS Clinical Trials Group. dues exceed $100,000, the organizations members called its origins unethical; it was
say. The government, which has been cut- set up “for the primary purpose of improve-
Mexico cuts off science dues ting the societies’ operating budgets since ment of the human race through research
2019, plans to use the funds to help fight and education in the field of eugenics.” The
SOCIETIES | Mexican scientists say a the COVID-19 pandemic. The move is “very university is considering new uses for the
government funding cut may force them myopic,” says María de la Luz Jímena de money, including financial aid for mem-
to leave a slew of international science Teresa de Oteyza, a former president of the bers of underrepresented minority groups
organizations, which they say would iso- Mexican Mathematical Society. and public education about the damage
late the country and deprive it of scientific wrought by the eugenics movement. For
opportunities. The National Council of Berkeley renounces eugenics fund decades during the 20th century, people
Science and Technology has informed who were Black, poor, or had disabilities
national science organizations that it will H U M A N R I G H TS | The University of were sterilized involuntarily at dispropor-
no longer fund their membership dues for California (UC), Berkeley, said this week it tionately high rates in California and other
at least nine international groups, Science would repurpose and rename a 60-year-old states under eugenics laws.

INVASIVE SPECIES

U.S. murder hornets get rounded up

F or the first time, entomologists last week found a nest of the to the nest in a tree trunk near Blaine, Washington. On 24 October, PHOTO: ELAINE THOMPSON/AP PHOTO
Asian giant hornet—dubbed the murder hornet—in the United workers in protective suits wrapped the trunk in plastic and vacu-
States. The largest hornet in the world (Vespa mandarinia), up umed about 100 hornets from the nest. The tree will be removed
to 5 centimeters long, rarely attacks people. But the hornets and searched for any remaining insects and signs that queens
do capture honey bee hives, decapitating all the bees in hours escaped capture. Researchers reported in the 6 October issue
and claiming the hive as their own. Native to Japan and now found of the Proceedings of the National Academy of Sciences that the
across Asia, the species was spotted last year in Washington state species could spread throughout coastal portions of Washington,
and Canada’s British Columbia province, most likely arriving as Oregon, and British Columbia within 20 years, threatening
stowaways in shipping containers. Researchers trapped several economic losses for growers who depend on bees for pollination.
hornets, fitted them with radio tracking devices, and followed one Researchers continue to search for other nests.

510 30 OCTOBER 2020 • VOL 370 ISSUE 6516 sciencemag.org SCIENCE

Published by AAAS

Since 2014, researchers have deployed more than
150 biogeochemical Argo floats in the Southern Ocean.

IN DEPTH paigns are expensive, and often limited
to common ocean trade routes, says Ken
OCEANOGRAPHY Johnson, a chemical oceanographer at the
Monterey Bay Aquarium Research Institute
U.S. funds new fleet of probes to and a leader of the new program. The floats,
explore ocean biogeochemistry he says, are “not as good as a ship, but they’re
there all the time.”
Drifting Argo floats will track oxygen loss from global
warming and the oceans’ ability to soak up carbon In addition to standard Argo measure-
ments of temperature and salinity, the new
PHOTO: GRETA SHUM/SOCCOM By Paul Voosen answers. This week, the National Science floats will have sensors measuring oxygen,
Foundation (NSF) announced it will spend sunlight, particles, chlorophyll (a gauge of
A single drop of seawater holds mil- $53 million to fund the new floats, mark- phytoplankton abundance), nitrate (a key
lions of phytoplankton, a mix of algae, ing the first major expansion of the Argo nutrient), and pH (acidity). Researchers will
bacteria, and protocellular creatures. array, a set of 4000 floats that for 15 years be watching that last reading closely, be-
Across the world’s oceans these photo- has tracked rising ocean temperatures. “This cause acidity reflects both the ocean’s uptake
synthesizing microbes pump out is going to be revolutionary,” says Wijffels, a of CO2 and its pernicious effect. When the
more than half of the planet’s oxygen, leader of the original Argo program. gas dissolves in seawater, it forms carbonic
while slowing climate change by captur- acid that eventually splits into bicarbonate
ing an estimated 25% of the carbon dioxide The biogeochemical (BGC) Argo floats, in and hydrogen ions, the latter increasing the
(CO2) released from humanity’s burning of development for nearly as long as Argo itself, water’s acidity. Ecologists are concerned that
fossil fuels. But the scale of this vital chemis- will operate much like their forerunners. Af- acidification, already 30% worse in surface
try is mostly a guess, and there’s little sense ter being tossed off a ship, each of the skinny, waters than preindustrial times, will make it
of how it will change as temperatures rise. 1-meter-tall floats drifts with deep ocean cur- more difficult for some phytoplankton, cor-
“What’s happening out there? We have no rents 1000 meters down. Every 10 days or als, bivalves, and many other species to as-
idea really,” says Susan Wijffels, a physical so, it uses an oil-filled bladder to change its semble their shells of calcium carbonate.
oceanographer at the Woods Hole Oceano- density, dropping to 2000 meters and then
graphic Institution. slowly rising to the surface, where it beams Researchers have been testing more than
the resulting profile home. Although instru- 150 prototype BGC floats in the Southern
Soon, 500 drifting ocean floats studded ments lowered from ships can make deeper Ocean since 2014, and the findings are tan-
with biogeochemical sensors will deliver and more precise measurements, ship cam- talizing. This ocean, encircling Antarctica,
is home to two seasonally contrasting CO2
fluxes. In the summer, algae draw down
CO2. But in the winter, ancient carbon,
stashed away for centuries in deep currents
traveling south from the Atlantic and Pacific
oceans, wells up, some escaping into the
atmosphere. Scientists have long assumed
that the carbon absorption dominates, with
the Southern Ocean accounting for a signif-
icant share of the oceans’ global CO2 stor-
age. But because almost no ships ventured
to the stormy, cold Southern Ocean, they
couldn’t check whether the winter release
really was smaller.

In the past few years, Alison Gray, an
oceanographer at the University of Wash-
ington, Seattle, and her colleagues have used
the trial BGC floats to show that the winter
exhalation of CO2 comes close to canceling
out the summer’s gains. She is now seeking
to understand why the outgassing seems to
peak on the Pacific side of the ocean. Surface
winds or currents smashing into undersea
ridges might sweep up more of the deep
waters there. Another explanation is bio-
logical: The region’s phytoplankton might be
less capable than their Atlantic counterparts
at staunching the CO2 outflow.

The BGC floats could also shed light on
a less-known ocean trend: a slow drop in
oxygen. Since the mid–20th century, it has
declined by some 2%. Much of the loss takes

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NEWS | IN DEPTH

place in anoxic dead zones like one in the Archaeologists wearing anticontamination gear sampled Baishiya Karst Cave on a winter night.
Gulf of Mexico, where nutrient runoffs from
overfertilized lands lead to algal blooms, ARCHAEOLOGY
and, eventually, bacterial surges that use
up oxygen in a frenzy of aerobic decomposi- Denisovan DNA found in cave
tion, suffocating fish. But researchers have on Tibetan Plateau
also found that vast tracts of open ocean are
losing oxygen because of warming, which “Molecular caving” shows archaic humans visited
limits water’s ability to hold oxygen, and de- high-altitude cave over long period
creased downward mixing. BGC-Argo could
reveal the true extent of these minimum By Ann Gibbons The find shows that even though their PHOTO: DONGJU ZHANG/LANZHOU UNIVERSITY
zones. “If you eat seafood or care about sea bones are rare, “Denisovans were widespread
life, you should care about deoxygenation,” F or today’s Buddhist monks, Baishiya in this hemisphere,” says University of Oxford
Gray says. Karst Cave, 3200 meters high on the geochronologist Tom Higham, who was not
Tibetan Plateau, is holy. For ancient part of the study. It also ends a long quest for
The floats aren’t only useful for large-scale Denisovans, extinct hominins known Denisovan DNA outside Siberia. “Every year,
trends. For instance, the trial floats discov- only from DNA, teeth, and bits of bone I’ve said we will find this,” says co-author
ered massive phytoplankton blooms in the found in another cave 2800 kilometers Svante Pääbo of the Max Planck Institute for
Southern Ocean, far from typical nutrient away in Siberia, it was a home. Last year, Evolutionary Anthropology (EVA). “It’s been
sources like melting sea ice, suggesting a researchers proposed that a jawbone found a decade.”
seafloor hydrothermal vent was providing long ago in the Tibetan cave was Denisovan,
the nutrients. The floats should also be able based on its ancient proteins. But archaeo- The presence of Denisovan DNA in the ge-
to detect short-lived phenomena such as logist Dongju Zhang of Lanzhou University nomes of living people across Asia suggested
the oxygen loss after a hurricane’s upheaval, and her team wanted more definitive evi- these ancient humans were widespread. But
or the injection of nutrients for species dence, including DNA, the molecular gold the partial jaw from Baishiya Karst Cave was
in the North Atlantic twilight zone, up to standard. So in December 2018, they began the first fossil evidence. Zhang and her col-
1000 meters down, that come from late- to dig, after promising the monks they would leagues identified the jaw as Denisovan based
winter plunges of surface water. “The ability excavate only at night and in winter to avoid on a new method that relies on variation in a
to observe these biogeochemical properties disturbing worshippers. protein (Science, 3 May 2019, p. 418). Some re-
in three dimensions is going to be huge,” searchers questioned the claim, however, be-
says Katja Fennel, an oceanographer at After working from dusk to dawn while cause the method was new, and no one knew
Dalhousie University, who is pushing for temperatures outside plunged to –18°C, then where in the cave the jaw had been found.
Canada to add 40 floats to BGC-Argo. covering traces of their dig every morning,
the scientists’ persistence paid off. On p. 584, Those questions are likely to fade. The dig,
Researchers plan to begin deploying the Zhang’s team reports the first Denisovan led by Zhang and Fahu Chen of the Insti-
new floats next year in the equatorial Pa- ancient DNA found outside Denisova Cave: tute of Tibetan Plateau Research, took many
cific, where El Niño and La Niña drive large mitochondrial DNA (mtDNA) gleaned not sediment samples and found charcoal from
temperature swings every year or two. The from fossils, but from the cave sediments fires, 1310 simple stone tools, and 579 pieces
floats could show how the swings affect the themselves. Precise dates show the Deniso- of bone from animals including rhinos and
ability of phytoplankton to soak up carbon, vans took shelter in the cave 100,000 years hyenas. Paleogeneticist Qiaomei Fu of the In-
offering clues to how a warming climate will and 60,000 years ago, and possibly as re- stitute of Vertebrate Paleontology and Paleo-
change the ocean’s overall carbon uptake. cently as 45,000 years ago, when modern hu- anthropology in Beijing managed to extract
mans were flowing into eastern Asia. hominin mtDNA from the sediment itself.
After the first 5 years of NSF financing, The mtDNA, perhaps shed in poop or urine,
Johnson and his colleagues would likely
need support from the National Oceanic
and Atmospheric Administration, which
pays for much of the main U.S. Argo fleet.
Expanding to 1000 floats, as the team hopes,
would require funding from France, Austra-
lia, Canada, China, and other countries. At
some point, they hope the Argo fleet will be
bolstered by 1200 deep Argo floats, which
can sink to 6000 meters without crush-
ing (Science, 8 September 2017, p. 956).
But money for upgrading the fleet, which
would remain at 4000 total floats, has been
elusive—even though Argo is a relative bar-
gain compared with ships.

If anything, the pandemic has under-
scored that point, Johnson says. “We’re all
sitting at home now,” he says. Yet out in the
ocean, the robotic fleet calls home week
after week, capturing otherwise invisible
changes. “Ten years ago, the ship was the
observing platform,” Johnson says. “Now,
it’s the tender.” j

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most closely matched that of Denisovans. COVID-19
Meanwhile, geochronologists led by Bo
Herd immunity? India still has
Li and Zenobia Jacobs of the University of a long way to go, scientists say
Wollongong dated material from those same
sediment samples. They used optical dating Cases are dropping, but critics question optimistic forecast
to reveal when light last struck mineral grains
in the samples, showing when each grain was By Vaishnavi Chandrashekhar, in Mumbai for antibodies in a population to gauge the
buried. The four layers that yielded Deniso-
van mtDNA were laid down 100,000, 60,000, fraction already infected—have found much
and as recently as 45,000 years ago, although
the younger sediments were disturbed. L ast week, a panel of leading scientists higher infection rates in Indian cities, and
appointed by the Indian government in particular in slum areas. Studies in Au-
The dates for the older sediments seem delivered a startlingly optimistic gust, for example, found antibodies in 41%
highly reliable, says Higham, who dated message: The world’s second largest of residents of Mumbai’s slums, compared
Denisova Cave. And by showing DNA and COVID-19 epidemic has rounded a with 18% elsewhere in the city. “Many dense
dates can be gleaned from the same sedi-
ment samples, the work opens “a new era corner. India’s daily number of cases pockets that can be easily infected have
of molecular caving,” says Oxford geo-
chronologist Katerina Douka. has declined by roughly half in the past [likely] already been infected,” Babu says.

The charcoal in the cave shows its occu- month, and a new mathematical model That could help explain the slowdown in
pants built fires. They also used simple stone
tools, and, from the cave’s high opening, must suggests “we may have reached herd im- new infections but suggests many more
have spied on animals grazing in the mead-
ows below. Some may also have been on the munity,” the panel wrote in a paper published people remain vulnerable.
lookout for modern humans, who were in the
region by 40,000 years ago. online by The Indian Journal of Medical Re- Gautam Menon of Ashoka University,

In a separate study on p. 579, Pääbo reports search. Assuming measures such as social a co-author on several COVID-19 model-
extracting modern human DNA, the oldest
yet in Asia, from 34,000- and 40,000-year-old distancing, wearing masks, and hand wash- ing studies, adds that the model suffers
fossils from what is now Mongolia and from
near Beijing, respectively. Those genomes ing remain in place, the group said the pan- from “a lack of epidemiological realism”
included Denisovan DNA, the legacy of mat-
ing that happened roughly 50,000 years ago. demic could be “controlled by early next year.” because it assumes an unusually large
But the Denisovan sequences differed from
those found in living New Guineans and But other scientists say the fraction of infected people re-
Australian Aboriginals. Homo sapiens must
have met and mated with two populations of “There are 100model overestimates the num- mains asymptomatic. He says
Denisovans—one in mainland Asia and one 200 million to 300 million is
in Southeast Asia, says EVA paleogeneticist ber of people already infected
Diyendo Massilani—further evidence that
they were once numerous and wide-ranging. and warn that with colder or more small a better estimate for the num-
temperatures and several re- epidemics in ber of infected people.
The Denisovans bequeathed a particular ligious holidays approaching, different states
genetic gift to modern Tibetans: a “super- India may well see a second Experts agree that spread
athlete” variant of a gene, called EPAS1, that wave. The positive national in rural areas, home to more
helps red blood cells use oxygen efficiently than half of the population, is
and is found in Denisovans from Denisova
Cave. Zhang and her colleagues think the and cities, risingtrends hide a more complex a challenge to both monitor
Tibetan Plateau Denisovans may have been and fight. Testing isn’t easily
adapted to life at high altitude, and that picture, suggests Giridhar
EPAS1 may have spread widely among them,
before they handed it on to modern Tibetans. Babu, an epidemiologist with and falling at available in many small towns
the Public Health Foundation and villages; serosurveys sug-
But molecular dating suggests EPAS1 of India. He believes the virus
spread rapidly only in the past 5000 years. different times.” gest official testing, now at
And natural selection would have favored may have burned through large, 1 million per day, vastly un-
that gene variant only in people who lived at densely packed populations but T. Jacob John, dercounts actual cases. Some
high altitude year-round, says archaeologist will continue to spread in ru- Christian Medical College states rely heavily on so-called
Mark Aldenderfer, professor emeritus at the
University of California, Merced. The Den- ral areas, at a lower rate, for rapid antigen tests, which
isovans may have lived only seasonally in the
cave. Zhang’s team will need to find nuclear many months: “We still have large num- range widely in sensitivity. Meanwhile, the
DNA to test its hunch.
bers of people for the virus to go through.” health infrastructure in many of India’s
Zhang expects more digs at the cave will
clarify the issue with DNA and perhaps fos- The encouraging projections come from rural states is weak, making it harder to
sils. “The study of this cave is only begin-
ning,” she says. j the National Supermodel Committee, treat patients.

which modeled the past and future of In- More granular data might help scientists

dia’s epidemic at the government’s request. better understand the pandemic’s trajec-

Its work suggests 380 million Indians had tory. The national epidemic is a “figment of

already been infected by mid-September statistical imagination,” says T. Jacob John,

and that there might be “minimal active former head of the department of viro-

symptomatic infections” by late February logy at Christian Medical College; instead,

2021 if control measures continue. (The “There are 100 or more small epidemics in

study also concluded that by flattening the different states and cities, rising and falling

curve, India’s lockdown in the spring saved at different times,” he says.

up to 2.6 million lives.) Babu warns against complacency. “The de-

The model did not take regional differ- cline [in cases] is real and valid, but no one

ences in viral spread into account. But Babu should rejoice yet,” he says. “It only means

notes that serological surveys—which test that the first set of formidable challenges is

over, and the next set is beginning.” j

Science’s COVID-19 reporting is supported by the
Pulitzer Center and the Heising-Simons Foundation. Vaishnavi Chandrashekhar is a journalist in Mumbai.

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NEWS | IN DEPTH

VOICES OF THE PANDEMIC

How an immunologist pivoted to tackle COVID-19

For Akiko Iwasaki, the pandemic has brought new research priorities—and new urgency

By Jennifer Couzin-Frankel where she studies how the body responds to patients in Connecticut to map the spread

and combats viruses. “Having to adapt to there and across the United States. She

U ntil this year, Akiko Iwasaki’s lab had different situations throughout my life,” she also launched a separate study to examine
never handled so many tubes of hu- says, “prepared me [for] a different virus.” patients’ immune responses, recruiting
man blood. “We were mostly work- 113 people with COVID-19 at Yale New
ing with mouse models,” says the Yale The shift called for new science, new col- Haven Hospital and redeploying skills in
University immunologist, who speaks laborations, and new skills. In February, her lab to make the project happen. Post-
Iwasaki’s lab joined a universitywide test-

precisely and thoughtfully. “We used ing effort for SARS-CoV-2 led by Albert Ko, doctoral fellow Carolina Lucas had been

to look at the data and contemplate it.” Then Nathan Grubaugh, and Anne Wyllie at Yale’s studying the mosquito-borne chikungunya

COVID-19 struck, and such unhurried mus- School of Public Health. Alice Lu-Culligan, a virus, and her project was housed in a bio-

ings flew out the window. In a matter safety level 3 lab at the university, the

of weeks, Iwasaki overhauled her re- kind used for hazardous pathogens.

search to launch a slew of studies on “Akiko asked me to coordinate this,”

how the new virus, SARS-CoV-2, takes says Lucas, who quickly agreed.

its toll on patients. She and her nearly Every few days, the team collected

two dozen lab members know their samples from the nose, throat, and

discoveries could impact people falling blood of patients. There were “all these

sick right now. “Every minute counts.” weird immune responses being en-

In the months since, she has pro- gaged,” Iwasaki says. In severe cases,

duced a string of high-profile papers the immune system churned out a

by redirecting her expertise in the im- flood of cytokine proteins. Lucas,

mune system, honed in mice, to ques- Iwasaki, and others found four im-

tions such as why men are more likely mune signatures that appeared to

to get severely ill and how immune correlate with later outcomes. That

responses in hospitalized patients can paper appeared in Nature in July.

help predict their prognosis. Now, Swiftly, the scientific questions

she is turning her attention to long- mushroomed. In mid-March, the

haulers, people who suffer a bout with Yale hospital treated a woman with

the virus and don’t fully recover. COVID-19 who was in her second tri-

Iwasaki has had decades of practice mester of pregnancy. The woman lost

adapting to new circumstances. As a her fetus—and a private tragedy be-

child growing up in rural Japan, she came interwoven with urgent ques-

dreamed of becoming a poet, turned tions about whether the virus could

off science by her physicist father’s im- infect the placenta and pose a dan-

mersion in his profession. “We’d go on ger to a pregnancy. A collaborator of

vacation and he’d bring papers with Iwasaki’s secured permission to col-

him,” she says, laughing. “I thought, lect the placenta, and late one night,

‘What kind of life is this?’” But when “Having to adapt to different Lu-Culligan retrieved it. Until that
a high school teacher hooked her on situations throughout mylife prepared moment, the only placentas Lu-
math, she began to reconsider. Soon Culligan had seen belonged to mice.
after, 9 months as an exchange stu- “This is big and bloody,” she says, and

dent in Canada left her itching to es- me [for] a differentvirus.” as she stared at it under a biosafety
cape the expectations for a woman in hood, “I’m thinking, ‘I don’t know

Japanese society—marry a nice man Akiko Iwasaki, Yale University what I’m doing here.’”

and have a family. Her mother, who In that case, the virus had indeed

worked at a local radio station, had endured graduate student of Iwasaki’s who had been infected the placenta, and Lu-Culligan

jeers from co-workers for sticking with the studying the immune system during preg- began to collaborate with Yale obstetri-

job while raising three children. “Know- nancy in mice, recalls the scramble. Lab mem- cians to recruit women delivering at the

ing how much she stood up for always has bers scouted for supplies such as swabs and hospital who were positive for the virus

stayed with me,” Iwasaki says. equipment. “We were going around our floor, to study their placentas, too. That paper is ILLUSTRATION: KATTY HUERTAS

So she reimagined her future, embracing to the neighboring labs, seeing how many nearing completion.

science and leaving Japan. She enrolled as an PCR [polymerase chain reaction] machines Meanwhile, Iwasaki began to investi-

undergraduate at the University of Toronto— they had,” Lu-Culligan says. It was “full-on gate sex differences and found the male

falling hard for immunology her senior year sprint mode, collaboration and chaos.” immune system is more likely to spark a

there—and stayed on for graduate school. Iwasaki’s lab began to help Grubaugh’s harmful inflammatory response to the vi-

Twenty years ago she founded her lab at Yale, group sequence viral genomes from early rus, whereas in women, T cells that fight

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it off are activated more robustly. These PEER REVIEW
distinctions, she reported in an August
paper in Nature, might help explain why Edit reviews without permission?
men who are infected tend to fare worse Some journal editors say it’s OK
than women.
Deleting offensive language is common, but some
Iwasaki’s juggling act impresses her col- editors alter reviewers’ overall recommendation
leagues. “She’s made it seem so effortless,
even though I know it’s probably not ef- By Cathleen O’Grady to find out how widespread this practice was.
fortless at all,” says Angela Rasmussen, a With colleagues, they’ve now surveyed
virologist at Columbia University’s Mail- F iona Fidler, a metaresearcher at the
man School of Public Health. Iwasaki’s University of Melbourne, was outraged. 322 editors at high-impact journals across
husband, Ruslan Medzhitov, is also a well- She had discovered that her appraisal ecology, economics, medicine, physics, and
known Yale immunologist (they discuss of a submitted paper had been changed psychology on when they think altering
COVID-19 while walking their dog), and before being sent to the author, some- peer-review reports is justified. Published as
the pair has two daughters, ages 11 and 13. times drastically. The words “very a preprint earlier this year at the Open Sci-
Iwasaki fears the pandemic is widening sympathetic” had become “generally sympa- ence Framework and now under review at
the gender gap in science as women face thetic.” “This one is a good example” ended eLife, the survey reports that 91% of the re-
disproportionate pressure to support their up as “this one still needs work.” Worst of spondents identified at least one situation in
children when schools are closed. Her hus- all, she felt that the bottom line of her peer- which they would edit a report. More than
band drives their daughters to in-person review report to the journal Educational and 80% said they would do so if a reviewer used
school each morning, but with COVID-19 Psychological Measurement, recommending offensive language or made inappropriate
cases climbing, she wonders how much that it accept the paper with minor revisions, personal comments about the authors. But
longer schools will be open. was misrepresented in the editor’s rejection 8% said they would change the reviewer’s
letter to the author. overall recommendation—even without their
Solutions to a COVID-19–fueled gender permission, a finding that shocked Hoekstra.
gap in science are elusive, she says, “other “I had never experienced anything like He believes that’s probably an underestimate,
than to really have a different mindset this before,” Fidler says about the 2012 inci- given the stigma of admitting to such dubi-
about evaluating progress in science dur- dent. She demanded explanations from the ous behavior in a survey. “I think there are
ing this time.” Iwasaki has long advocated journal editor. And she later partnered with probably even more who actually do it.”
for female and minority scientists on Twit- the snubbed paper author, Rink Hoekstra, a
ter, where she has 80,000 followers. In one psychologist at the University of Groningen, The survey comes amid a wider push for
post, she minced no words in advising fe- consistent guidelines. There’s little dispute
male scientists who worry about pregnancy
torpedoing a job interview: “If they don’t Red lines
welcome you with open arms and offer
child care options, they don’t deserve you.” A survey of 322 editors at high-impact journals has found a wide range of attitudes toward altering peer-review
reports. About 8% believe it’s OK to change the reviewer’s recommendation, even without permission.
Her advocacy goes beyond rhetoric. Lu-
GRAPHIC: HAMILTON ET AL., METAARXIV, 10.31222/OSF.IO/QKJY4 (2020), ADAPTED BY A. CUADRA/SCIENCE Culligan met Iwasaki at a luncheon for Never acceptable Acceptable to edit Acceptable to edit,
women in science at Yale, while struggling to edit the report without reviewer’s but only with
with bullying and harassment in another
lab. Iwasaki said, “We have to get you When a reviewer has used 15% permission reviewer’s permission
out of there,” Lu-Culligan recalls. A few inappropriate or ofensive 17% 58% 26%
months later, the young scientist aban- language (N=291)
doned more than 2 years of graduate work 17% 56% 27%
to start over with Iwasaki—later learning When the reviewer has made
that she wasn’t the first person her new an inappropriate reference to an 62% 21%
mentor had rescued from a miserable ex- author’s gender, age, etc. (N=290)
perience elsewhere.
When the reviewer has left in their
Some 8 months into the pandemic, lab comments to the editor (N=290)
life has settled down—somewhat. Iwa-
saki’s latest passion is long-haulers who When the review has English 33% 42% 25%
can’t shake symptoms like fatigue and language problems (N=292) 34% 39% 27%
brain fog. Volunteers find her via word of 35%
mouth. The project faces hurdles, though: When a reviewer identifes 48% 17%
Iwasaki is hunting for a facility to draw themself in a blinded peer- 81% 8% 11%
blood from her volunteers, who are still review framework (N=276)
symptomatic and potentially contagious.
With many competing studies, such space When there are spelling and/or
is at a premium and she hasn’t yet been grammatical errors in the review
able to secure any. She’s also racing to ap- (N=294)
ply for grants to fund the project.
When the editor disagrees
“We really want to get to the bottom with the reviewer’s
of what’s going on,” she says impatiently. recommendation (N=293)
Until then—along with so many other
researchers—she’ll be in overdrive. j

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NEWS | IN DEPTH

that editors should intervene when peer- been deleted. Other sentences criticizing NEUROSCIENCE

review comments are hostile. Such com- Hoekstra’s methods had been added. She Efforts to
control monkey
ments have a disproportionate impact on emailed Marcoulides, who replied that the brains get
a boost
minorities and other marginalized groups, journal computer system sometimes blended
With open data project,
inducing self-doubt and harming productiv- and distorted reviewer comments. primate optogenetics
confronts stumbling blocks
ity, according to a 2019 PeerJ paper. It’s not Fidler calls that explanation “preposter-
By Kelly Servick
just ethical to edit such review reports—it’s ous,” saying it would be impossible for a tech-
W hen neuroscientist Sébastien
essential, says Seth Leopold, editor-in-chief of nical glitch to create “perfectly grammatical Tremblay set out to manipulate
monkeys’ brains with light, col-
Clinical Orthopaedics and Related Research. sentences that are exactly opposite in mean- leagues had sobering advice: “It’s
more difficult than it sounds.”
Jane Alfred, director of Catalyst Editorial, ing.” She reached out to contacts at SAGE, the Tremblay, who works in neuro-
scientist Michael Platt’s lab at the University
which offers training on research integrity journal’s publisher, who said they would in- of Pennsylvania, uses light to activate or si-
lence precise groups of neurons and probe
and publication ethics, thinks it’s best to vestigate, but she heard no more from them. their role in brain function. The method,
called optogenetics, works well in rodents,
return reports containing hostile language In an email to Science, a SAGE spokesperson but studies in nonhuman primates are criti-
cal if it’s ever going to become a therapy for
and ask the reviewer to change it. Review- wrote that the publisher “addressed the issue humans—to suppress seizures, for example,
disrupt tremors in Parkinson’s disease, or
ers are often grateful for the chance to re- directly with the editor at the time” and that even project images into the brain of a blind
person (Science, 8 November 2019, p. 671).
vise ill-considered comments, she says. But Marcoulides now double-checks reviewer
But in spite of more than 10 years of work,
Leopold says this may be impractical at comments for consistency. progress has been slow. The tools for render-
ing cells light sensitive were largely refined
fast-paced journals, and trying to educate Later in 2012, Marcoulides invited Hoeks- in rodents and behave unpredictably in mon-
keys. It’s hard to illuminate enough tissue
reviewers who make unprofessional com- tra to resubmit his paper. This time, Fidler’s in large primate brains to reliably change
animals’ behavior. Researchers have devised
ments is likely futile. It’s better, he says, not review made it through intact, and Hoeks- their approaches by trial and error, often
without knowing what had or hadn’t worked
to ask that person to review again. tra’s paper was accepted—pivotal for others.

Changing a reviewer’s recom- “I think it’s for him winning a permanent Tremblay, Platt, and colleagues from
mendation is another matter, especially job at Groningen. In an email 45 primate optogenetics labs in nine coun-
says Howard Browman, a council important to Science, Marcoulides wrote tries hope to change that with the Nonhuman
member of the nonprofit Com- that the reviewer comments au- Primate Optogenetics Open Database, which
mittee on Publication Ethics, tomatically attached to his deci- published its first results last week. The data-
base contains minute details of successes and
which is developing guidance that [editors] sion letter were “distorted” and failures, many of which have gone unpub-
on how to navigate the ethics have really his edits were intended to clarify lished. And if it can be sustained, it may soon
of editing reviewers’ comments. hard and his interpretation of Fidler’s as- include tests in monkeys of promising new
“It’s so obviously something you sessment. “In hindsight, I should optogenetic tools. The open-data approach
wouldn’t do,” he says. have contacted her rather than “is tremendously powerful, tremendously
useful to the community,” says Hongkui Zeng,
fast rules forYet it apparently happened attempting to resolve the prob- a neuroscientist who develops optogenetic
lem on my own,” he wrote. He tools for mice at the Allen Institute for Brain
to Fidler, who stumbled on the Science and was not involved in the project.

themselves.”changes to her report by accident. added that he still sometimes In optogenetics, researchers endow brain
edits reports for clarity or to re-
Although the review process was

double-blinded, she recognized Simine Vazire, move inappropriate language.

the paper as Hoekstra’s because Collabra: Psychology Few journals offer explicit guid-

she had seen him present the ance on when editing peer-review

work, on Ph.D. students’ statistical reasoning, reports is and isn’t permissible. Alfred says

at a conference in Slovenia. So after sending they ought to, and should also allow review-

in her review, she emailed him to congratu- ers to opt out from being edited. No matter

late him and tell him that her review was nit- how well-intentioned editors may be, she

picky but positive. says, clear policies will ensure a transparent

That same day, Hoekstra’s paper was re- and unbiased process. Many journals have a

jected by the journal. “The reviewers have safeguard: They share all reviews and the edi-

spoken in nearly a single voice in their rec- torial decision with reviewers, allowing them

ommendation to me that I decline publica- to see how their comments were communi-

tion of the paper in its current form,” wrote cated to the authors. But about 20% of the

the editor-in-chief, George Marcoulides, a editors in the survey report that their jour-

research methodologist at the University of nals do not send out either the reports or the

California, Santa Barbara. Although editors decision letters to reviewers.

may override reviewer recommendations, Simine Vazire, editor-in-chief of Collabra:

the normal practice is to explain this in the Psychology and a colleague of Fidler’s, ar-

decision letter. Hoekstra wrote back to Fidler, gues for a bright line on the question: no

attaching the two reviews he got from the edits without reviewer permission. Her

journal and asking for suggestions of other journal has no policy on the issue, but she

journals that might publish the work. is considering proposing one. Without clear

When she saw the reviews, Fidler cot- boundaries, she says, it becomes easy to

toned on. “I think we have a controversy rationalize changes, adding that journal

on our hands,” she wrote to Hoekstra. She editors have lots of power and little ac-

downloaded her review from the online jour- countability. “There’s no one watching over

nal system, and compared it, word by word, editors,” she says. “I think it’s especially im-

with the review Hoekstra received. Her sen- portant that they have really hard and fast

tence saying her concerns were minor had rules for themselves.” j

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Methods to influence rodent neurons using light have
not translated smoothly into primate brains.

CREDITS: (PHOTO) JOHN SERRAO/SCIENCE SOURCE; (GRAPHIC) C. BICKEL/SCIENCE cells with a gene for one of several opsins, In a 19 October paper in Neuron introduc- brain, Tremblay says. A single injection can
light-sensitive proteins from microbes. These ing the database, the team estimates the suc- infect about 1 cubic millimeter of tissue—a
proteins can influence the flow of ions in and cess rate of the most commonly used vectors, broad swath of a mouse’s brain, but a puny
out of a neuron to control whether it fires promoters, and opsins in the data set. About fraction of a monkey’s. And scientists want to
an electrical signal. Depending on the opsin, half of the experiments in monkey brains avoid multiple injections that could cause ex-
researchers can excite or inhibit neurons by looked for changes in neural activity after cessive tissue damage. Instead, some labs are
shining light on them, usually via an im- cells were hit with light; 69% found a strong trying to send the virus farther by injecting it
planted optical fiber. effect. Of the 20% of experiments that aimed at high volumes and pressures, a technique
to influence an animal’s behavior—to prompt called convection-enhanced delivery.
Strains of mice have been genetically en- an eye or hand movement, for example—
gineered to express opsins in their brains nearly half saw a weak effect or none at all. Others hope to eliminate the need for
from birth. But for now, getting an opsin brain injections by designing viruses that
into monkey neurons means infecting the Failure likely discouraged some re- are small enough to cross into the brain
cells with a virus injected through a hole in searchers from publishing studies, says via its tiny capillaries after being infused
the skull. Along with opsin DNA, the virus Julio Martinez-Trujillo, a neurophysiologist into a vein. In a June preprint on bioRxiv,
typically carries a sequence called a pro- at Western University and contributor to the neuroscientist and bioengineer Viviana
moter, which restricts the opsin’s expres- project. His group has tried, without success, Gradinaru and her team at the California
sion to certain cell types. to evoke eye movements in one macaque and Institute of Technology describe such an
to impair working memory function in an- engineered virus that selectively infects the
There’s no proven formula for getting mon- other. “This is the first paper that shows our neurons of a marmoset.
key brain cells to make opsins. In the hunt experience,” he says.
for the right combination of viral strains and Delivering light to large brains is a hur-
promoters, “we kind of entered this voodoo Such attempts probably fail in part be- dle as well. “Say I am using a 200-micron-
land,” says Arash Afraz, a neuroscientist at cause the virus doesn’t reach enough of the diameter fiber optic for stimulating my
the U.S. National Institute of Mental Health. mouse brain,” Afraz explains. “To scale that
Scientists relied on rumors of other labs’ suc- Scaling up up, I’d have to stick a flashlight in the mon-
cesses and failures, he says, and were afraid key’s head.” In a bioRxiv preprint last month,
to vary a recipe once they got it working. Un- Monkey brains have been harder to manipulate Afraz and colleagues describe a possible
like with plentiful mice, researchers couldn’t with light than mouse brains, in part because alternative: a 5-square-millimeter array of
afford to use lots of monkeys to hone their they’re much larger. 24 light-emitting diodes (LEDs), each of
technique, he adds. “We value them more. which can produce as much light as a typical
They have names. We view them as our col- Optical fber Macaque optical fiber. By laying this array over a mon-
leagues, in a sense.” Mouse key’s cortex, researchers might illuminate a
relatively broad brain area without multiple
Afraz hopes the database, which he con- implanted fibers, Afraz says. They can also
tributed to, will minimize wasted effort use individual LEDs to excite separate parts
by pooling the field’s failures. It catalogs of the cortex in precise patterns.
1042 viral injections performed in non-
human primates, 552 of them previously un- Other groups are developing more sensi-
published. Seven-tenths of the experiments tive opsins so that weaker light can affect
were in rhesus macaque monkeys. Tremblay more distant tissue. In a study in mice re-
can’t be sure the database is exhaustive, but ported on 5 October in Nature Biotechno-
the 66 groups he invited to contribute— logy, a group led by Stanford University
identified through publications and refer- neuroscientist Karl Deisseroth—one of the
rals from colleagues—represent the major- original developers of optogenetics—used
ity of labs active in the field, he says. a highly sensitive opsin called ChRmine to
activate neurons several millimeters below
the brain’s surface with light from outside
the rodent’s skull.

“I can’t wait to test them,” Laval Univer-
sity molecular biologist Marie-Ève Paquet
says of these ultrasensitive opsins. She’s
part of a Canadian collaboration that tests
and disseminates emerging optogenetics
tools. As opsins, promoters, and viruses
make their way to participating research
groups, Paquet’s team plans to upload its
results to the new database.

To keep the database up to date, she says,
“the community really has to be motivated,”
especially because she expects the next few
years to bring a boom in studies to influ-
ence and understand the brain circuits of
some of our closest animal relatives. j

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The 110 members
of the U.K. Climate

Assembly were
randomly selected.

FEATURES

POWER TO THE PEOPLE

Nations are turning to citizen assemblies to weigh up climate policies

U ntil recently, Sue Peachey, an By Cathleen O’Grady announced their own upcoming climate as- PHOTO: FABIO DE PAOLA/PA WIRE
apartment building manager in semblies, although they have been delayed
Bath, U.K., didn’t think much was more than a focus group or a town hall by the coronavirus pandemic. And at the
about climate change. “I did my meeting: It was an experiment in handing regional and local level, dozens of citizens’
recycling,” she says. “I just wasn’t political power to a random but representa- juries and councils have drawn up policies
aware of how serious it was.” She tive set of citizens. Last month, it produced on climate adaptation, air quality, and envi-
never imagined the U.K. Parlia- its final report, and its recommendations ronmental protection.
ment asking for her advice on cli- will shape debates in Parliament.
mate policy. But last year, a letter Advocates say these carefully designed
arrived in her mailbox inviting her to do The U.K. Climate Assembly is one of a “minipublics” can break political stale-
just that, by joining the United Kingdom’s growing number of similar gatherings pop- mates by bringing together citizens to
first ever climate assembly. “I’d never done ping up across Europe, many of them charged hear evidence and deliberate. They point
jury service—I’d never done anything like with addressing climate change and other to evidence of high-quality policy created
it before,” Peachey says. She thought about science-heavy issues. A citizens’ assembly in by fresh and diverse perspectives, and to
her stepchildren and stepgrandchildren, Ireland that deliberated from 2016 to 2018 behavioral research showing the power of
and the legacy they would inherit. “That led to a referendum that legalized abor- guided deliberation to change minds and
was the main reason why I thought, ‘Well, if tion and a government plan to quadruple reduce polarization. What began as an ab-
somebody is going to have input on it, why its carbon tax by 2030. This year in France, stract, academic model has taken off in real-
shouldn’t it be me?’” an assembly made 149 climate policy rec- world settings, says David Van Reybrouck,
ommendations, and President Emmanuel a Belgian historian, author, and advocate
So, Peachey signed up to spend four week- Macron has agreed to push for 146 of them, of minipublics. “We’ve really seen a wave, a
ends driving to Birmingham to listen to ex- including making “ecocide” a crime and in- surge, of deliberative democracy.”
perts, deliberate with 109 fellow citizens, and cluding climate goals in the French consti-
recommend climate policies. The assembly tution. Spain, Denmark, and Scotland have Claudia Chwalisz, a policy analyst who
has tracked the growing wave of mini-

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NEWS

publics for the Organisation for Economic a car would now be further disadvantaged. mitments to the 2016 Paris agreement. But
Co-operation and Development, a club of When Van Reybrouck started to talk about since then, there’s been no action to meet
economically developed nations, says these minipublics, he says, “[Macron] puts down the goal, says Darren Jones, a Labour Party
deliberative bodies are well-suited to tack- his fork and takes a ballpoint and starts politician. “We’ve legislated this target, and
ling long-term issues because citizens need taking notes.” that’s great,” he says. “But now how are we
not worry about the short-term incentives going to get there?” Climate policies need
of electoral cycles, giving them more free- The next month, Macron’s administration the backing of the public, Willis says, which
dom than elected politicians. A minipublic walked back the tax hike and announced means the public should be involved in
can also embody a wide range of perspec- a series of public town hall meetings for creating them. And so, like Macron, Jones
tives, an advantage for problems with com- citizens to air grievances. In April 2019, and other members of the U.K. Parliament
plex trade-offs and value-based dilemmas. Macron announced the Citizens’ Conven- asked the public to help.
Climate policy, she adds, ticks both boxes. tion on Climate. Among the assembly’s
many eventual proposals were a fuel tax Peachey was one of the 30,000 people
Letting ordinary people determine cli- for recreational aviation, an insurance tax whose postcode came up in a random lot-
mate policy might seem risky, but “if climate
scientists have learned anything over the last
couple of decades, it’s that they can’t just do
the science and expect it to speak for itself,”
says John Dryzek, a political scientist at the
University of Canberra who wants to use the
approach to tackle another fraught science
issue. Last month, he and other minipublic
advocates published a call for what would be
the first global citizens’ assembly. He wants
it to take on the issue of genome editing, on
the grounds that its widespread ramifica-
tions demand international agreements. For
this and many other science policy questions,
he argues, minipublics are an excellent way
to integrate public values with advice from
scientists and ethicists. “Scientists don’t have
a monopoly on public values,” he says.

RANDOMLY ASSIGNING CITIZENS to positions The U.K. Climate Assembly deliberated in Birmingham, after hearing from climate scientists and advocacy groups.
of political power has a history stretching
PHOTO: FABIO DE PAOLA/PA WIRE back to ancient Greece, where the Athe- based on vehicle emissions, and a tax on tery to choose potential participants, and
nians used the practice to select magistrates vehicle weight—but no fuel tax for drivers. one of 1748 people who responded to the in-
and members of their representative Coun- vitation. An algorithm whittled the sample
cil of Five Hundred. But the architects of Macron’s situation was hardly unique. down to 110 people who matched the over-
electoral systems in postrevolution France Governments are hamstrung by the prob- all U.K. population’s gender, age, ethnicity,
and the United States preferred a republi- lem of climate action, says Rebecca Willis, education level, geographic region—and,
can system of professional politicians—an an environmental social scientist at Lan- crucially, their degree of concern about cli-
“elected aristocracy”—over outright rule caster University who helped choose expert mate change. This two-stage process limits
by the masses, Van Reybrouck says. “They speakers for the U.K. Climate Assembly. She the influence of self-selection, which skews
were as much afraid of democracy then as interviewed U.K. politicians and studied toward people who already have strong in-
we would be of anarchy today.” their speeches and found that they under- terests in a topic and drives polarization,
estimated public support for climate action. says Stephen Elstub, a political scientist at
Now, however, electoral democracies “They didn’t feel under any pressure to Newcastle University who is studying how
are floundering in the face of partisan- act,” she says. Politicians also tend to over- well the U.K. Climate Assembly worked.
ship and populism. In November 2018, estimate the opposition of a vocal minority
Van Reybrouck attended a lunch during to some climate measures—such as onshore The nonprofit Involve, contracted by Par-
a French state visit to Belgium and was wind farms, she says. And they fear punish- liament to run the assembly, tried to eliminate
pulled into a conversation with Macron. At ment at the ballot box, where citizens ex- barriers to entry, says Sarah Allan, Involve’s
the time, France was on fire: Thousands of press their opinions about a multitude of head of engagement. The team chose Bir-
protesters furious at the prospect of a fuel policies at the same time: “Voting is such a mingham as a geographically central city and
tax hike were expressing their rage in the blunt instrument.” arranged travel, accommodation, child care,
streets. “What did they want me to do?” Van and accessibility adaptations like large-print
Reybrouck recalls Macron asking in frustra- In mid-2019, the United Kingdom set reading materials. They covered all the mem-
tion. “They want me to save the environ- a target of net zero carbon emissions by bers’ costs, paying upfront when necessary so
ment and at the same time to keep petrol 2050, a first step toward keeping its com-
prices low.”

Bringing citizens into the discussion
would help, Van Reybrouck says he told
the French president. Not everyone in
France has access to public transit, and
those already struggling with the costs of

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NEWS | FEATURES

as not to exclude members who couldn’t pay agreed, and 95% felt they were given “ample reform in Northern Ireland. A deliberative

out of pocket. And they paid all members an opportunity” to express their views. In an poll held in Dallas last year saw Repub-

honorarium of £150 for each weekend, a lure age of polarization, a willingness to respect- licans and Democrats moving toward a

to those with little preexisting interest in the fully hear other views, and the reasons peo- middle ground on divisive issues such as

subject. “It’s really important to try and get ple hold them, changes the hostile dynamic refugee resettlement and a minimum wage.

the people who wouldn’t normally partici- of politics entirely, says Alice Siu, a political Across the board, the researchers found

pate,” Elstub says. scientist at Stanford University: “Something participants could back up their opinions

magical happens.” with clear reasoning. Siu, analyzing tran-

ON A GLOOMY FRIDAY evening in late Janu- Some researchers contend that entrust- scripts from these experiments, has found

ary, the assembly members gathered for ing policymaking to ordinary citizens that men and women contributed equally

the first time on the top floor of the glossy, is risky. Cass Sunstein, a legal scholar at to discussions, contrary to expectations that

high-rise Park Regis hotel. Famed natural- Harvard Law School, has argued that de- men would dominate.

ist David Attenborough made an appear- liberating groups can be fertile ground for Such good outcomes aren’t guaranteed,

ance to greet the members and host a Q&A polarization, pointing to evidence from says Sander van der Linden, a Univer-

about his work. In the first sessions, U.K. experiments showing that groups such as sity of Cambridge social psychologist who

academics explained climate science basics: churchgoers or jury members can spiral studies decision-making. In some cases

the greenhouse effect, the impacts of rising into polarized conclusions. participants do become more polarized,

temperatures. Peachey’s understanding sky- But a long tradition of research sug- rather than less, in the face of disagree-

rocketed. “I just thought it was getting hot- gests the discussions are often construc- ment; that happened in group discussions

ter, but that’d be nice,” she says. “I bet you tive. In 1994, Stanford political scientist of gay rights in Poland—not one of Fishkin’s

there’s a lot of people out there who think James Fishkin polled 869 people—randomly experiments—that had recruited partici-

the same thing.” pants from pools with

Over three weekends— strong opinions. And in

and a fourth weekend Deliberative surge groups with a majority and
forced online and stretched minority opinion, “polar-
over three weekends be- The number of national and local minipublics—randomly selected assemblies that deliberate ization cascades” can over-
cause of the pandemic— over policy recommendations—has risen in the past decade. Many dealt with scientific questions. ride the minority, causing
the assembly listened not them to shift their opinion
Science policy** Other policy

only to scientists, but also 40 for reasons that have noth-

to representatives of inter- ing to do with evidence and

est groups such as Green- 30Number per year good arguments.

peace and industry body CREDITS: (GRAPHIC) C. O’GRADY AND N. DESAI/SCIENCE; (DATA) OECD DATABASE OF REPRESENTATIVE DELIBERATIVE PROCESSES AND INSTITUTIONS (2020)But with high-quality

Energy UK. The goal was 20 information, facilitators to
to provide both impartial keep discussions on track,

information and explicitly 10 and rules to enforce civility,
labeled opinions from advo- it is possible to steer people

cates, says Chris Stark, chief away from group biases, van

executive of the Commit- 0 der Linden says. In 2017,
tee on Climate Change, an 1995 2000 2005 2010 2015 2019* Kim Strandberg, a behav-

independent body advising *The Organisation for Economic Co-operation and Development tallied minipublics through November 2019; ioral scientist at Åbo Aka-
the government. Assembly Science assembled data for the rest of 2019. demi University in Finland,
member Ibrahim Wali, a **Dealt with questions on climate, environment, health, biotechnology, neuroscience, research priorities, or food technology. and his colleagues found

doctor from Epsom, says that although some selected from the U.K. electoral register— such measures prevented polarization in

members didn’t believe the scientists or on their attitudes toward rising levels of discussions about the status of the Swedish

think climate action was worthwhile, it was crime, asking questions such as whether language, spoken by a minority in Finland.

clear to everyone that they were not there “to more people should be sent to prison and “The people who are polarized and tribal are

argue about whether climate change is real.” whether sentences should be tougher. Next, actually a minority,” Dryzek says. A good as-

The assembly’s clear task—identifying poli- 301 of them agreed to meet for 2 days in sembly may include some members of this

cies to reach net zero by 2050—kept discus- Manchester, where they heard from politi- minority, he says. “But most of the people in

sions on track, he adds. cians, lawyers, and police. They asked ques- a minipublic have no history of activism or

Sessions shifted between speaker pre- tions and discussed policy proposals in small involvement with an issue, and so they’re in

sentations and small group discussions, groups before being polled again. The results a good position to reflect on what they hear.”

where members deliberated on policy showed participants had changed their opin- What makes deliberation so power-

recommendations, then voted on them by ions, in some cases dramatically: For each ful and positive seeming is still a bit of a

secret ballot. The ballot papers combined question in the poll, at least one-third of the black box, says André Bächtiger, a political

predetermined policy suggestions—like a deliberators had shifted their stance to some scientist at the University of Stuttgart. Re-

ban on the sale of petrol, diesel, and hybrid degree, and on some questions, as many as cent experiments like Strandberg’s seem to

cars by 2035—with ideas and amendments two-thirds had changed their minds. demonstrate the effects of deliberation and

suggested by members. Fishkin and his collaborators around the good design. But a deliberative experience

With facilitators making space for every- world went on to conduct more than 100 of is made up of countless moving parts of

one to chime in, Wali says no one domi- these experiments, which they call delib- human interaction, and “we just don’t have

nated in the small group discussions. A erative polls. They have explored opinions everything under control,” Bächtiger says.

poll of members found that 94% felt their on flood management in Uganda, constitu- “We’re still in the infancy of all of this.”

views were respected, even when others dis- tional reform in Mongolia, and educational And the growing popularity of mini-

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An Extinction Rebellion climate protest in London in September. Social scientists have found that politicians underestimate public support for climate action.

PHOTO: DAN KITWOOD/GETTY IMAGES publics carries another risk: Some will be less direct, Smith says. The parliamentary wider public. And being too enthralled by
constituted as cheap imitations, without committees that established it will use the the results of “lottocratic” minipublics runs
the crucial design elements. Fishkin trade- report to introduce debates, inform their the risk of encouraging a lazy shortcut to
marked the term “deliberative poll” partly own recommendations, and scrutinize good governance, she says: “Why not let the
to maintain quality control, and Chwalisz legislation coming from Johnson and his minipublics do the thinking and the decid-
and her colleagues have published guid- government, but “we’ve yet to see how the ing for us?”
ance on best practices. But citizens’ pan- government will respond,” Smith says.
els, juries, and conferences that rely on Dryzek agrees that democracies should
self-selected participants still spring up. Even if a minipublic’s recommendations not blindly defer to the decisions of mini-
“Lots of people are calling a lot of different are discussed by politicians, it’s difficult publics. But they still offer a critical piece
things citizens’ assemblies now, because to say how much they influence later poli- of information for policymakers that ex-
it’s kind of a trendy method,” says Graham cies, says Émilien Paulis, a political scientist perts can’t provide, he argues: a meaning-
Smith, a political scientist at the University at the French-speaking Free University of ful gauge of public values.
of Westminster. Brussels. But in an analysis of data on the
policy impact of 55 minipublics, Chwalisz For Peachey, the climate assembly made
THE U.K. CLIMATE ASSEMBLY’S final report, and her colleagues found that, 75% of the the right course clear. Her new awareness
published on 10 September, says climate ac- time, public authorities implemented more of climate change and its impacts has galva-
tion should be based on cross-party leader- than half the citizens’ suggestions. Only six nized her on behalf of her stepgrandchildren.
ship and principles of fairness to different minipublics in the sample saw none of their “We’re not going to benefit,” she says. “But fu-
groups of people. Its policy recommenda- recommendations implemented. ture generations will.” Since the U.K. assem-
tions, supported by a majority of assembly bly’s final meeting, Peachey has joined her
members, include restoring public owner- Some advocates have suggested imbuing local parish council and worked with fellow
ship for public transit—largely privatized minipublics with official legislative powers, councilors to declare a climate emergency—a
in the United Kingdom—introducing air but that would be antidemocratic because symbolic gesture that has led to local climate
travel taxes that increase as people fly they were never given consent to govern, minipublics elsewhere in the country. She
more often, and adding labeling to food says Cristina Lafont, a political philosopher daydreams about bringing a wind farm to an
that indicates its carbon footprint. at Northwestern University who describes old military airfield near Bath.
herself as a “frenemy” of the deliberative
Will those recommendations be adopted bodies. Keeping minipublics in an advisory Her own habits have changed, too. She
in the end? Whereas the French assembly role, rather than enabling them to produce now shops at her local farmer’s market
was set up by Macron himself, the U.K. as- binding recommendations, is more truly and plans to get solar panels for her home.
sembly was run at arm’s length from Prime democratic, she says. Although she wants Her new electric car is a great conversation
Minister Boris Johnson’s Conservative gov- the public to engage in thoughtful delib- starter, a chance for her to unpack what she
ernment, which means its impact will be eration, she worries that minipublic par- learned at the assembly, she says. “I’ve been
ticipants cannot be held to account by the given this information. It seems a shame
not to use it.” j

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INSIGHTS

PERSPECTIVES

EVOLUTIONARY GENETICS

Of dogs and men

Ancient genomes
reveal the common history
of human and dog

By Pavlos Pavlidis1 and Mehmet Somel2 tiple times, whether dog dispersals and (LGM). If so, the domestication of dogs pre- PHOTO: JOE & CLAIR CARNEGIE/LIBYAN SOUP/GETTY IMAGES
adaptations were coupled to those of hu- dated other Neolithic domestications—such
“B ut Argos passed into the darkness of mans, and how dogs interacted with their as sheep, pig, and cattle—and may have
death, now that he had fulfilled his wild sisters, the wolves. even facilitated them. Interestingly, many
destiny of faith and seen his master of these later domestications happened in-
once more after twenty years.” This Dogs likely evolved from a wolf population dependently in multiple local wild popula-
quote from The Odyssey vividly il- that self-domesticated, scavenging for left- tions. For example, there is evidence that
lustrates the bond between dog and overs from Paleolithic hunter-gatherers in pigs were domesticated in both Anatolia
human. These two species, separated by Eurasia (2, 3). However, the exact timing and and China (6). For dogs, however, the story
90 million years of evolutionary history, geographic location where the dog lineage is different. Dogs and modern-day Eurasian
have spent much of their recent past in started remain unknown, owing to the scar- gray wolves appear as monophyletic
each other’s service. This interaction has city of Paleolithic dogs in the archaeological groups; that is, any dog is genetically closer
remodeled both species’ environments and record. Analyses of genetic data suggest that to another dog than to a wolf, and vice versa
has modified the phenotypic and genetic dog-wolf divergence took place ~25,000 to (7). Monophyly supports a single origin of
composition of dog populations. On page 40,000 years ago (4, 5), providing an earliest dogs from a possibly extinct wolf lineage.
557 of this issue, Bergström et al. (1) use 27 possible date for dog domestication.
ancient dog genomes from across Eurasia, 1Foundation for Research and Technology Hellas, Institute
going back 11,000 years, to resolve whether Consistent with previous analyses (2–5), of Computer Science, 70013 Heraklion, Greece. 2Middle
dog domestication happened once or mul- Bergström and colleagues support a sce- East Technical University, 06800 Ankara, Turkey.
nario where dogs were domesticated 20,000 Email: [email protected]; [email protected]
years ago, around the Last Glacial Maximum

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A hunter and dog are depicted in rock art that dated study on Arctic sled dogs reported genetic NOISE POLLUTION
to between 5000 and 2000 BCE. It is located in Wadi signatures of adaptation in their fatty acid
Tashwinet, Tadrart Acacus, Libyan Sahara, Libya. metabolism genes (12), analogous to their The quiet
Inuit masters who carry adaptive changes spring of 2020
Although this remspeculative, Bergström in the same metabolic pathways—a likely
and colleagues show that by 11,000 years response to the high-fat Arctic diet (13). Anthropogenic noise
ago dog lineages had already diversified has no legacy
and spread worldwide. But how did they After their split, dogs and wolves have effects on bird song
spread? Even though human movement continued to occasionally interbreed. For
may have contributed to this expansion, instance, it was shown that a black coat By Wouter Halfwerk
LGM human migrations were probably not color allele passed from dogs to wolves in
extensive enough to explain these patterns. North America (14). Bergström et al. also S ounds of the past can be easily for-
Instead, dogs could have been exchanged confirm regional wolf-dog admixture. They gotten, especially when soundscapes
between forager groups, or may have spread show that Iberian wolves are genetically change gradually over long periods of
autonomously in a semi-feral state. closer to European dogs than to Asian time. This past spring, many people
dogs, whereas Mongolian wolves are closer got a chance to experience how the
Bergström et al. show that during the to Asian dogs. But did gene flow occur outside world sounded in the 1950s.
next 10,000 years, diversified dog lineages from wolf to dog, from dog to wolf, or both Global transport came to a halt as human
interbred frequently over wide geographi- ways? Bergström et al. reason that in the activities decreased abruptly (either volun-
cal areas. Further, they directly compare case of wolf-to-dog gene flow, all wolves tarily or under direct order for lockdown)
quantitative measures of population history should be more similar to those wolf-like to stem the spread of coronavirus disease
of humans and of dogs. They show that the dogs than to non-admixed dogs. However, 2019 (COVID-19). With fewer people driv-
genetic relations between human popula- they do not find such a pattern. Specifically, ing cars and hardly any airplanes travers-
tions largely match the genetic relations be- a wolf from Xinjiang, China, was identified ing the skies, the amount of background
tween proximal dog populations in Eurasia as equally distant from all dogs, past and noise across whole continents dropped
and the Americas, suggesting that move- present, suggesting mainly unidirectional substantially. On page 575 of this issue,
ment patterns are correlated between dog gene flow from dog to wolf. This intrigu- Derryberry et al. (1) report the impact of
and human. For instance, about half of the ing finding could be linked with wolf or the COVID-19 shutdown on animal behav-
ancestry of European dogs originates from dog behaviors (e.g., going feral) or asym- ior—namely, the songs of white-crowned
Paleolithic West Eurasia, and the other half metry in population sizes. There might sparrows. The findings suggest that miti-
from Southwest Asia; similarly, modern-day also be selection against such hybrids, gation measures against noise pollution
Europeans are a mixture between pre-Neo- perhaps as a result of their unbiddable or could yield immediate beneficial effects on
lithic hunter-gatherers and Neolithic farm- suboptimal behavior (12). Studying and urban wildlife.
ers from Anatolia. However, as shown by dating the distribution of introgression
Bergström and colleagues, dogs have not al- signatures across wolf genomes would be Derryberry et al. observed white-crowned
ways faithfully followed humans, resulting interesting. If population size asymmetry sparrows in the San Francisco Bay Area. The
in cases of decoupling between dog history is the reason, then we might expect admix- males of this species have a beautiful, crys-
and human history. For instance, compar- ture to intensify after agriculture began. tal-clear song, that starts with a long whis-
ing Neolithic and Chalcolithic Iran, they Studying signatures of sex bias in dog-to- tle, followed by a series of fast, down-swept
find that people have remained, but indige- wolf gene flow could also provide insight notes. Males use their song to keep territorial
nous dogs have been replaced by Levantine into the behavioral background of the pro- intruders at bay (2, 3). In urban areas, with
dogs. Conversely, in Neolithic Germany and cess. We further anticipate that successful high amounts of anthropogenic background
Ireland, incoming farmers of Anatolian de- genetic analyses of early dog-like fossils noise, males normally sing louder songs
scent appear to have adopted dogs from lo- from Eurasia may help to resolve the long- compared to their rural counterparts (4).
cal foragers. standing debate surrounding the origins of Although increasing song amplitude (mak-
dog domestication. j ing songs louder) is an effective communi-
In addition to sharing dispersal paths, cation strategy to overcome the masking
dogs and humans have traced parallel paths REFERENCES AND NOTES impact of urban noise (5), it is often traded
of evolutionary adaptation. Variation in the against other song components such as re-
copy number of genes encoding amylase, the 1. A. Bergström et al., Science 370, 557 (2020). duced song complexity. In the case of Bay
enzyme required for breaking down starch, 2. G. D.Wang et al., Nat. Commun. 4, 1860 (2013). Area white-crowned sparrows, increasing
is such an example of convergent evolution. 3. L. M. Shannon et al., Proc. Natl.Acad. Sci. U.S.A. 112, song amplitude comes at the cost of reduced
Humans carry extra salivary amylase cop- trill performance ( 4).
ies compared to chimpanzees (8, 9), owing 13639 (2015).
to high starch consumption that perhaps 4. P. Skoglund, E. Ersmark, E. Palkopoulou, L. Dalén, Curr. Derryberry et al. recorded white-crowned
began before farming (10). Likewise, most sparrow males during the shutdown in March
dogs, compared to wolves, carry extra pan- Biol. 25, 1515 (2015). and April of 2020 in San Francisco as well as
creatic amylase (AMYB2) copies, possibly 5. L. R. Botigué et al., Nat. Commun. 8, 16082 (2017). in nearby rural areas. The authors measured
facilitating starch digestion in their new 6. M. Price, H. Hongo, J.Archaeol. Res. 28, 557 (2020). background noise data from their recordings
environment (11). Bergström and colleagues 7. A. H. Freedman et al., PLOS Genet. 10, e1004016 (2014). and used toll data since the opening of the
show that early dogs already carried extra 8. G. H. Perry et al., Nat. Genet. 39, 1256 (2007). Golden Gate Bridge in 1937 to extrapolate
amylase copies compared to wolves, but 9. P. Pajic et al., eLife 8, e44628 (2019). traffic data. During the lockdown period,
amylase copy numbers further expanded 10. S. Mathieson, I. Mathieson, Mol. Biol. Evol. 35, 2957
following the increasing reliance on starch-
rich agricultural diets in prehistoric Eurasia (2018).
over the past 7000 years. Similarly, a recent 11. E.Axelsson et al., Nature 495, 360 (2013).
12. M. S. Sinding et al., Science 368, 1495 (2020).
13. M. Fumagalli et al., Science 349, 1343 (2015).
14. T. M.Anderson et al., Science 323, 1339 (2009).

ACKNOWLEDGMENTS

We thank E.Tsaglioti and the METU CompEvo group for help-
ful suggestions.

10.1126/science.abe7823

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traffic was reduced to amounts resembling Urban white-crowned sparrows absence of seed predators and seed dispers- PHOTO: JN PHILLIPS
those of the 1950s, which was accompanied improved song performance ers near noisy gas-compressor stations (12).
by a large reduction in noise amounts in the It would therefore be very interesting to track
urban areas (on average 7 dB), but not rural during the coronavirus disease the fates of urban animals that were born
areas. Comparing songs from the 2016 breed- 2019 (COVID-19) shutdown. during the quiet spring of 2020 and assess
ing season with songs recorded in 2020, the whether they develop and behave similarly to
authors found that urban males sang with Such a fast return to preexposure condi- their rural counterparts (but different from
higher trill performance (rapid and complex tions suggests that anthropogenic noise may their urban predecessors).
motor control) during the pandemic shut- not suffer from the same legacy effects as
down. By modeling detection distances, the other environmental pollutants, particularly The findings of Derryberry et al. suggest
authors further showed that urban birds chemical compounds. Sensory pollution in- that temporary noise reduction immedi-
communicated over twice the distance dur- cludes anthropogenic stimuli, such as vibra- ately influences animal behavior, providing
ing lockdown when compared to preshut- tional or airborne noise caused by traffic and policy-makers with a possible solution to the
down periods, despite a notable reduction of industry, or artificial light at night, which harmful effects of this sensory pollution on
4 dB in song amplitude. Rural birds did not hampers animals in acquiring environmental animal populations, namely reducing expo-
experience changes in background noise and information (9, 10). These stimuli generally sure to pollutants during critical stages of
consequently did not alter their songs. The leave no traces when the source of pollution an animal’s life cycle (e.g., during migration
magnitude of change in effective communi- is taken away, and we would therefore expect or dispersal). Mitigation measures to reduce
cation was beyond expectation, suggesting their disruptive impact to stop immediately, the impact of artificial light at night or an-
that noise pollution is even more detrimental without legacy effects on animal behavior. thropogenic noise should therefore be tai-
than has been so far assumed. lored to taxon-specific needs. Shutting down
Sensory pollutants may, however, have the 9/11 memorial lights in New York City for
Previous work has shown that many song- other longer-lasting impacts through direct a few minutes during peak periods, for ex-
birds immediately change their songs when effects on the animal’s development (11), ample, may greatly reduce fatalities among
they are experimentally exposed to short through behaviors involved in important nocturnal migrating birds (9). Likewise, brief
periods of traffic noise by either increasing life-history decisions (9), or through changes road closures during specific times of day or
their amplitude or pitch (6, 7) or changing in community composition (12). Animals ex- breeding season may prevent the develop-
the length and shape of individual song ele- posed to high amounts of sensory pollutants ment of chronic stress in endangered spe-
ments (8). Derryberry et al. reveal that the during critical stages in their lives may de- cies, with long-lasting impacts.
opposite is also true: When noise pollution velop specific morphological, physiological,
is removed, birds sing immediately as if they or cognitive traits that remain fixed long af- Spring 2020 not only reminded us how
have never been exposed to any traffic noise. ter these pollutants have been reduced. Noise the natural world of 1950s felt (14), smelt
exposure over multiple days, for example, can (15), and sounded like, but it also highlighted
Department of Ecological Sciences, Vrije Universiteit influence learning and cognition in birds (13). the impact of anthropogenic activities on our
Amsterdam, Amsterdam, Netherlands. Likewise, animals that made a poor decision daily lives and the lives of organisms with
Email: [email protected] by breeding in a place considered suboptimal whom we share this planet. It taught us that
because of sensory pollution may remain we can change the way we live in a rapid and
there for the rest of their lives, irrespective drastic manner and that it is not too late to
of changes in exposure amounts (9). Sensory do so because species may still recover from
pollution also may lead to long-lasting com- anthropogenic stresses. It is an important
munity-level changes, such as changes in lesson that we may need to remember again
vegetation as the result of the presence or soon to cope with serious pressing chal-
lenges of the 21st century—namely mass
extinction and climate change. j

REFERENCES AND NOTES

1. E. P. Derryberry et al., Science 370, 575 (2020).
2. D.A. Luther,J. Phillips, E. P. Derryberry, Behav. Ecol. 27,

332 (2016).
3. J. Podos, Evolution 51, 537 (1997).
4. D.A. Luther, E. P. Derryberry, Anim. Behav. 83, 1059

(2012).
5. H. Brumm, H. Slabbekoorn, in vol. 35 of Advances in the

Study of Behavior, P.J. B. Slater et al., Eds. (Academic
Press, 2005), pp. 151–209.
6. W. Halfwerk, H. Slabbekoorn, Anim. Behav. 78, 1301
(2009).
7. H. Brumm, D.Todt, Anim. Behav. 63, 891 (2002).
8. M.J. Montague, M. Danek-Gontard, H. P. Kunc, Behav.
Ecol. 24, 343 (2013).
9. D. M. Dominoni et al., Nat. Ecol. Evol. 4, 502 (2020).
10. W. Halfwerk, H. Slabbekoorn, Biol. Lett. 11, e20141051
(2015).
11. S. L. Nedelec et al., Sci. Rep. 4, 5891 (2014).
12. C. D. Francis, N.J. Kleist, C. P. Ortega,A. Cruz, Proc. R.
Soc. London Ser. B 279, 2727 (2012).
13. W. Halfwerk, K. van Oers, Proc. R. Soc. London Ser. B 287,
20192951 (2020).
14. T. Lecocq et al., Science 369, 1338 (2020).
15. M. B. Karuppasamy et al., Air Qual.Atoms. Health
10.1007/s11869-020-00892-w (2020).

10.1126/science.abe8026

524 30 OCTOBER 2020 • VOL 370 ISSUE 6516 sciencemag.org SCIENCE

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INSIGHTS | PERSPECTIVES

PROTON MEMBRANES

Speeding protons with metal vacancies

Membranes made from nanosheets derived from CdPS3 have high proton conductivity

By Fengmei Wang1 and Jun He1,2 port, with high selectivity. Delicate pores contain various metals M (Cd, Mn, Fe, Co,

must be created that can be hydrated (3), Ni, or Zn) and chalcogenides X (S or Se).

P roton exchange membranes (PEMs) and hydrophilic groups (6) are purposely For example, each layer of MPS3 consists of
find applications not only in fuel cells introduced to attain improved functional- infinite arrays of P2S64– units coordinated
and sensors but as chemical filters ity. For organic polymers, –SO3H groups in to M2+ cations by S atoms (8). The fairly
and in biological systems. In particu- Nafion are much more hydrophilic than
lar, the Nafion (Chemours Company) the fluorocarbon-based backbone, and ionic M–S bonds, especially in MnPS and
PEM, which consists of sulfonated these groups line the inner walls of nano- 3

CdPS , enable an intercalation process
3

that removes M2+ cations to create vacan-

tetrafluoroethylene–based fluoropolymer- channels for proton conduction (1). The cies under mild aqueous conditions (9).

copolymer, is widely used in practical elec- oxygenated functional groups (hydroxyl, A heterogeneous equilibrium that occurs

trochemical processes. It has a high proton carboxyl, and epoxide) of graphene oxide between M2+ ions and solvated P2S64–, in
conductivity up to 0.2 S/cm below 80°C and (GO) also play the same role to establish which M2+ ions are then easily displaced by

high relative humidity (RH) (>93%) (1), but hydrogen-bonded channels in water-mole- other alkali ions (Li+, Na+, and K+) or pro-

its conductivity drops severely at higher cule networks for proton transport (6). tons (H+) present in the aqueous solution,

temperatures or at low RH (below 50%). On The TMPTCs explored by Qian et al. maintains charge balance (see the figure,

page 596 of this issue, Qian et al. (2) report are layered van der Waals materials that top). After this intercalation and exchange

a new class of proton membranes process, a complete chemical trans-

assembled from two-dimensional formation of the entire structure is

(2D) layered transition-metal phos- Ionic defects and water networks ensured and not limited by ion dif-
phorus trichalcogenide (TMPTC) fusion within the host lattice. Both
nanosheets in which metal vacan- The high proton conductivity of the Cd1–xPS3LixHx membranes Cd0.85PS3Li0.3 and Cd0.85PS3Li0.15H0.15
cies boost ion conductivity. These fabricated by Qian et al. results from sites created by cadmium have different structural features,

vacancies and the formation of water networks.

membranes exhibit a proton con- except for the valence state of each

ductivity of ~0.95 S/cm at 90°C and H+ Li+ H+ element, compared with the pris-
98% RH but still have a conductivity tine CdPS . Either Cd vacancies (or
of 0.26 S/cm even at 60% RH.
3

Mn vacancies in Mn analogs) in the

Various materials under differ- matrix serve as a donor center for

ent conditions have been explored P mobile H+ or of lithium ions to boost
as PEMs, including organic poly- S ion conductivity.
mers other than Nafion, inorganic-
In PEMs, two mechanisms for

organic nanohybrids (3), metal Formation of a Cd2+ Protons enter Li+ proton transport (10), the vehicle
organic frameworks (MOFs)(4), Cd vacancy allows the lattice through ion mechanism and Grotthuss mecha-
bioderived materials (5), and 2D lay- adsorption of Li+. exchange with Li+. nism, can operate. In the former,
ered materials such as graphene (6) which operates in Nafion films,

and graphdiyne (7). However, these Ion exchange in layered materials water molecules come together to
alternatives to Nafion have much form a cluster (or nanochannel)
lower proton conductivity (10–5 to A heterogeneous equilibrium can occur between the solid CdPS3 structure that act as a vehicle for transport-
10–2 S/cm). To understand why the and Li+ ions and protons (H+) in aqueous solution to form Cd1–xPS3LixHx. ing protons. Thus, ion conductivity

TMPTC-based assembled PEM fab- starts to dramatically decrease in

ricated by Qian et al. has much Nafion PEMs at high temperatures

higher performance, it is necessary H+ or at low RH as the water clusters
to look in general at the structures Li+ become disconnected.

and mechanisms underlying proton Hydrogen However, conditions of low RH
and elevated temperatures have
conductivity in PEMs. bonding

A high-performing PEM usually H2O no obvious effect on the Grotthuss

has a large density of optimally mechanism, in which the protons

sized channels for proton trans- hop along the hydrogen-bonded

water-molecular network, such as

GRAPHIC: A. KITTERMAN/SCIENCE 1Chinese Academy of Sciences (CAS) Center H+ those in GO membranes and the
for Excellence in Nanoscience, CAS Key Li+ 2D layered Cd0.85PS3Li0.15H0.15 stacked
Laboratory of Nanosystem and Hierarchical nanosheets Qian et al. assembled
Fabrication, National Center for Nanoscience Proton transport in the layered membrane into membranes through vacuum
and Technology, Beijing 100190, P. R. China. filtration. In their system, the uni-
2Key Laboratory of Artificial Micro- and Ordered water networks between the monolayers, created through form Cd2+ vacancies negatively
Nano-structures of Ministry of Education, hydrogen bonding, along with protons in the Cd vacancies create proton charge the surfaces of each layer
School of Physics and Technology, Wuhan transport channels. to provide uniform donor centers
University, Wuhan 430072, P. R. China.
E-mail: [email protected]; [email protected]

SCIENCE sciencemag.org 30 OCTOBER 2020 • VOL 370 ISSUE 6516 525

Published by AAAS

INSIGHTS | PERSPECTIVES

to adsorb H+ and form monolayers that are ECOLOGY
highly hydrophilic on both sides (see the
figure, bottom). The ordered water molecu- Should I stay or should I go?
lar network between the monolayers pro-
vides a proton transport channel. The ad- Pinpointing genetic alleles that influence the timing
sorbed H+ in Cd vacancies join this network of salmon migration might aid restoration efforts
and accelerate proton conduction through
the Grotthuss mechanism under humidified By Garrett McKinney are threatened or even extirpated in many
conditions to form a one-dimensional (1D regions. An understanding of the genetic ba-
hydrogen-bonded chain (see the figure, bot- A common assumption in genetics is sis of migration timing can illuminate con-
tom). A large capillary-like force develops that complex traits are influenced servation actions that are most appropriate
in the 2D layered material assembled mem- by many genes, each with small ef- for protecting and restoring threatened pop-
brane that can also guide and accelerate ion fect. However, a growing number of ulations. Previous research identified a small
transport (6, 11). Even at low RH (53%), the examples reveal that single genes or genomic region associated with migration
water clusters can expand and join each gene regions can have a strong influ- timing; however, these studies examined
other to form a monolayer water network ence on phenotypic traits (1–3). The genetic subsets of the genome (6, 7), excluded indi-
within the Cd0.85PS3Li0.15H0.15 framework. architecture of a trait has implications for viduals with intermediate run timing (8), or
how traits are inherited and how trait varia- used pooled-genome resequencing, which
As an emerging family of 2D layered ma- tion is viewed in the context of conservation cannot reconstruct individual haplotypes
terials, the MPX series has promising fea- (maintenance and recovery). On page 609 of (9). The new study answers multiple linger-
this issue, Thompson et al. (4) examine the ing questions, including the genetic variants
3 genetic basis of migration timing in Chinook associated with differences in run timing
salmon and find that timing is controlled and the degree to which there is gene flow
tures in coordination chemistry and solid- by a single genomic region containing two (mating) among different run types.
genes, GREB1L (GREB1-like retinoic acid
“The ordered water molecular receptor coactivator) and ROCK1 (Rho- Although declining populations have
network between the associated coiled-coil containing protein been observed for both spring- and fall-run
monolayers provides a proton kinase 1). Genetic variants in this region Chinook, spring-run Chinook have exhib-
transport channel.” include single-nucleotide polymorphisms ited particularly steep declines, resulting
(SNPs) and short duplications that together at least in part from habitat degradation.
state chemistry. Besides the univalent ion form distinct haplogroups with linked alleles Spring-run salmon return to freshwater
conductivity in an aqueous system induced (inherited together from one parent) that ef- months before spawning and rely on cold-
by tailoring chemical coordination envi- fectively function as small supergenes. water pools for survival during the summer.
ronment, the divalent ionic (Zn2+) conduc- This makes them particularly vulnerable to
tivity in the solid-state MPX3 (like ZnPS3) is Chinook salmon complete their ocean mi- anthropogenic changes that alter summer
also worth studying (12). The polarizable gration and return to streams to spawn as water flows or increase water temperature,
lattice provided by the sulfide anions and either early migrants (usually called spring- such as logging, mining, water diversion,
the layered structure offers pathways for or summer-run Chinook) or late migrants and dam building (6). Before the discovery
ion conduction in the solid-state structure. (usually called fall- or late fall–run Chinook). that the GREB1L-ROCK1 genomic region
This discovery of extremely high proton Despite this difference in return timing, in- influences run timing, researchers noted
conductivity in a membrane based on 2D dividuals of each type spawn at relatively that spring- and fall-run populations within
MPX3 represents a step toward practical similar times, with spring-migrating salmon coastal drainages were often closely related
PEM in energy conversion and storage. j remaining in streams for several months genetically. This led to the conclusion that
before spawning and fall-migrating salmon run timing had evolved independently
REFERENCES AND NOTES spawning soon after returning to streams. many times and the corollary that a specific
The difference in migration timing can be run-time trait that is lost could reevolve
1. S. Bose et al., Prog. Polym. Sci. 36, 813 (2011). associated with a number of traits, including (10). However, the results of Thompson et
2. X. Qian et al., Science 370, 596 (2020). body size, fat content, difference in spawn al. and other recent studies on the GREB1L-
3. S. Moghaddam et al., Nat. Nanotechnol. 5, 230 (2010). timing, and, in many cases, use of a different ROCK1 region (4, 6, 8) suggest that loss of
4. M. Liu et al., Nat. Commun. 7, 12750 (2016). habitat. Spring-migrating salmon are highly spring-run alleles in a population equates to
5. C. Ma et al., Sci.Adv. 6, eabc0810 (2020). prized by anglers because of their high fat loss of the spring-run trait and that reevolu-
6. M. R. Karim et al., J.Am. Chem. Soc. 135, 8097 (2013). content. These fish also fill a vital ecological tion of the trait through mutation is exceed-
7. J.Xu et al., Nat. Commun. 10, 3971 (2019). function by serving as a food source for pred- ingly unlikely (11).
8. F.Wang et al., Adv. Funct. Mater. 28, 1802151 (2018). ators when other salmon species are not in
9. R. Clement, O. Garnier,J.Jegoudez, Inorg. Chem. 25, streams and by transporting marine-derived This conclusion raises an obvious ques-
nutrients into an up-river habitat that is in- tion: Can fall-run Chinook act as a reservoir
1404 (1986). accessible to fall-migrating salmon (5). for spring-run alleles (4, 6), thereby allow-
10. J.Wei, in Polymer-Based Multifunctional ing individuals with the spring-run pheno-
Unfortunately, spring-migrating Chinook type to reemerge from fall-run populations?
Nanocomposites and Their Applications, K. Song, C. Liu, Thus far, two studies have examined this
J. Guo, Eds. (Elsevier, 2019). pp. 245–260. National Research Council Research Associateship question; both found that spring-run al-
11. R. R. Nair, H.A.Wu, P. N.Jayaram, I.V. Grigorieva,A. K. Program, Northwest Fisheries Science Center, National leles are either very rare or absent in fall-
Geim, Science 335, 442 (2012). Marine Fisheries Service, National Oceanic and run populations where the spring-run has
12. A.J. Martinolich et al., Chem. Mater. 31, 3652 (2019). Atmospheric Administration, Seattle, WA 98112, USA. been extirpated. This suggests that recovery
Email: [email protected]
ACKNOWLEDGMENTS
F.W. and J. H. thank the National Natural Science Foundation
of China (nos. 21805057 and 61625401) and the National
Key R&D Program of China (nos. 2018YFA0703700 and
2016YFA0200700).

10.1126/science.abe6166

526 30 OCTOBER 2020 • VOL 370 ISSUE 6516 sciencemag.org SCIENCE

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VIEWPOINT: COVID-19

Will SARS-
CoV-2 become
endemic?

Reinfection, seasonality,
and viral competition
will shape endemic
transmission patterns

By Jeffrey Shaman and Marta Galanti

Chinook salmon return to spawn as early migrants in spring or late migrants in fall. This important life-history R einfection, in which an individual is
variation is under the control of a single genetic region. subject to multiple, distinct infec-
tions from the same virus species
PHOTO: CRISTINA MITTERMEIER/NATGEOIMAGECOLLECTION of extirpated spring-run populations will re- netic variants or distinct haplotypes related throughout their lifetime, is a salient
quire either natural immigration of spring- to migration. feature of many respiratory viruses.
run individuals or human intervention to Indeed, the persistence and ubiquity
reintroduce fish with the spring-run alleles, Differential migration timing has also in human society of common respiratory
likely through translocation of individuals. been documented in other salmon species, viruses—including influenza viruses, re-
A frequent concern with salmon restora- and the GREB1L-ROCK1 genomic region has spiratory syncytial virus (RSV), rhinovi-
tion efforts is that translocated individuals been found to influence migration timing in rus, and the endemic coronaviruses—are
might not have the appropriate adaptations steelhead trout (8, 12). Although Micheletti et largely due to their ability to produce re-
to thrive under local conditions. Thompson al. (12) used whole-genome sequencing, these peat infection. Since the emergence of se-
et al. showed evidence of natural historic results have not been directly compared with vere acute respiratory syndrome coronavi-
interbreeding between run types in the studies of Chinook salmon. Thus, it is not yet rus 2 (SARS-CoV-2), the virus responsible
Klamath River that is sufficient to homog- known if the same genetic variants within for the ongoing coronavirus disease 2019
enize the genome outside of the region asso- this region influence run timing in both spe- (COVID-19) pandemic, a critical concern
ciated with run-timing differentiation. This cies or if run timing in each species is the has been whether humans will experience
finding suggests that in these populations, result of parallel evolution using the same reinfections with this pathogen, which
locally adapted alleles for other traits still molecular pathway. Comparative analyses of might enable it to become endemic.
exist in the fall-run population. Rebuilding these two species as well as other salmon that
of spring-run Chinook populations will exhibit run-timing variation offer appealing Typically, following an initial infection,
most likely be achieved through restoration opportunities to study how similar traits can the human adaptive immune system devel-
or improvement of upriver habitats tradi- evolve across populations and species. j ops a suite of defenses, including memory
tionally used by these salmon. B lymphocytes capable of producing neu-
REFERENCES AND NOTES tralizing antibodies targeted to bind to
The study by Thompson et al. provides that particular pathogen, and memory T
a deeper view into the genetic basis of 1. N.J. Barson et al., Nature 528, 405 (2015). lymphocytes that help regulate immune
migration in Chinook salmon. However, 2. M. R.Jones et al., Science 360, 1355 (2018). responses and induce death of infected
additional avenues must be explored to 3. S. E.Johnston et al., Mol. Ecol. 20, 2555 (2011). cells. These adaptive immune components,
fully decipher the mechanisms underlying 4. N. F.Thompson et al., Science 370,XXX (2020). particularly B cells, can produce steril-
migration timing. The new study focused 5. T. P. Quinn, P. McGinnity,T. E. Reed, Can.J. Fish.Aquat. izing immunity in which the pathogen, if
only on Chinook salmon from California reintroduced to the host, is prevented from
and Oregon. Also, although previous stud- Sci. 73, 1015 (2015). replicating within the body.
ies found SNPs or haplotype blocks within 6. T. Q.Thompson et al., Proc. Natl.Acad. Sci. U.S.A. 116, 177
the GREB1L-ROCK1 region that are associ- However, for many viruses, a number of
ated with migration throughout the spe- (2019). processes, particularly insufficient adap-
cies range, these studies either examined 7. I.J. Koch, S. R. Narum, Evol.Appl. 13, 2316 (2020). tive immune response, waning immunity,
individual SNPs or used pooled rather than 8. D.J. Prince et al., Sci.Adv. 3, e1603198 (2017). and immune escape, can undermine or
individual-level whole-genome sequences. 9. S. R. Narum,A. Di Genova, S.J. Micheletti,A. Maass, Proc. circumvent the sterilizing character of im-
Thus, it is unclear if the specific haplotypes munity and allow subsequent reinfection.
identified in the new study exist through- Biol. Sci. 285, 20180935 (2018). In the first instance, an initial infection
out the species range or if populations from 10. R. S.Waples, D.J.Teel,J. M. Myers,A. R. Marshall, with a particular agent may not engender
Washington to Alaska harbor additional ge- an adaptive immune response sufficient
Evolution 58, 386 (2004). to confer sterilizing immunity. Serological
11. M. Ford et al.,“Reviewing and synthesizing the state studies indicate that most SARS-CoV-2 in-
fections, regardless of severity, induce de-
of the science regarding associations between adult
run timing and specific genotypes in Chinook salmon
and steelhead”(NOAA Processed Report NMFS-
NWFSC-PR-2020-06, U.S. Department of Commerce,
2020).
12. S.J. Micheletti,J. E. Hess,J. S.Zendt, S. R. Narum, BMC
Evol. Biol. 18, 140 (2018).

10.1126/science.abe9169

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INSIGHTS | PERSPECTIVES

Factors influencing postpandemic transmission of SARS-CoV-2 in genes encoding surface pro-

Rates of repeat infection, factors modulating seasonality, competition with other circulating respiratory viruses, and control teins such as the spike protein,

measures will influence the endemic pattern of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) transmission. indicating that considerable di-

versification can occur. To date,

Immunity Incidence Short-lived immunity Interventions Incidence No intervention some evidence of SARS-CoV-2-
specific antibody waning has
Adaptive immune Time Vaccination (timing Time been captured in a longitudinal
response following Longer immunity eCciency, coverage) Interventions study (2), and a few verified re-
infection peat SARS-CoV-2 infections have
Drug treatments been documented (3). Although
Severity of infection reinfections can occur, the num-
Nonpharmaceutical ber of reinfection cases is not
Waning of immunity interventions currently sufficient to general-
(personal protective ize the duration of immunity at
Immune escape equipment, social
distancing, travel
Incidence restrictions, hygiene Incidence

measures) population scales or the severity

of repeat infection. Whether re-
Time Time infections will be commonplace,

Endemic pattern how often they will occur, how
contagious reinfected individu-

als will be, and whether the

risk of severe clinical outcomes

changes with subsequent infec-

tion remain to be understood.

Insight from other respi-

Seasonality Incidence No seasonality Virus interactions Incidence No interference ratory viruses points to the
possibility of reinfection with
Impact of WSWS Transmissibility of Virus 1 SARS-CoV-2. Naturally ac-
environmental Time each virus Virus 2 quired infections with the four
conditions on endemic HCoVs (OC43, HKU1,
transmissibility Winter transmission Order of exposure Time 229E, and NL63) indicate that
reinfections with the same
Seasonal changes WSWS Degree of cross Interference of HCoV type are common within
in host behavior, Time protection co-circulating 1 year (4); sequential infections
school calendar, with the same influenza virus
and indoor/outdoor Incidence Incidence virus strain can occur in less than 2
gatherings years (5); and reinfections of
Time adults with RSV within 1 year
Seasonal changes have also been documented (6).
in immune function

By contrast, more pathogenic

velopment of some specific antibodies (1); ing the host vulnerable to reinfection, viruses that induce systemic effects on the

however, despite encouraging results from may also undermine sterilizing immunity. host may elicit a longer-lasting adaptive

the experimental vaccination of primates, Immune escape is a third process that can immune response. For example, longitudi-

it remains unclear whether those anti- facilitate reinfection, in particular by vi- nal immune profiles from SARS survivors

bodies are sufficient to provide long-term ruses. Here, a virus, during its continued showed a stronger immune response with

effective protection or if other adaptive serial passage through a host population, neutralizing antibodies persisting for 2 to

immune components are present and func- accumulates point mutations. This accu- 5 years (7). However, it could not be con-

tional. Furthermore, immune response to mulation, termed antigenic drift, may lead firmed if and for how long this response

SARS-CoV-2 infection is heterogeneous, to conformational changes of viral surface conferred immunity because the SARS out-

with individuals who experience asymp- proteins that disrupt the binding of anti- break lasted less than 1 year.

tomatic infections manifesting a weaker bodies previously generated against an In addition to duration of protective

immune response than those experiencing earlier variant. Immune escape is a conse- immunity, the long-term effects of SARS-

more severe disease (1). It is possible that quence of this antigenic drift that enables CoV-2 on humans will depend on the se-

some individuals never develop sterilizing reinfection through the evasion of adap- verity of reinfection. Sequential infections

immunity following infection with SARS- tive protection. with influenza virus have been associated

CoV-2, or that multiple exposures will be The time scales of waning immunity and with less severe symptoms (8), whereas

needed for affinity maturation and devel- immune escape differ by pathogen and have no association between reinfection and

opment of long-lasting protection. yet to be defined for SARS-CoV-2. Thus far, symptom severity was found in recurring

Waning immunity, in which the initial the mutation rate of the SARS-CoV-2 genome endemic HCoV infections (4). In addition, GRAPHIC: C. BICKEL/SCIENCE

adaptive immune response is robust and appears to be slower than that of influenza for other viruses (e.g., RSV and dengue),

protective but dissipates over time, leav- viruses. This lower rate may be a conse- suboptimal binding of naturally induced

quence of proof-reading during replication, or vaccine-induced antibodies can enhance

Department of Environmental Health Sciences, Mailman which is exclusive to coronaviruses among infection severity upon subsequent expo-
School of Public Health, Columbia University, New York, NY RNA viruses. Conversely, human coronavirus sure, a phenomenon called antibody-de-
10032, USA. Email: [email protected] (HCoV) OC43 is highly variable, particularly pendent enhancement (ADE) (9). To date,

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responses among the few patients with manifest as a function of reinfection rates, sion (personal protective equipment, so-
verified SARS-CoV-2 reinfection have been vaccine availability and efficacy, and social, cial distancing, increased hygiene, limited
heterogeneous with one apparent repeat immune, and innate factors that modulate indoor gatherings) may reduce the magni-
infection requiring hospitalization. Thus, virus transmissibility (see the figure). In tude of seasonal influenza outbreaks. Such
thorough serological and prospective stud- addition, the cyclic persistence of SARS- increased use of nonpharmaceutical mea-
ies are needed to determine whether ADE CoV-2 in human populations may be af- sures, and possible virus interference, could
manifests among SARS-CoV-2 infections, fected by ongoing opportunities for inter- be responsible for the reduced incidence of
either because of prior homologous in- action with other respiratory pathogens. influenza during the recent winter of the
fection or cross-reactive antibodies from Southern Hemisphere (15).
other HCoVs. This will have particular Co-circulating respiratory viruses may in-
relevance for vaccines and convalescent terfere with one another while competing The phases and magnitudes of differ-
plasma therapy. for the same resources, and their interac- ent outbreaks in a multipathogen system
tions have been studied at population and are dictated by the interaction dynamics
Should reinfection prove commonplace, individual levels, in reconstructed human between those pathogens: from large over-
and barring a highly effective vaccine de- tissues and in animal models. The outcomes lapping phases when pathogens enhance
livered to most of the world’s population, in individuals experiencing serial exposure one another’s transmission, to complete
SARS-CoV-2 will likely become endemic to different viruses vary and in general ap- inhibition of a strain by the neutralizing
(10). The typical time scale at which in- pear to depend on the order and timing of cross-reactivity of a more transmissible
dividuals experience reinfection and exposures. Many studies have documented one (9). Several postpandemic scenarios
seasonal differences in transmissibility evidence of negative interference between for SARS-CoV-2 have been modeled (10),
will determine the pattern of endemic- viruses caused by short-lived (days) protec- postulated on duration of immunity and
ity. Outside the tropics, the incidence of tion elicited from the first infection. Host cross-immunity between SARS-CoV-2 and
many common respiratory virus infections antiviral interferon responses are often re- the other betacoronaviruses (OC43 and
increases during particular times of the garded as the main mechanism by which HKU1). A duration of immunity similar to
year. This phase-locked behavior is due to interference manifests; that is, as a result of that of the other betacoronaviruses (~40
accumulated susceptibility to reinfection, a recent infection, the host cells up-regulate weeks) could lead to yearly outbreaks of
which increases over time because of im- the synthesis of interferons, potentially in- SARS-CoV-2, whereas a longer immunity
mune escape and waning immunity, and hibiting a secondary infection. Even though profile, coupled with a small degree of
seasonal modulation of virus transmissi- it is short-lived, this effect can be strong at protective cross-immunity from other be-
bility derived from environmental condi- population scales and temporarily reduce tacoronaviruses, could lead to the appar-
tions, changing behavior (e.g., mixing in- the prevalence of a virus or shift the timing ent elimination of the virus followed by re-
doors in cold weather), or altered immune of its circulation. For example, it is hypoth- surgence after a few years. Other scenarios
function. For example, influenza incidence esized that a large summer 2009 rhinovirus are, of course, possible, because there are
is greatest during winter in temperate re- outbreak delayed pandemic influenza virus many processes at play and much that re-
gions. Once expelled from an infectious emergence in Europe (13). mains unresolved. j
host, the influenza virus appears to be
more stable in low-humidity conditions The clinical and population-scale inter- REFERENCES AND NOTES
(11), which are prevalent both indoors and actions of SARS-CoV-2 with other respira-
outdoors during winter. Further, during tory viruses, particularly influenza viruses 1. Q.-X. Long et al., Nat. Med. 26, 1200 (2020).
colder months, people spend more time in- and other HCoVs, need to be monitored 2. J. Seow et al., medRxiv 10.1101/2020.07.09.20148429
doors and school is in session, which may in the coming years. To date, some SARS-
facilitate transmission, and shorter days CoV-2 coinfections have been documented (2020).
and less sunlight exposure may suppress (14), including coinfections with influenza 3. K. K.-W.To et al., Clin. Infect. Dis. 10.1093/cid/ciaa1275
immune function. and RSV; however, testing for multiple
pathogens has not been routinely carried (2020).
The endemic HCoVs (OC43, HKU1, NL63, out, and the scarce data that do exist, 4. M. Galanti,J. Shaman, J. Infect. Dis. 10.1093/infdis/
and 229E) all exhibit a seasonality in tem- mostly for older adults with high rates of
perate regions, similar to influenza viruses preexisting medical conditions, do not sup- jiaa392 (2020).
(12). Consequently, numerous studies have port a definitive evaluation of coinfection 5. M.J. Memoli et al., Clin. Infect. Dis. 70, 748 (2020).
sought to determine whether conditions likelihood or severity. Studies prior to the 6. C. B. Hall, E. E.Walsh, C. E. Long, K. C. Schnabel, J. Infect.
such as temperature, sunlight, humidity, pandemic indicate that simultaneous in-
ozone, and pollution affect SARS-CoV-2 vi- fections with multiple respiratory viruses Dis. 163, 693 (1991).
ability and transmissibility. The results are are not uncommon but are not associated 7. H. Mo et al., Respirology 11, 49 (2006).
not currently conclusive, although it ap- with increased disease severity. 8. J. R. Davies, E.A. Grilli,A.J. Smith, J. Hyg. (Lond.) 92, 125
pears that environmental conditions, such
as sunlight and humidity, may modulate At the population scale, a possible over- (1984).
SARS-CoV-2 transmissibility—not enough lap between influenza and SARS-CoV-2 9. N. Ferguson, R.Anderson, S. Gupta, Proc. Natl.Acad. Sci.
to preclude transmission during the first outbreaks poses a serious threat to public
waves of the pandemic when immunity is health systems. Seasonal influenza pro- U.S.A. 96, 790 (1999).
generally low—but perhaps sufficient to duces millions of severe infections world- 10. S. M. Kissler, C.Tedijanto, E. Goldstein,Y. H. Grad, M.
favor seasonal, phase-locked transmission wide every year, and this additional burden
during winter in temperate regions, similar could be catastrophic on systems already Lipsitch, Science 368, 860 (2020).
to influenza virus, once immunity increases. challenged by the COVID-19 pandemic. 11. J. Shaman, M. Kohn, Proc. Natl.Acad. Sci. U.S.A. 106,
Conversely, given similar modes of trans-
Like the 2009 influenza pandemic, the mission among different respiratory vi- 3243 (2009).
continued circulation by SARS-CoV-2 fol- ruses, the nonpharmaceutical interventions 12. A. S. Monto et al., J. Infect. Dis. 222, 9 (2020).
lowing this initial pandemic period will adopted to mitigate SARS-CoV-2 transmis- 13. A.Wu et al., Lancet Microbe 10.1016/S2666-

5247(20)30114-2 (2020).
14. D. Kim,J. Quinn, B. Pinsky, N. H. Shah, I. Brown, JAMA

323, 2085 (2020).
15. WHO,www.who.int/influenza/surveillance_monitoring/

updates/2020_08_31_update_GIP_surveillance/en/
(2020).

ACKNOWLEDGMENTS

J.S. and Columbia University partially own SK Analytics. J.S.
consults for BNI. This work was supported by U.S. National
Science Foundation grant DMS-2027369 and a gift from the
Morris-Singer Foundation.

Published online 14 October 2020

10.1126/science.abe5960

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INSIGHTS | PERSPECTIVES

LANDMARK: ANIMAL INTELLIGENCE

Charles H. Turner, pioneer in animal cognition

An African American scientist’s early discoveries are forgotten for all the wrong reasons

By Hiruni Samadi Galpayage Dona He obtained his M.Sc. from the University cap was moved to a nearby location next to
and Lars Chittka of Cincinnati in 1892 (4). In the same year, an artificial burrow that Turner had made,
the 25-year-old published two single-author the bee crawled into that burrow without
I n the late 19th and early 20th centu- papers in Science—one of which was a short hesitation—indicating, just as in Tinbergen’s
ries, Charles Henry Turner (1867–1923) version of his B.Sc. work on the comparative experiments, that the insect had a memory
established a research program that was anatomy of bird brains, whose relative size for landmarks rather than, for example, be-
in sharp contrast to prevailing ideas re- and complexity he compared with those of ing guided by an instinct to follow the scent
garding animal behavior and cognition. reptiles (1). Turner’s verdict was, “When we of the nest (8).
Despite facing almost insurmountable compare the brain of a crow or a titmouse
barriers because of his African American with the brain of a snake or a turtle, it is no In 1912, in a study that explored how a prey-
ethnicity, he published more than 70 pa- longer a marvel that birds bear towards their carrying walking wasp finds its way home
pers, including several in Science (1–3), on reptilian cousins the relation of intellectual around obstacles in the path, Turner explic-
comparative brain anatomy in birds and in- giants to intellectual dwarfs” [(1), p. 16]. The itly confronted Thorndike, affirming that the
vertebrates, individual variation of behavior same year also saw the publication of an- wasp’s behavior is not explicable by trial-and-
and learning competences, and intelligent other remarkable study on variations in web error learning and is instead consistent with
problem-solving in a large variety of animals, building by gallery spiders (5) that contained a form of intentionality and an awareness of
at a time when the dominant ideas only cred- key ingredients of Turner’s distinct interpre- the desired outcome of the wasp’s actions (9).
ited animals with the simplest of learning tation of animal behavior that was to accom- Moreover, Turner found that an ant stuck on
abilities. But his discoveries and conceptual pany his entire body of work. Like many of a small island began assembling a bridge to
advances failed to gain the recognition they his future papers, the study interfaces care- the “mainland,” using three different mate-
deserved, and his works were later all but ful field observations with meticulously con- rials (10). The ant’s behavior could not eas-
forgotten—indeed, some recent animal cogni- trolled laboratory work. Contrary to the still- ily be explained by then-popular notions of
tion research has reinvented wheels that had popular view that spider web construction instinct or trial-and-error learning; instead,
already been fashioned by Turner. is a prime example of invertebrates’ robotic, the ant appeared to appreciate the nature of
repetitive action patterns, Turner reported the problem, imagined a solution, and then
Charles Darwin (1809–1882) and George variation between individuals in adapting worked toward this goal.
Romanes (1848–1894) were famously gener- their construction to the geometry of avail-
ous in attributing intelligent behavior and able space and the functionality in captur- The view that animals are capable of in-
mental abilities to animals, but their mus- ing prey: “we may safely conclude that an sightful problem-solving was also apparent
ings were largely based on observation and instinctive impulse prompts gallery spiders in Turner’s interpretation of his field obser-
inference. The predominant experimentalist to weave gallery webs, but the details of the vations of the hunting behavior of a snake
theories of animal behavior in the early 20th construction are the products of intelligent pursuing a lizard (3). The lizard had escaped
century, however, largely rejected notions action” [(5), p. 110]. In the year of his Ph.D. up a tree and looked downward where it ex-
of advanced animal intelligence or insight. (1907), Turner published on associative and pected the snake to launch the next attack.
Early ethologists such as Oskar Heinroth, spatial learning in ants and reported individ- The snake, which had been pursuing the liz-
Charles Whitman, and Wallace Craig focused ual learning curves of their performance (6). ard for some time, instead ascended another
instead on innate behavior and imprinting, Turner’s focus on individual differences in tree, crossed over when it had reached a point
a simple form of learning. Where problem- behavior is a constant theme in his studies. higher than the lizard, and then attacked from
solving was observed, such as when ani- It is deplorable that the now-popular field of behind. These observations are reminiscent
mals open puzzle boxes, behaviorists such as “animal personality” has taken so little no- of the detour behavior seen when jumping
Edward Thorndike proposed that this ma- tice of Turner’s trailblazing approach. spiders hunt—discovered in the 1990s (11). It
terialized as a result of trial and error, not is remarkable that Turner’s views on animal
insight or understanding of the nature of The list of Turner’s discoveries and in- intentionality preceded present-day explora-
the challenge. None of these scientists were sights that should have garnered attention, tions of the same topic by a century. Even
interested in individual variation of behav- but did not, is long. Every student of animal though his experimental work was known
ior. Enter Charles H. Turner, who took seri- behavior knows Nikolaas Tinbergen’s study to contemporary giants such as John Watson
ously Darwin’s assertion of the importance of from 1932 on spatial learning, in which the and Thorndike (4) and across the Atlantic by
individual variation as well as the idea that later Nobel laureate (awarded for studies of later Nobel laureate Karl von Frisch, Turner’s
humans were not the only intelligent animal individual and social behavior in animals) visionary ideas about animal intelligence did
species. But Turner backed up this possibility first marked a beewolf’s nest entrance with not resonate in the field; perhaps they were
with a rigorous experimental approach. pine cones, then moved them to demonstrate simply too far ahead of the time. Accordingly,
that the insect was guided by a memory of they are almost completely unrecognized in
Turner was born just 2 years after the the landmarks (7). But it is mostly unknown the current literature.
end of slavery in the United States in 1865. that Turner had already published similar
findings in 1908, observing a solitary bur- Further highlighting the importance and
Department of Psychology, School of Biolological and rowing bee whose nest entrance was close to insightful nature of Turner’s work, in 1913
Chemical Sciences, Queen Mary University of London, a discarded Coca Cola bottle cap. When the he reported on the effects of age and sex on
London, UK. Email: [email protected]; cockroaches trained to navigate mazes (12).
[email protected] Turner found that individuals placed an em-

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From Charles H. Turner to 1 2
comparative cognition: 1850–2020 3

Charles H. Turner made important observations about animal cognition, which went
against the leading paradigms of the time. His ideas have stood the test of history, but
Turner’s work has largely been forgotten, likely because his ethnicity prevented him
from becoming a research team leader and so he could not train scientists who might
have continued his approach. Turner was active in the U.S. civil rights movement and
advocated that education is key to overcoming ethnic barriers in society.

1867 1891 1907 1913 1917
Charles B.Sc., University of Ph.D., University of Maze learning E. St. Louis
Turner is born Cincinnati; publishes Chicago; publishes in cockroach; massacre while
in Cincinnati on comparative individual learning discusses a Turner teaches at
anatomy of bird brains curves of ants “will” in roaches school in St. Louis

1 23

1865 1892 1908 1909 1923 1932 1994 2009
End of M.Sc., University of Demonstrates Discovers Turner dies Tinbergen publishes his Tarsitano and Heisenberg
American Cincinnati; publishes on spatial learning in detour “pine cone” experiment on Jackson discover discusses “free
Civil War individual variation and a bee by moving behavior in Chicago spatial learning in wasps detour behavior will” in insects
intelligence in spiders landmark at nest in a snake in a spider

GRAPHIC: V. ALTOUNIAN/SCIENCE; (IMAGES, CLOCKWISE FROM LEFT) WIKIMEDIA COMMONS;C. H. TURNER ET AL.(12); ST. LOUIS GLOBE-DEMOCRAT, 3 JULY 1917, P. 1 phasis on either speed or accuracy: Older that learning largely happens in the form of minority students can also make a substan-
cockroaches choose slowly but more pre- simple associations), if Turner’s ideas about
cisely. Extraordinarily, Turner suggests that advanced cognition in animals had generated tial difference to inspire budding scientists.
the hesitation that cockroaches display when a movement at the time he expressed them?
evaluating their options bears the hallmarks Institutions must make still-stronger efforts
of will, a facet of consciousness. The question African American historian William
of whether humans and other animals exhibit Du Bois (1868–1963) lamented that “C. H. to eliminate biases in hiring, promotions,
free will continues to generate controversy Turner, one of the great world authorities on
among neuroscientists and philosophers. insects, nearly entered the faculty of Chicago and salary decisions and to celebrate the
That insights from insect behavior could con- University; but the head professor who called
tribute to this debate has only recently been him died, and his successor would not have successes of ethnic minority scholars. Even
suggested again by neuroscientist Martin a “N-----,” despite a reputation which was
Heisenberg (13), who proposed that insects European; Turner died in a high school of ne- where they do (and there is likely plenty of
display an awareness of the consequences of glect and overwork” [(4), p. 348]. The institu-
their actions and evidence of free will in de- tion at which Turner taught from 1908 to 1922 room for improvement), overt or poorly con-
ciding between options. was Sumner High School, a school for African
American children in St. Louis. During his cealed racism is still commonly experienced
Why is Turner not more widely credited as time there, he and his pupils would have wit-
a major luminary in research on animal in- nessed the East St. Louis massacre in 1917, by underrepresented ethnic groups, even in
telligence? Turner faced substantial obstacles during which white mobs murdered more
because of his ethnicity. Despite publishing than 100 African Americans; another 6000 academia. This will likely discourage many
many important papers, he was not given lost their homes as a result of arson attacks
a post at a major U.S. research university. on their neighborhoods (14). Turner was ac- aspiring scientists from venturing further. A
Turner’s work was thus conducted without tive in the U.S. civil rights movement, and
access to state-of-the-art laboratory facilities years before coming to St. Louis, he wrote hopeful development is that some conference
or library resources. One reason for Turner’s that an emphasis on high-quality education
relative obscurity today may be that he had and a conscious effort to abandon prejudices organizers are taking steps in the right direc-
no possibility of mentoring research students might eliminate barriers between Blacks and
who would have carried his ideas into subse- whites within a few decades (15). tion to increase inclusivity; for example, the
quent generations. For comparison, Russian
Nobel laureate Ivan Pavlov (1849–1936), One would hope that nowadays, a person Animal Behavior Society annually supplies
famed for his studies on classical condition- of Turner’s caliber might not face similar ad-
ing, trained more than 140 co-workers. One versity in terms of academic employment op- the Charles H. Turner award that prioritizes
cannot help but wonder what Turner might portunities or long-term recognition of their
have achieved if he had had comparable re- contribution to science. But even today, very traditionally underrepresented groups for
sources and manpower. The entire field of few scholars in animal cognition, or indeed
animal cognition may have developed dif- across biology, are Black. Turner clearly rec- conference travel funding. More than ever,
ferently. Would a “cognitive revolution” have ognized the importance of ethnic-minority
been needed against the dominant ideas of role models from the earliest stages of educa- humanity needs to be inclusive to confront
behaviorism that ruled psychology for the tion; their near-complete absence in a field of
first half of the 20th century (postulating scholarly study will require concerted coun- current and future challenges. Diversity in-
terefforts. Funded summer schools for ethnic
creases the pool of talent and, as Turner’s

example shows, has the potential to trans-

form entire fields. j

REFERENCES AND NOTES

1. C. H.Turner, Science 19, 16 (1892).
2. C. H.Turner, Science 20, 39 (1892).
3. C. H.Turner, Science 30, 563 (1909).
4. C. I.Abramson, Annu. Rev. Entomol. 54, 343 (2009).
5. C. H.Turner, J. Comp. Neurol. 2, 95 (1892).
6. C. H.Turner, J. Comp. Neurol. Psychol. 17, 367 (1907).
7. N.Tinbergen, J. Comp. Physiol.A Neuroethol. Sens.

Neural Behav. Physiol. 16, 305 (1932).
8. C. H.Turner, Biol. Bull. 15, 247 (1908).
9. C. H.Turner, Psyche 19, 100 (1912).
10. C. H.Turner, Biol. Bull. 13, 333 (1907).
11. M. S.Tarsitano, R. R.Jackson, Behaviour 131, 65 (1994).
12. C. H.Turner, Biol. Bull. 25, 348 (1913).
13. M. Heisenberg, Nature 459, 164 (2009).
14. J. N. Harrington, Buzzing with Questions: The Inquisitive

Mind of Charles Henry Turner (Boyds Mills Press, 2019).
15. C. H.Turner, in Twentieth Century Negro Literature (J. L.

Nichols, 1902), pp. 162–166.

10.1126/science.abd8754

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INSIGHTS | PERSPECTIVES

RETROSPECTIVE

Paolo Sassone-Corsi (1956–2020)

Groundbreaking molecular biologist and epigeneticist

By Eric Verdin period, he identified a previously un- neering studies, Paolo became a leader in PHOTO: STEVE ZYLIUS/UCI
known messenger in the cAMP signaling the fields of circadian rhythms, epigenetics,
P aolo Sassone-Corsi, eminent molecu- pathway—the cAMP-responsive element and metabolism.
lar biologist, died unexpectedly at the modulator (CREM)—and characterized its
age of 64 on 22 July in Laguna Beach, role in spermiogenesis and germ cell apo- Having worked in similar fields, I came
California. Paolo made seminal con- ptosis. The identification of a distinctive to know Paolo at scientific meetings and
tributions in the fields of transcrip- circadian fluctuation of CREM expression through service on advisory boards, visits
tional regulation, epigenetics, circa- in the pineal gland led Paolo and his team to UCI, and collaborative efforts. I will re-
dian biology, and metabolic regulation, and into chronobiology, a fitting reconnection member him for his beautiful lectures, his
he pioneered the discovery of key links be- with astronomy, as this field of biology ex- charm, his warmth, the twinkle in his eye
tween these disciplines. plores the consequences of Earth’s rotation when he would gently tease you, his passion
and the 24-hour cycle of light and darkness for science, and his love and pride for his
Born in Naples, Italy, in 1956, Paolo de- that it imposes on all living organisms. students and postdocs. More than anything,
voted himself to science and discovery many of us will remember his zest for life,
from an early age. At just 12 years old, he In 2006, the University of California, food, wine, and science and his incredibly
founded an amateur astronomy club with Irvine (UCI), recruited Paolo and his generous hospitality.
his brother Emilio in Naples. (Ten years wife, prominent neurobiologist Emiliana
later, the two brothers would publish a pa- Borrelli. Paolo was hired as a distinguished Paolo and Emiliana excelled at organiz-
per on the bands of Saturn.) Although he ing memorable meetings. Their biannual
retained his passion for astronomy, Paolo professor and led the Department of Epigenetic Control and Cellular Plasticity
decided to focus his graduate studies on Pharmacology for 5 years. He then founded International Symposium was known not
yeast biology; he received his doctorate the university’s Center for Epigenetics and only for the caliber of its science but also
in biological sciences in 1979 from the Metabolism, an interdisciplinary center re- for Paolo and Emiliana’s warmth and hos-
University of Naples Federico II. The uni- flecting his increasing interest in metabo- pitality. They had moved to UCI in hopes
versity would honor him as a most merito- lism and circadian biology in relation to of living somewhere climatically and geo-
rious alumnus in 2016. epigenetics. Paolo’s singular understand- graphically similar to their native Italy. In
ing of transcriptional regulation led to a the process, they brought a big slice of Italy
During a postdoc under the mentorship series of additional groundbreaking dis- and its dolce vita to California for everyone
of molecular biologist Pierre Chambon at coveries, including the dissection of tran- to enjoy. Paolo made all of us, his guests,
the Institut de Génétique et de Biologie scriptional and epigenetic mechanisms feel truly special. His pride and joy in want-
Moléculaire et Cellulaire (IGBMC) in that regulate circadian rhythms and an ing to share with me a beautiful sunset at
Strasbourg, France, Paolo was drawn to explanation of how they respond to meta- the Pelican Inn in Newport Beach remains
the basic mechanisms of transcription. He bolic states. He was first to demonstrate to this day a special moment with a cher-
contributed key work on promoters, en- that the key oscillating transcription fac- ished colleague and friend.
hancers, and transactivating factors as well tor CLOCK is a histone acetyltransferase,
as the identification and characterization and he characterized how the deacetylase Paolo’s creativity, originality, and scien-
of a promoter sequence of the adenovirus SIRT1 and fluctuations in concentrations tific courage were recognized by his elec-
major late gene that became known as the of nicotinamide adenine dinucleotide and tion as a fellow of the American Association
TATA box, a hallmark regulatory element its reduced form participate in the control for the Advancement of Science (AAAS, the
of most eukaryotic genes. He then moved of circadian rhythms. Through these pio- publisher of Science) in 2014, as well as nu-
to the Salk Institute for Biological Studies merous awards. He received the Grand Prix
in San Diego, California, where he studied Liliane Bettencourt in 1997 and the Grand
the intracellular pathway leading to the ac- Prix Charles-Léopold Mayer de l’Académie
tivation of the proto-oncogenes c-fos and des Sciences in 2003. He also served on var-
c-jun and demonstrated their mechanism ious scientific advisory boards and journal
of action in the regulation of transcrip- editorial boards.
tion; he showed that c-fos and c-jun inter-
act with each other, and he identified the The scientific community has lost in
regulation of c-fos by cyclic adenosine mo- Paolo a trailblazing scientist, a superb
nophosphate (cAMP). and generous colleague and mentor, and a
witty, adventurous, and warm friend. Paolo
In 1989, Paolo established his first inde- is survived by Emiliana and his brothers
pendent laboratory at the IGBMC, where Lucio and Emilio Sassone-Corsi. For all of
he rapidly progressed to the level of di- us who counted Paolo as a close friend, his
rector of research at the Centre National early departure is hard to accept. Our loss
de la Recherche Scientifique. During this is balanced only by the gratitude we feel for
having had the chance to cross paths with
Buck Institute for Research on Aging, Novato, CA 94945, and draw inspiration from this brilliant,
USA. Email: [email protected] generous colleague. j

10.1126/science.abe9149

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POLICY FORUM POLITICAL SECTARIANISM
In the past decade, political scientists have

introduced various constructs to capture this

SOCIAL SCIENCE nonideological type of polarization, includ-

Political sectarianism in America ing “affective polarization” (1) and “social
polarization” (4). Scholars from psychology
and other disciplines have introduced con-
structs, such as “tribalism” (SM), to flesh out

A poisonous cocktail of othering, aversion, and moralization its social-psychological properties.

poses a threat to democracy We propose here a superordinate con-
struct, political sectarianism—the tendency

to adopt a moralized identification with

By Eli J. Finkel1,Christopher A. Bail2,Mina ward the in-party (see the figure, bottom one political group and against another.

Cikara3,Peter H. Ditto4,Shanto Iyengar5, panel). Out-party hate has also become Whereas the foundational metaphor for trib-

Samara Klar6,Lilliana Mason7,Mary C. more powerful than in-party love as a pre- alism is kinship, the foundational metaphor

McGrath1,Brendan Nyhan8,David G. Rand9, dictor of voting behavior (2), and by some for political sectarianism is religion, which

Linda J. Skitka10,Joshua A. Tucker11,Jay J. Van metrics, it exceeds long-standing antipa- evokes analogies focusing less on genetic re-

Bavel11,Cynthia S. Wang1,James N. Druckman1 thies around race and religion (SM). latedness than on strong faith in the moral

This aversion to opposing partisans might correctness and superiority of one’s sect.

P olitical polarization, a concern in make strategic sense if partisan identity Political identity is secondary to religion
many countries, is especially acrimo- served as a strong proxy for political ideas. in traditional forms of sectarianism, but it
nious in the United States (see the But given that sectarianism is not driven pri- is primary in political sectarianism. In the
first box). For decades, scholars have marily by such ideas (SM), holding opposing United States today, even though Democrats
studied polarization as an ideologi- partisans in contempt on the basis of their and Republicans differ on average in terms

cal matter—how strongly Democrats identity alone precludes innovative cross- of religious affiliation, their schism is funda-

and Republicans diverge vis-à-vis political party solutions and mutually beneficial com- mentally political rather than religious. It is,

ideals and policy goals. Such competition promises. This preclusion is unfortunate, as in this sense, quite distinct from the Sunni-

among groups in the marketplace of ideas common ground remains plentiful. Indeed, versus-Shia sectarian schisms that character-

is a hallmark of a healthy democracy. But despite the clear evidence that partisans have ize politics in some Muslim-majority nations.

more recently, researchers have identified grown increasingly disdainful of one another, Political sectarianism consists of three core

a second type of polarization, one focusing the evidence that they have polarized in ingredients: othering—the tendency to view

less on triumphs of ideas than on dominat- terms of policy preferences is equivocal (3). opposing partisans as essentially different or

ing the abhorrent supporters of the oppos- Along the way, the causal connection be- alien to oneself; aversion—the tendency to

ing party (1). This literature has produced tween policy preferences and party loyalty dislike and distrust opposing partisans; and

a proliferation of insights and constructs has become warped, with partisans adjust- moralization—the tendency to view opposing

but few interdisciplinary efforts to inte- ing their policy preferences to align with partisans as iniquitous. It is the confluence

grate them. We offer such an integration, their party identity (SM). For example, a of these ingredients that makes sectarianism

pinpointing the superordinate construct recent experiment demonstrated that Re- so corrosive in the political sphere. Viewing

of political sectarianism and identifying publicans exhibit a liberal attitude shift opposing partisans as different, or even as

its three core ingredients: othering, aver- after exposure to a clip of President Don- dislikable or immoral, may not be problem-

sion, and moralization. We then consider ald Trump voicing a liberal policy position atic in isolation. But when all three converge,

the causes of political sectarianism and its (SM); there is little evidence to suggest that political losses can feel like existential threats

consequences for U.S. society—especially Democrats are immune to analogous shifts that must be averted—whatever the cost.

the threat it poses to democracy. Finally, in response to their own political leaders.

we propose interventions for minimizing Overall, the severity of political conflict WHY SECTARIANISM IS SURGING

its most corrosive aspects. has grown increasingly divorced from the Rising political sectarianism in the United

magnitude of policy disagreement (4). States is multiply determined; here we con-

ASCENDANCE OF POLITICAL HATRED

Democrats and Republicans—the 85% of

U.S. citizens who do not identify as pure On American exceptionalism
independents—have grown more contemp-
tuous of opposing partisans for decades, A recent study offers valuable international perspective on political polarization,
and at similar rates [see supplementary leveraging data from 1975 through 2017 in nine Western democracies to examine feel-
materials (SM)]. Only recently, however, ings toward copartisans and opposing partisans. The study controls statistically for the
has this aversion exceeded their affection number of parties and offers a valuable, albeit noncomprehensive, comparison set (13).
for copartisans. On a “feeling thermome-
ter” scale ranging from cold (0°) to neutral Four nations—America, Canada, New Zealand, and Switzerland—exhibit increasing
(50°) to warm (100°), affect toward copar- sectarianism over time, with the rate steepest in America. By contrast, Australia, Britain,
tisans has consistently hovered in the 70° Norway, Sweden, and Germany exhibit decreasing sectarianism over time. The most
to 75° range. By contrast, affect toward op- notable findings pertain to out-party hate [increasingly “frigid” evaluations of opposing
posing partisans has plummeted from 48° partisans, via a “feeling thermometer” (see main text)]. Across the eight other nations,
in the 1970s to 20° today (see the figure, the mean rate of change in out-party hate was 0.004° per year (range: –0.2° to +0.2°)
top panel). And cold feelings toward the on the 0°-to-100° scale. In the United States, the rate of change was –0.6° per year. By
2017, out-party hate was stronger in America than in any other nation.

out-party now exceed warm feelings to-

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INSIGHTS | POLICY FORUM

The rise of out-party hate ducing cable news faltered with the launch
of the conservative Fox News in 1996 and the
With the exception of 2020, all data come from the American National Election Study (ANES), as reported in (1). liberal pivot of MSNBC a decade later. People
To calculate the estimates for the lower panel, we used upper-panel estimates to compute, relative to the neutral who are already sectarian selectively seek out
point on the feeling thermometer, the strength of in-party love (in-party score – 50) and out-party hate (50 – congenial news, but consuming such content
out-party score), and then took the difference of those two scores. See supplementary materials for details. also amplifies their sectarianism (SM).

Warmth toward the opposing party (out-party) has diminished for decades In recent years, social media companies
like Facebook and Twitter have played an
In-party Out-party influential role in political discourse, inten-
100° Warm sifying political sectarianism. Scholars from
sociology, political science, economics, psy-
Feeling thermometer ratings 75° chology, and computational social science
50° Neutral debate whether such web platforms create
polarizing echo chambers (7) (SM). However,
25° a recent field experiment offers intriguing ev-
idence that Americans who deactivate their
0° Cold 1984 1988 1992 1996 2000 2004 2008 2012 2016 2020 Facebook account become less politically po-
1980 larized (8). In addition, emotional and mor-
alized posts—those containing words like
In-party love – Out-party hateOut-party hate has emerged as a stronger force than in-party loveMean = –4.5 “hate,” “shame,” or “greed”—are especially
2012 2016 2020 likely to be retweeted within rather than be-
25° Mean = 19.2 tween partisan networks (9). Social-media
technology employs popularity-based algo-
20° rithms that tailor content to maximize user
Mean = 11.3 engagement, increasing sectarianism within
homogeneous networks (SM), in part be-
15° cause of the contagious power of content that
elicits sectarian fear or indignation.
10°
5° Third, in contrast to the equivocal ideo-
logical-polarization trends among the pub-
0° lic, politicians and other political elites have
unambiguously polarized recently on ideo-
-5° logical grounds, with Republican politicians
moving further to the right than Democratic
-10° politicians have moved to the left (SM). This
ideological divergence is driven in part by ex-
-15° treme economic inequality in America today,
1980 1984 1988 1992 1996 2000 2004 2008 especially in conjunction with candidates be-
coming increasingly reliant on ideologically
sider three crucial causes. First, in recent litically engaged, contemptuous, and unco- extreme donors. As politicians chase cam- GRAPHIC: N. CARY/SCIENCE
decades, the nation’s major political parties operative than is actually the case (5) (SM), paign dollars, these extreme voices garner
have sorted in terms of ideological identity thereby exacerbating political sectarianism. disproportionate influence (SM).
and demography. Whereas self-identified For example, Republicans estimate that
liberals and conservatives used to be dis- 32% of Democrats are LGBT when in real- The ideological divergence of political
tributed broadly between the two parties, ity it is 6%; Democrats estimate that 38% elites contributes to political sectarianism, es-
today the former are overwhelmingly Dem- of Republicans earn over $250,000 per year pecially as these individuals increasingly use
ocrats and the latter are overwhelmingly when in reality it is 2% (6). disciplined messaging to discuss their pre-
Republicans (SM). The parties also have ferred topics in their preferred manner (SM).
sorted along racial, religious, educational, Second, as Americans have grown more Such messaging leads the public to perceive
and geographic lines. Although far from receptive to consuming information slanted sharper ideological distinctions between the
absolute, such alignment of ideological through a partisan lens, the media ecosys- parties than actually exists, which inflames
identities and demography transforms po- tem has inflamed political sectarianism. The sectarianism (SM). In addition, Newt Gin-
litical orientation into a mega-identity that decline of the broadcast news era, during grich and his followers achieved electoral
renders opposing partisans different from, which impartiality was prized, began in the success with strongly moralized language in
even incomprehensible to, one another (4). 1980s, driven in part by the Reagan admin- the 1980s and 1990s, inspiring political elites
This mega-identity can grow so powerful istration’s termination of the Federal Com- on both sides to double down on the rhetoric
that it changes other identities, as when munications Commission (FCC) “fairness
partisans alter their self-identified religion, doctrine” in 1987. This doctrine, introduced 1Northwestern University, Evanston, IL, USA.2Duke
class, or sexual orientation to align with in 1949, required that broadcasters discuss University, Durham, NC, USA.3Harvard University,
their political identity (SM). controversial topics in a manner that the FCC Cambridge, MA, USA.4University of California, Irvine,
assesses as unbiased. Among the first media Irvine, CA ,USA.5Stanford University, Stanford, CA, USA.
As distinct as Democrats and Republi- figures to leverage the demise of the fairness 6University of Arizona, Tuscon, AZ, USA.7University of
cans actually are today, partisans neverthe- doctrine was Rush Limbaugh, whose influen- Maryland, College Park, MD, USA.8Dartmouth College,
less vastly overestimate such differences. tial conservative radio program went into na- Hanover, NH, USA.9Massachusetts Institute of Technology,
They view opposing partisans as more tional syndication in 1988 (SM). The ethos of Cambridge, MA, USA.10University of Illinois at Chicago,
socially distant, ideologically extreme, po- impartiality that CNN espoused when intro- Chicago, IL, USA.11New York University, New York, NY, USA.
Email: [email protected]; [email protected]

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of moral outrage (e.g., “disgraceful,” “shame- checks and balances, or civil liberties (11). gating climate change, reducing the federal
ful”), further exacerbating sectarianism (SM). Voters’ decisions to support such a candidate debt, and safeguarding democratic rights.
may seem sensible if they believe the harm to
These three trends—identity alignment, democracy from any such decision is small America’s response to the coronavirus
the rise of partisan media, and elite ideo- while the consequences of having the vile disease 2019 (COVID-19) pandemic high-
logical polarization—have contributed to opposition win the election are catastrophic. lights the perils of political sectarianism. An
radically different sectarian narratives about However, the accumulation of such choices October 2019 report from Johns Hopkins
American society and politics. Although the undermines representative democracy. And University suggested that America was bet-
content of these narratives is entirely differ- a society that pretends to adhere to demo- ter prepared for a pandemic than any other
ent across the political divide, their structure cratic principles but actually does not is one nation (SM), but that report failed to account
is similar: The other side cheats, so our side in which people who possess resources and for the sort of political sectarianism that
would be foolish to adhere to long-standing influence can leverage democratic gray zones would, months later, make mask-wearing a
democratic norms. These narratives, which to impose their will on those who do not. partisan symbol, one favored more by Demo-
partisans experience less as stories than as crats than by Republicans. Democrats were
truth (SM), increase their willingness to sac- Sectarianism stimulates activism (SM), also more likely to prioritize stay-at-home
rifice those norms in pursuit of partisan ends. but also a willingness to inflict collateral orders despite their massive, immediate eco-

DARK CONSEQUENCES Is motivated partisan cognition bipartisan?
Rising political sectarianism has, not sur-
prisingly, increased the social distance The extent to which each side exhibits motivated partisan (or biased) cognition is a
between Democrats and Republicans. Com- focus of ongoing debate. Some scholars argue for symmetry (SM). For example, a
pared to a few decades ago, Americans today recent meta-analysis demonstrates equivalent levels of motivated partisan cognition
are much more opposed to dating or marry- across 51 experiments investigating the tendency to evaluate otherwise identical in-
ing an opposing partisan; they are also wary formation more favorably when it supports versus challenges one’s political beliefs or
of living near or working for one. They tend allegiances (14). In an illustrative experiment, liberals and conservatives viewed a film
to discriminate, as when paying an opposing clip of a political demonstration in which protestors clashed with police. Despite view-
partisan less than a copartisan for identical ing the identical clip, liberals rated the protesters as more violent when they believed
job performance or recommending that an it was an anti-abortion protest (a conservative cause) rather than a gay-rights protest
opposing partisan be denied a scholarship (a liberal cause), whereas conservatives exhibited the opposite pattern (SM).
despite being the more qualified applicant
(1). They are also susceptible to motivated Other scholars argue for asymmetry. For example, some evidence suggests that,
partisan cognition—seeking out, believing, relative to Democrats, Republicans have a higher need for order and greater trust in
and approving of information more readily their gut-level intuitions. Such tendencies appear to motivate them to favor explana-
when it reflects positively on copartisans or tions that are straightforward and intuitive rather than complex and abstract, even
negatively on opposing partisans (10) (SM)— when the latter types of explanation might be more accurate (15) (SM). Such findings
although scholars debate whether such ten- are representative of the existing evidence, but conclusions remain tentative.
dencies are equally strong among Democrats
and Republicans (see the second box). damage in pursuit of political goals (SM) nomic cost—a pattern that was especially
and to view copartisans who compromise prominent among highly sectarian partisans
These manifestations of political sectari- as apostates (SM). As political sectarianism (SM). This schism, fomented in part by Presi-
anism echo those that emerge from religious has surged in recent years, so too has sup- dent Trump, pushed toward a disequilibrium
sectarianism. What is distinctive about po- port for violent tactics (SM). In addition, in which too few people engaged sufficiently
litical sectarianism—beyond its largely non- highly sectarian partisans are vulnerable to in commerce to stimulate economic growth
theological foundation—is the immediacy of exploitation. In 2016, Russia sought to stoke while too few social-distanced sufficiently to
its links to governance. Political sectarianism partisan outrage during America’s election contain the pandemic. The result has been
compromises the core government function by creating fake social-media avatars with lethal and expensive for Americans across
of representation. Because sectarian parti- names like “Blacktivist” and “army_of_je- the political spectrum.
sans almost never vote for the opposition, sus.” These efforts succeeded in duping sec-
politicians lack the incentive to represent tarian extremists—especially those who were MITIGATING SECTARIANISM
all of their constituents. Straight-ticket vot- older and more conservative than average— Political sectarianism is neither inevitable
ing has grown increasingly widespread. In into amplifying the avatars’ memes about nor irreversible. When considering promis-
contested districts, the correlation of the the depravity of opposing partisans (SM). In ing avenues for intervention, the goal is not
Democratic share of the House vote and the doing so, these partisans served as pawns in to restore America to some halcyon republic
Democratic share of the presidential vote— Russia’s efforts to weaken America. of yore. As exemplified by the 1870s transi-
the association of district-level with national tion from the relatively antiracist Reconstruc-
representation—surged from 0.54 in the Political sectarianism also undermines the tion era to the deeply racist Redemption era,
1970s to 0.94 by the 2010s (2). core government function of competence— many historic episodes of partisan comity
of providing for and protecting the people. rested upon bipartisan support for (or at least
Perhaps most troubling of all, the politi- Members of Congress increasingly prioritize acquiescence to) antidemocratic institutions
cal sectarianism of the public incentivizes partisan purity over the sorts of compro- and behaviors, including the marginalization
politicians to adopt antidemocratic tactics mises that appeal to a large proportion of the and disenfranchisement of women and racial
when pursuing electoral or political victo- population, a tendency that creates legisla- minorities. The current divide is so potent in
ries. A recent experiment shows that, to- tive gridlock. Issues that are not inherently part because battles surrounding sexism and
day, a majority-party candidate in most U.S. partisan become politicized, impeding the racism have grown strongly partisan.
House districts—Democrat or Republican— ability to make progress on goals like miti-
could get elected despite openly violating
democratic principles like electoral fairness,

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INSIGHTS | POLICY FORUM

Rather, the goal of these interventions is for surging sectarianism, but simply tweak- fact-checkers and mobilizing sectarian loy-
to move toward a system in which the public ing algorithms to show partisans more alists to believe “alternative facts.”
forcefully debates political ideals and policies content from the opposition may aggravate
while resisting tendencies that undermine sectarianism rather than reducing it (7). As political sectarianism grows more ex-
democracy and human rights. Given that More promising are interventions that en- treme, pushing strong partisans deeper into
substantial swaths of American society (in- courage people to deliberate about the accu- congenial media enclaves that reinforce
cluding many who identify as Democrat or racy of claims on social media, which causes their narratives of moral righteousness, it
Republican) are fed up with surging sectari- them to evaluate the substance of arguments may also become self-reinforcing, rendering
anism (SM), dedicated efforts to mitigate it and reduces their likelihood of sharing false mitigation efforts more difficult. Scholars
may well land in fertile soil. Such efforts or hyperpartisan content (12) (SM). Another have long argued that a shared threat can
must circumvent the sectarian true believ- option is to use crowdsourcing to identify bring people together; indeed, some suggest
ers, profiteers, and chaos-seekers who ben- such content and the outlets that emit it, that rising sectarianism in America is due
efit from stoking sectarianism. These actors relying on users’ ratings of trustworthiness in part to the loss of the Soviet Union as
contribute directly to political sectarianism, to augment the efforts of professional fact- a unifying arch-nemesis. But such threats
and they leverage the government sclerosis checkers. Such information can be incorpo- may do the opposite when sectarianism is
caused by political sectarianism to derail rated into algorithmic rankings to reduce the extreme. COVID-19 offered a test case (SM).
efforts to address structural sources of that presence of false or hyperpartisan content in By the summer of 2020, 77% of Americans
sectarianism, such as economic inequities people’s news feeds (SM). believed that the nation had grown more
and biased electoral procedures (SM). divided since the pandemic arrived that
A third avenue involves creating incen- winter, a response 2.8 standard deviations
Nonetheless, scholars have begun to iden- tives for politicians and other elites to reduce higher than the mean of the 13 other na-
tify procedures that can potentially mitigate their sectarianizing behaviors. People be- tions in the study and 1.6 standard devia-
political sectarianism. These include efforts come less divided after observing politicians tions higher than the second-highest nation
to help Americans comprehend opposing treating opposing partisans warmly, and (Spain). Such findings underscore the ur-
partisans regardless of their level of agree- nonpartisan statements from leaders can re- gent need to counteract sectarianism before
ment, such as by focusing on commonalities duce violence. Campaign finance reform may it grows more poisonous.
rather than differences (e.g., “we’re all Amer- help, especially by eliminating huge contri-
icans”; SM) or communicating in the moral butions from ideological extremists (SM). Political sectarianism cripples a nation’s
language of the other side (e.g., when liberals Reducing partisan gerrymandering likely ability to confront challenges. Bolstering
frame the consequences of climate change in would make representation fairer, generate the emphasis on political ideas rather than
terms of sanctity violations; SM). more robust competition in the marketplace political adversaries is not a sufficient solu-
of political ideas, and send fewer extremists tion, but it is likely to be a major step in the
Here, we consider three avenues for in- to the House of Representatives (SM). right direction. The interventions proposed
tervention that hold particular promise for above offer some promising leads, but any se-
ameliorating political sectarianism. The first A FIERCE URGENCY rious effort will require multifaceted efforts
addresses people’s faulty perceptions or in- In 1950, the American Political Science As- to change leadership, media, and democratic
tuitions. For example, correcting mispercep- sociation issued a report expressing concern systems in ways that are sensitive to human
tions of opposing partisans, such as their that America was insufficiently polarized, a psychology. There are no silver bullets. j
level of hostility toward one’s copartisans, perspective that remained dominant in the
reduces sectarianism (5) (SM). Such correc- ensuing decades (SM). Ideological differen- REFERENCES AND NOTES
tion efforts can encourage people to engage tiation is an essential feature of party-based
in cross-party interactions (SM) or to con- democracy, sharpening debates on impor- 1. S.Iyengar,Y.Lelkes,M.Levendusky,N.Malhotra,S.J.
sider their own positive experiences with op- tant topics. Because most people lack the Westwood,Annu.Rev.Polit.Sci.22,129 (2019).
posing partisans, especially a friend, family expertise required to make informed judg-
member, or neighbor. Doing so can reduce ments on specific policies, divergent and in- 2. A.I.Abramowitz,S.Webster,Elect.Stud. 41,12 (2016).
the role of motivated partisan reasoning in ternally coherent party platforms function 3. Y.Lelkes,Public Opin.Q.80 (S1),392 (2016).
the formation of policy opinions (SM). as helpful heuristics that voters can use to 4. L.Mason,UncivilAgreement: How Politics Became Our
prioritize their preferred policies and hold
A related idea is to instill intellectual hu- politicians accountable. Identity (Univ.of Chicago Press,2018).
mility, such as by asking people to explain 5. J.Lees,M.Cikara,Nat.Hum.Behav.4,279 (2020).
policy preferences at a mechanistic level—for But the ideological polarization the 6. D.J.Ahler,G.Sood,J.Polit.80,964 (2018).
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According to a recent study, relative to peo- eclipsed among the public by political
ple assigned to the more lawyerly approach sectarianism. When politics becomes an Econ.Rev.110,629 (2020).
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ences, those asked to provide mechanistic opponents—when ideals and policies matter
explanations gain appreciation for the com- less than dominating foes—government be- Proc.Natl.Acad.Sci.U.S.A. 114,7313 (2017).
plexities involved (SM). Leaders of civic, re- comes dysfunctional. Viable political strat- 10. J.J.Van Bavel,A.Pereira,Trends Cogn.Sci.22,213 (2018).
ligious, and media organizations committed egies focus less on policy-based arguments 11. M.H.Graham,M.W.Svolik,Am.Polit.Sci.Rev.114,392
to bridging divides can look to such strate- and more on marginalizing the opposition,
gies to reduce intellectual self-righteousness with false smears and antidemocratic tac- (2020).
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pursuing unpopular policies, they are in-
A second avenue involves altering social- centivized to destroy the idea of objectivity Psychol.Sci. 31,770 (2020).
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ideas along these lines may be counterpro-
ductive. Echo chambers are widely blamed polarization (no.w26669),”National Bureau of Economic
Research; www.nber.org/papers/w26669 (2020).
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ACKNOWLEDGMENTS

We thank the Kellogg School of Management’s Dispute
Resolution Research Center and the Institute for Policy
Research, both at Northwestern University.We thank S. Matz
and A.Wilson for feedback on an earlier draft and T. Brader,
D. Costanzo, M. DeBell, L. Harbridge-Yong, E. Groenendyk, M.
Levendusky, and S.Westwood for responding to questions.

SUPPLEMENTARY MATERIALS

science.sciencemag.org/content/370/6516/533/suppl/DC1

10.1126/science.abe1715

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A woman examines a model of a Neanderthal man
at the Natural History Museum in London in 2014.

Neanderthal interactions with each other

and with human ancestors, and she con-

vincingly argues that we must recognize

the potential role of other characteristics,

including cooperation, sharing, and social

bonds, in shaping their lives.

Wragg Sykes takes a similarly consid-

ered approach in discussing why Neander-

thals went extinct. Rather than framing the

question in terms of winners and losers,

or superior and inferior species, she eval-

uates modern humans and Neanderthals

in parallel, comparing the successes and

shortcomings of each. While it is true that

Neanderthals are the ones that went ex-

tinct, our story is not one of unmitigated

success, she notes. Modern humans did not

successfully settle in Europe until long af-

ter we evolved in Africa and reached Asia,

for example, and those earliest modern hu-

BOOKS et al. mans in Europe were eventually replaced
by later waves of migration. Meanwhile, the

fact that Neanderthals existed for around

350,000 years hardly suggests failure. We,

PA L E OA N T H R O P O L O GY too, may yet succumb to environmental

The vibrant lives of Neanderthals challenges or bring about our own downfall.
In Kindred’s final chapter, Wragg Sykes
tackles broader ethical questions faced in
paleoanthropology and adjacent fields,

A nuanced portrait of our evolutionary cousins encourages which have recently come into sharp fo-

empathy and understanding cus. She highlights the problematic ways
in which human remains and cultures

have been treated in research, arguing that

By Emma Pomeroy art evidence with parallels from everyday these practices must change and, where

experience, which frame the interpretations possible, be redressed. These are uncom-

O ver the past several decades, many and challenges inherent in the data in more fortable topics to confront, but it is vital
academic and popular writers have familiar terms. that we do so in order to understand the
attempted to narrow the long- full legacies of the field and to hold future
entrenched gulf between humans and A recurring perspective in Kindred is research to higher ethical standards.
Neanderthals, focusing, for example, that diversity can and should be expected
in Neanderthal behavior, given She also addresses the possibil-

on the misinterpretations and rac- their existence over hundreds of ity of reviving Neanderthal tissues

ist presumptions of the 19th and early 20th thousands of years and their vast in the near future and the major

centuries out of which the dim view of our geographical range. The culture of ethical concerns this could entail,

evolutionary cousin arose, or on more recent groups separated by space or time arguing that the recent production

paleoanthropological, archaeological, and ge- would likely have seemed just as of Neanderthal brain organoids

netic evidence suggesting that they interbred foreign (had they met) as it does (1), together with the unsanctioned

PHOTO: WILL OLIVER - PA IMAGES/CONTRIBUTOR/GETTY IMAGES with our ancestors and displayed a range of when we encounter unfamiliar cul- gene editing of human babies (2),

sophisticated behaviors. In her new book, tures today, argues Wragg Sykes. makes Neanderthal de-extinction

Kindred, Rebecca Wragg Sykes nevertheless “Those living in Wales would have Kindred not as far-fetched a notion as it may
brings something new to this discussion. been surprised—even turned their Rebecca Wragg Sykes initially seem. Without forcing the
noses up—at what others of their Bloomsbury Sigma, point, Kindred closes by returning
The book’s scope is impressive, spanning own kind from Palestine consumed to the value of empathy and com-
from the initial discoveries and interpreta- 2020. 400 pp.

tions of Neanderthals to the diverse aspects with relish,” she suggests, for example, passion, arguing that both deserve a more

of their biology and behavior, including about the population’s varied food cultures prominent place in our theories about Nean-

their childhoods, lifestyles, technologies, and preferences. derthals and in our attitudes toward our fel-

art, and approaches to death. All of these Wragg Sykes evaluates the available evi- low humans and other sentient creatures. j

individual components are beautifully de- dence on Neanderthals with empathy and REFERENCES AND NOTES
tailed, combining overviews of state-of-the- even-handedness, revealing the group to 1. J. Cohen, Science 360, 1284 (2018).
be less “them” and more “us.” She rejects 2. D. Normile, Science aba7347 (2019).
The reviewer is at the Department of Archaeology, University of aggression-centered narratives that have
Cambridge, Cambridge CB2 3DZ, UK. Email: [email protected] previously shaped our interpretations of 10.1126/science.abe5143

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INSIGHTS | BOOKS

MARINE CONSERVATION

A profound plan to save the seas

Rejecting piecemeal strategies, a conservationist encourages total ocean protection

By Mary Ellen Hannibal perts. “It’s a familiar and tedious tale,” she Sea—is an existing treaty signed by 180 coun-

A long-time marine conservation ad- writes, “authorities giving way to the short- tries (the United States is notably absent),
vocate, Deborah Rowan Wright has
spent decades supporting piecemeal term economic demands of the fishing in- which covers most of the bases necessary to
strategies to protect the oceans. Yet
despite her efforts and those of many dustry rather than ensuring the long-term mitigate damage to the ocean, from catch-size
others, our ocean life-support system
continues to buckle under human pressures. viability of wild fish populations.” limits to guidelines for minimizing pollution.
We have been approaching marine conserva-
tion backward, she argues at the outset of Oceans are vulnerable to what Garrett The problem, argues Rowan Wright, is lax
her new book, Future Sea. Instead of regulat-
ing individual fisheries or putting boundar- Hardin memorably called “the tragedy of the enforcement and apathy. Sovereignties are
ies around select areas of the ocean, we need
to protect the whole thing. commons,” wherein individuals fail to act in inconsistent and self-serving when it comes

The ocean waters that make Earth habit- accordance with the common good and col- to upholding the rules to which they have
able for humans are becoming increasingly
polluted with plastics and chemicals; they lectively exploit a shared resource (3). This is agreed, and we have not put pressure on our
are acidifying and warming. They are also
losing species at a rate that could drive many particularly true of the high seas, where both governments to do better. “Most of us simply
to extinction. The profound interconnectivity
of ocean organisms means that negative im- the lack of sovereign jurisdiction don’t see the connection between
pacts are amplified throughout the food web.
But, according to Rowan Wright, the biggest and technological advances have healthy oceans and a better future
problem many ocean denizens face is a short-
age of food. Humanity is eating it all. In 2018, allowed humanity to penetrate the (in fact, any future)” she writes.
the Food and Agriculture Organization of the
United Nations reported 4.6 million fishing ocean’s farthest reaches, leading to Last month, the sun did not
vessels in operation, harvesting two-thirds of
commercial stocks to capacity and the final the decimation of harvests even in rise in San Francisco. Or at least
third in biologically unsustainable numbers.
the most remote waters. that is what it felt like, as smoke
Science has long shown the negative im-
pacts of lower-trophic-level overharvests on Rowan Wright’s solution to from fires around the West blot-
the rest of the food web (1). In Antarctica,
we harvest krill—small planktonic crusta- the current plight of the seas is ted out the light. Amid the help-
ceans near the bottom of the food chain—
for use in health supplements and fish-farm to reinvigorate existing interna- lessness and panic, I kept think-
feed. Krill are eaten by a wide panoply of
seabirds, by invertebrates such as squid, tional laws according to econo- Future Sea: How to ing: if only. If only we could go
and by fish. They are also an important part mist Elinor Ostrom’s principles Rescue and Protect the back 20 years and listen to the
of the whale diet. Take out the krill, and for good commons governance. natural resource managers, scien-
many other species go hungry; eventually, These include a “common-pur- World’s Oceans tists, and Indigenous peoples who
the ecosystem will collapse. pose, cross-sector, tiered (but non- predicted this exact scenario and
hierarchical) system…rooted in Deborah Rowan Wright offered strategies to mitigate such
Removal of top predators likewise has University of Chicago
negative impacts on the process, function, Press, 2020. 200 pp.
and resilience of the ecosystem (2). Humans
like to eat bluefin tuna, for example, which the ecosystem-based and precautionary ap- a tragedy. We know the disaster that awaits
have been hunted nearly to extinction.
proaches and coordinated by a central agency.” us when the ocean reaches its tipping point.
As Rowan Wright probes catch limits pu-
tatively designed to prevent collapse of the As she sets out to aggregate the various trea- Will this ecosystem meet the same fate? j
fishery, she finds that, often, these limits are
set well above those recommended by ex- ties and agreements that address human im- REFERENCES AND NOTES
pacts on the ocean, Rowan Wright is surprised
The reviewer is the author of Citizen Scientist: Searching to learn that “virtually all the seas and oceans 1. A. D. M. Smith et al., Science 333, 1147 (2011).
for Heroes and Hope in an Age of Extinction (The Experiment, in the whole world are already protected by 2. J.A. Estes et al., Science 333, 301 (2011).
2016). Email: [email protected] international law.” The comprehensive United 3. G. Hardin, Science 162, 1243 (1968).

Nations effort—called, simply, the Law of the 10.1126/science.abe0339

Sourdough offers a lesson in microbial fermentation. PODCAST PHOTO: ISTOCK.COM/LEONORI

Science and Cooking:
Physics Meets Food, From
Homemade to Haute Cuisine
Michael Brenner, Pia Sörensen,
David Weitz
Norton, 2020. 320 pp.

From melting temperature to
phase transformation, cooking
holds great pedagogical potential
for communicating scientific prin-
ciples. This week on the Science
podcast, Pia Sörensen reveals how
experiments in the kitchen can
serve as an easy entry point for
understanding a range of physical
and chemical concepts.
http://scim.ag/2Hko12K

10.1126/science.abf0517

538 30 OCTOBER 2020 • VOL 370 ISSUE 6516 sciencemag.org SCIENCE

Published by AAAS

LETTERS

The mink industry is associated with human disease, animal cruelty, and environmental pollution.

PHOTO: MADS CLAUS RASMUSSEN/RITZAU SCANPIX/AFP/GETTY IMAGES Edited by Jennifer Sills the SARS-CoV-2 genome and mutations 4. F. Ramírez-Pizarro et al.,Vector Borne Zoonotic Dis. 19,
suggests that the virus might be able to 908 (2019).
Ban unsustainable mink spread from minks to humans (9).
production 5. E. Cahan, Science 10.1126/science.abe3870 (2020).
The mink industry is problematic 6. S. Mallapaty, Nature 10.1038/d41586-020-01574-4
More than 50 million minks are produced beyond its potential to spread disease.
annually—primarily in China, Denmark, Animal welfare practices fall short, with (2020).
the Netherlands, and Poland (1)—to minks showing signs of fearfulness, 7. “Coronavirus: Denmark culls 2.5 million mink amid
sustain the demand from the interna- self-mutilation, infanticide, and breeding
tional fur industry (2, 3). In June, the difficulties (10). Mink production also outbreak on dozens of fur farms,”Independent (2020).
Netherlands adopted a proposal to ban leads to high N O emissions, eutrophica- 8. J. Dalton,“Coronavirus fears as China plans to protect
mink farming by the end of 2020 instead
of phasing out the industry through 2024 2 vast mink and fox fur industry from backlash at wildlife
(1). The Netherlands’ decision was a step trade,”Independent (2020).
toward better protections for humans, tion, and water consumption (11); the 9. B. B. O. Munnink et al., bioaRxiv
animals, and the environment. China, climate footprint of producing 1 kg of 10.1101/2020.09.01.277152 (2020).
Denmark, and Poland should support and mink fur is 5 times as high as the foot- 10. R. Bale,“Fur farms still unfashionably cruel, critics say,”
extend the immediate and complete ban print of producing 1 kg of wool (11). National Geographic (2016).
of mink production. 11. CE Delft,“The environmental impact of mink fur produc-
The unsustainable use of natural tion” (2011).
Minks harbor zoonotic infectious resources by the mink industry impedes our 12. J.Tollefson, Nature 584, 175 (2020).
diseases such as leptospirosis, which response and recovery from the pandemic,
leads to kidney failure in humans (4), and puts animals in harmful conditions, and 10.1126/science.abf0461
coronavirus disease 2019 (COVID-19), the jeopardizes our ability to achieve the United
illness caused by severe acute respiratory Nations’ Sustainable Development Goals Support U.S. research
syndrome coronavirus 2 (SARS-CoV-2). (12). It is urgent to monitor, restrict, and—
COVID-19 has been found in minks in where possible—ban mink production. during COVID-19
the Netherlands, Denmark, Spain, and
the United States (5, 6). In October, the Changlei Xia1, Su Shiung Lam2,1, Christian Sonne3,1* Colleges and universities are critical com-
spread of COVID-19 in Danish mink 1Nanjing Forestry University, Nanjing, China. ponents of the U.S. innovation ecosystem.
farms spun out of control, threatening 2Universiti Malaysia Terengganu, Terengganu, These institutions are called upon to play
the country’s disease control and public Malaysia. 3Aarhus University, Roskilde, Denmark. ever-evolving roles in building talent for a
health and resulting in the culling of *Corresponding author. Email: [email protected] changing workforce; achieving scientific
millions of minks (7). Similar cases are breakthroughs; creating new technologies,
likely in China, which harbors a multispe- REFERENCES AND NOTES products, and companies; and contribut-
cies fur industry (8). A recent study of ing to local economic development. Yet,
1. Party for the Animals,“The end of the Dutch mink farm- as the pace of change accelerates across
SCIENCE sciencemag.org ing industry—one of the largest in the world”(2020); our economy, federal and state budget
www.partyfortheanimals.com/the-end-of-the-dutch- constraints have made meeting these expec-
mink-farming-industry-one-of-the-largest-in-the-world. tations increasingly challenging. The federal
commitment to research and development
2. Kopenhagen Fur,“World production of mink drops” stands at a multidecadal low as a percent-
(2016); www.kopenhagenfur.com/en/news/2016/ age of GDP (1). Now, the coronavirus disease
june/world-production-of-mink-drops/.

3. Danish Agriculture and Food Council,“Mink
and Fur”(2020); https://agricultureandfood.dk/
danish-agriculture-and-food/mink-and-fur.

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INSIGHTS | LETTERS

2019 (COVID-19) pandemic has disrupted Columbia University, New York, NY 10027, USA. their habitat of tropical and seasonal rain-
11President, Boston University, Boston, MA 02215, forests suffered from overexploitation and
almost all aspects of higher education, USA. 12President, American University, Washington, deforestation (2, 4), the peacock-pheasant
DC 20016, USA. 13Director, Emory Biomedical population declined from about 2700 in
including the ability to keep laboratories Catalyst, Emory University, Atlanta, GA 30322, 1990 (4) to only about 300 individuals in
USA. 14President, Clemson University, Clemson, SC 2000 (3). With such small numbers, Hainan
open, conduct research in a timely manner, 29634, USA. 15President, University of South Florida, peacock-pheasants could lose their ability to
Tampa, FL 33620, USA. 16President, Georgetown maintain a self-sustaining population (5).
collect and process data, and collaborate University, Washington, DC 20057, USA. 17President,
University of Miami, Miami, FL, 33123, USA. The Hainan peacock-pheasant has
with colleagues and students. 18President, University of Florida, Gainesville, FL been categorized as Endangered on the
32611, USA. 19President, University of Minnesota, International Union for Conservation of
As colleges and universities across the Minneapolis, MN 55455, USA. 20Chancellor, Nature (IUCN) Red List since 2016 (6)
University of Pittsburgh, Pittsburgh, PA 15213, USA. and is classified as Category I in China’s
nation make difficult decisions to advance 21President, West Virginia University, Morgantown, list of nationally protected animals (3).
WV 26506, USA. 22President, Carnegie Institute for Despite this recognition, current con-
their vital missions this fall, the $55 Science, Washington, DC 20005, USA. 23Former servation efforts are insufficient (7). The
President, University of Toledo, Toledo, OH 43606, Chinese government should continue
billion in federal support for university- USA. 24President, Carnegie Mellon University, to strengthen the protection of moun-
Pittsburgh, PA 15213, USA. 25President, University tain rainforest vegetation and prohibit
performed R&D (i.e., on-campus research) of Notre Dame, Notre Dame, IN 56446, USA. recreational hunting, especially at the
26President, The Ohio State University, Columbus, altitudes the peacock-pheasants inhabit
is at risk (2). Maintaining the strength of OH 43210, USA. 27Executive Director, College [up to about 1500 meters (8)]. Fortunately,
Promise Campaign, Washington, DC 20009, USA. Hainan Tropical Rainforest National Park,
the U.S. research enterprise—the same 28Laboratory Director, Argonne National Laboratory, now under construction, could provide
Lemont, IL 60439, USA. 29President, University of the peacock-pheasant with a more stable
research enterprise that has enabled the Colorado, Boulder, CO 80309, USA. 30Chancellor, habitat (9, 10). If the peacock-pheasant’s
University of California, San Diego, La Jolla, CA original habitat can no longer meet the
rapid sequencing of the COVID-19 genome 92093, USA. 31President, Worcester Polytechnic needs of survival and reproduction, rescue
Institute, Worcester, MA 01609, USA. 32President, measures should be taken, including
and launched numerous treatment and Marquette University, Milwaukee, WI 53233, USA. breeding bases, gene banks, germplasm
33Chancellor, University of California, Davis, Davis, resource banks, and relocation to pro-
vaccine studies—must be a national prior- CA 95616, USA. 34President, University of Georgia, tected areas where they are more likely
Athens, GA 30602, USA. 35President, Kansas State to thrive.
ity. Laboratories must remain open, and University, Manhattan, KS 66506, USA. 36President
Emeritus, The University of Akron, Akron, OH Song Guan1,2*, Hanlin Zhou1,2, Yanfu He3
researchers must be allowed to continue 44325, USA. 37President, Bowdoin College, 1Tropical Crops Genetic Resources Institute,
Brunswick, ME 04011, USA. 38President, University Chinese Academy of Tropical Agricultural
data collection and analysis, with all the of Memphis, Memphis, TN 38152, USA. 39President, Sciences, Haikou 571101, China. 2Institute of
Virginia Polytechnic Institute and State University, Zoology, Chinese Academy of Tropical Agricultural
necessary health protocols in place. Blacksburg, VA 24061, USA. 40President, University Sciences, Haikou 571101, China. 3College of Food
of Michigan, Ann Arbor, MI 48109, USA. 41President, Science and Engineering, Hainan University,
We cannot afford to shut down critical Academy of Art University, San Francisco, CA Haikou 570228, China.
94105, USA. 42Chancellor, Webster University, St. *Corresponding author.
projects with long-term national benefits Louis, MO 63119, USA. 43Chancellor, University of Email: [email protected]
Massachusetts, Amherst, Amherst, MA 01003, USA.
or to postpone projects that provide the 44President, University at Buffalo, Buffalo, NY 14260, REFERENCES AND NOTES
USA. 45President, University of Utah, Salt Lake City,
hands-on graduate and undergraduate UT 84112, USA. 46President, Denison University, 1. G. M. Zheng, A Checklist on the Classification
Granville, OH 43023, USA. 47Chancellor, University and Distribution of the Birds of China (Science Press,
student research experiences necessary of California, Riverside, Riverside, CA 92521, USA. Beijing, 2005).
48President & CEO, Council on Competitiveness,
to train the next generation of scientists Washington, DC 20006, USA. 49President, Iowa 2. J. Chang et al., Zool. Sci. 25, 30 (2008).
State University, Ames, IA 50011, USA. 50Chancellor, 3. G. M. Zheng, Q. S. Wang, China Red Data Book of
and engineers. In these difficult times, North Carolina State University, Raleigh, NC
27607, USA. 51President, The University of Chicago, Endangered Animals (Aves) (Science Press, Beijing,
we call upon the federal government to Chicago, IL 60637, USA. 1998).
*Corresponding author. 4. Y. R. Gao, D. Q. Yu, Chin. J. Zool. 25, 42 (1990).
provide the leadership, critical funding, Email: [email protected] 5. J. Chang et al., Chin. Sci. Bull. 58, 2185 (2013).
All authors are members of the Council 6. BirdLife International, Polyplectron katsumatae (IUCN
and programmatic flexibility necessary to on Competitiveness. Red List of Threatened Species, 2016).
7. W. Liang, Z. W. Zhang, Chin. Birds 2, 116 (2011).
enable the nation’s colleges and universi- REFERENCES AND NOTES 8. xzwyu.com,“Hainan peacock-pheasant” (2015);
www.xzwyu.com/article-19556-1.html [in Chinese].
ties to continue the U.S. commitment to 1. AAAS,“Federal R&D as a Percent of GDP” (2020); 9. State Forestry and Grassland Administration, National
www.aaas.org/sites/default/files/2020-07/RDGDP.png. Park Administration,“Protect this precious virgin
research, exploration, and new knowledge tropical rainforest,” Guang-ming Daily (2020);
2. AAAS,“R&D at colleges and universities”(2018); www.forestry.gov.cn/main/6004/20201014/085431
creation that will power our economy and www.aaas.org/programs/r-d-budget-and-policy/ 339375989.html.
rd-colleges-and-universities. 10. Hainan Provincial People’s Congress Standing
provide opportunity for all. Committee,“Hainan Tropical Rainforest National Park
10.1126/science.abf1225 regulations (trial)” (2020); http://lyj.hainan.gov.cn/
Michael M. Crow1,2, Jonathan Alger3, Michael xxgk/0200/0202/202009/t20200906_2845900.
Amiridis4, Dennis Assanis5, Eric Barron6, Mark P. Hainan peacock-pheasant html [in Chinese].
Becker7, Rebecca M. Blank8, Gene D. Block9, Lee C.
Bollinger10, Robert A. Brown11, Sylvia M. Burwell12, needs focused protection 10.1126/science.abf0489
C. Michael Cassidy13, James P. Clements14, Steven
Currall15, John J. DeGioia16, Julio Frenk17, W. Kent The Hainan peacock-pheasant (Polyplectron
Fuchs18, Joan T. A. Gabel19, Patrick D. Gallagher20,
E. Gordon Gee21, Eric Isaacs22, Lloyd A. Jacobs23, katsumatae), a distinct species endemic to
Farnam Jahanian24, John Jenkins Sr.25, Kristina
Johnson26, Martha Kanter27, Paul K. Kearns28, Mark Hainan island (1, 2), requires protection.
Kennedy29, Pradeep K. Khosla30, Laurie Leshin31,
Michael Lovell32, Gary S. May33, Jere Morehead34, Since the 1950s (3), the Hainan peacock-
Richard B. Myers35, Luis M. Proenza36, Clayton
Rose37, M. David Rudd38, Timothy D. Sands39, Mark pheasant population has dispersed into
S. Schlissel40, Elisa Stephens41, Elizabeth Stroble42,
Kumble Subbaswamy43, Satish Tripathi44, Ruth small, partially isolated subpopulations. As
Watkins45, Adam Weinberg46, Kim Wilcox47, Deborah
Wince-Smith48*, Wendy Wintersteen49, W. Randolph
Woodson50, Robert J. Zimmer51
1University Vice-Chair, Council on Competitiveness,
Washington, DC 20006, USA. 2President, Arizona
State University, Tempe, AZ 85281, USA. 3President,
James Madison University, Harrisonburg, VA 22807,
USA. 4Chancellor, University of Illinois at Chicago,
Chicago, IL 60607, USA. 5President, University
of Delaware, Newark, DE 19716, USA. 6President,
Pennsylvania State University, University Park, PA
16802, USA. 7President, Georgia State University,
Atlanta, GA 30302, USA. 8Chancellor, University
of Wisconsin–Madison, Madison, WI 53706,
USA. 9Chancellor, University of California, Los
Angeles, Los Angeles, CA 90095, USA. 10President,

540 30 OCTOBER 2020 • VOL 370 ISSUE 6516 sciencemag.org SCIENCE

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AAAS NEWS & NOTES

The diverse 2019–2020 Science & Technology Policy Fellows “look like America,” said AAAS CEO Sudip Parikh.

AAAS drafts plan to address systemic racism in sciences

Diversity assessment within the organization’s programs among plan’s first steps

PHOTO: AAAS S&T POLICY FELLOWSHIPS By Becky Ham the difference, Parikh said, noting that the data offer a glimpse at
how “baked-in” policies often can exclude minorities in science.
The American Association for the Advancement of Science has
released two parts of a draft plan that directs the organization to “Those policies, they do their work even if the people who are carry-
strengthen its advocacy on behalf of diversity, equity, and inclusion— ing them out have no racist tendencies, and it’s the system itself that
while taking a hard look at its own demographics and related policies. actually causes the problem,” he said.

AAAS’s “Addressing Systemic Racism in the Sciences” plans were To bring these policies to light, AAAS will undergo the SEA Change
developed by AAAS CEO Sudip Parikh and AAAS leadership, after self-assessment, said Shirley Malcom, AAAS senior adviser and the
discussions inside and outside the association prompted by a year program’s director. SEA Change provides support to universities and
that Parikh calls “an opportunity born of tragedy.” colleges as they transform campus cultures, policies, and procedures
that disadvantage or exclude participation in science, technology,
Protests over police brutality against Black people in the United engineering, mathematics, and medicine.
States and the disproportionate impact of COVID-19 on Black and
brown communities are sharp reminders that no part of society is im- Malcom and her colleagues are seeking support to modify and
mune from discrimination, Parikh said. “We haven’t yet held a mirror to adapt SEA Change for educational and professional organizations,
the scientific enterprise, and we may not like everything we see.” she said. “Some of the societies we work with in SEA Change—disci-
plinary groups and professional societies—have said, ‘we don’t think
AAAS is holding up that mirror with a report that will be published in we can subject our community to something we’re not willing to
late October, compiling demographic data on the association’s Fellows, undergo ourselves.’”
Science & Technology Policy Fellows, award recipients, Science authors,
and AAAS governing bodies. These groups are critical to supporting SEA Change will move the AAAS demographic reports “beyond the
diversity, Parikh said, because they represent the ways in which “AAAS numbers to how did we get to those numbers,” Malcom said. “What
functions as a career advancement enabler in science and engineering.” are our processes in place that would support either diversifying those
numbers or may be a barrier to diversifying those numbers?”
The report by Jen Sargent and Marietta Damond in the Office of
Membership provides a baseline accounting of diversity in terms “This requires a certain amount of reflection,” she added. “We’re
of race, ethnicity, and gender. Because most of the data are self- not going to move forward unless we’re honest about what we find
reported by individuals, there are gaps in coverage, said Damond. For and what it requires us to do.”
instance, the Science family of journals authors and reviewers had
the smallest amount of available data, with gender data available for The second part of the draft plan, released in September, dis-
13% of the group (before using a statistical estimate that brought cusses how AAAS programs and initiatives can help increase diver-
coverage up to 53%) and race and ethnicity data available for only sity and equity throughout the scientific enterprise. Under the plan,
12% of the group. AAAS will advocate for increased salaries for graduate students and
postdoctoral researchers, mentor training, and funding for govern-
Although the data are “messy,” Parikh acknowledged, there are still ment and industry science programs for minority students.
some notable trends that shed light on how AAAS’s practices may
encourage or discourage diversity. For instance, “the S&T Policy Fellows The need for a financial safety net for young scientists has grown
look like America. It’s extremely diverse, it’s got great gender parity, has with COVID-19. The pandemic is having a disproportionate effect on
good geographic diversity,” he said. “For the honorary Fellows, the East women and people of color in the sciences, who are most likely to
and West Coasts and white males are overrepresented.” bear the brunt of a collision between career advancement and family
and health responsibilities, said Malcom.
S&T Policy Fellows apply for the fellowship program, while honor-
ary Fellows are nominated by colleagues, which could account for At the same time, more scientists are speaking bluntly and publicly
about the impacts of racism in their fields. “We have not had that in
the past, and so I live in hope that we are at a different place,” she said.

SCIENCE sciencemag.org 30 OCTOBER 2020 • VOL 370 ISSUE 6516 541

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Where AAAS NEWS & NOTES
Science
Encouraging diversity is more than a moral issue, Parikh said.
Gets Countries like China and India draw on “huge human capital” for their
Social. scientific enterprises, and it makes competitive sense that the United
States should expand its own pool of talent, he noted. “If we’re only
AAAS.ORG/COMMUNITY pulling from the East and West Coasts, and we’re only pulling from
communities that can afford to go into the sciences, then we are fight-
ing with one hand tied behind our back in that global competition.”

The third part of the AAAS plan, which looks at diversity within the
AAAS staff, will be shared in late 2020. For the AAAS leadership, the
most important part of the plans is to keep them moving forward
beyond the draft stage.

Parikh recalled that AAAS had a similar moment of opportunity in
the late 1960s and early 1970s, when students and younger scientists
protested at the association’s Annual Meetings for more inclusive
policies. After the 1969 meeting, a Committee on Young Scientists was
formed. Students began to attend Board meetings, and AAAS devel-
oped its first signature programs in education and advocacy.

But the committee disbanded within a few years, leaving many of
the diversity issues it raised unaddressed, said Parikh. “My takeaway
from that is that you have to keep up momentum, you can’t stop
talking about the issues at hand.”

AAAS annual election: Preliminary announcement

The 2020 AAAS election of general and section ofcers is scheduled
to begin later this fall. All members will receive a ballot for election
of the president-elect, members of the Board of Directors, and
members of the Committee on Nominations. Additionally, members
registered in sections (up to three) will receive ballots for the speci-
fed section elections. Biographical information for the candidates
will be provided along with ballots. The general election slate is listed
below. The list of section candidates is still being compiled.

AAAS’ Member Community is a Notice to our General Election Slate
one-stop destination for scientists international members:
In an efort to conserve PRESIDENT-ELECT
and STEM enthusiasts alike. It’s resources, AAAS will be sending Gilda Barabino, Ph.D., President,
“Where Science Gets Social”: a electronic election ballots to our Olin College of Engineering
community where facts matter, non–U.S.-based members. To
ideas are big and there’s always a ensure you receive your ballot, David Ho, M.D., Director, Aaron
reason to come hang out, share, please make sure your email is Diamond AIDS Research Center,
up-to-date with AAAS by logging Clyde ’56 and Helen Wu Professor
discuss and explore. on to www.aaas.org. 1) Click on of Medicine, Columbia University
“Member Login” (if you have not
yet created an account, you will DIRECTOR
be prompted to do so); 2) After R. Alta Charo, J.D., Warren P. Knowles
you log in, click on the red “My Professor of Law and Bioethics,
Profle” button in the upper right- University of Wisconsin-Madison
hand corner of the page; 3) Click
on “Edit My Contact Information” Janine Clayton, M.D., Associate
in the left-hand side bar; Director for Research on Women’s
4) Update your email and click Health and Director of the Ofce
on the “Save” button. of Research on Women’s Health,
National Institutes of Health
If you would like to request a
special paper ballot, please send Kaye Husbands Fealing, Ph.D.,
an email with your name and Dean and Ivan Allen Jr. Chair, Ivan Allen
address with your request to College of Liberal Arts, Georgia Tech
[email protected].
Nora Newcombe, Ph.D., Laura H.
Carnell Professor of Psychology,
Temple University

sciencemag.org SCIENCE

Published by AAAS

RESEARCH national policies were forged in
response. Now that many thou-
IN SCIENCE JOURNALS sands of virus sequences are
available, two studies analyzed
Edited by Michael Funk some of the key early events
in the spread of SARS-CoV-2.
Transmission electron Bedford et al. found that the
microscopy image of a white virus arrived in Washington state
in late January or early February.
blood cell infected with The viral genome from the first
the parasite Trypanosoma case detected had mutations
cruzi, which causes Chagas disease similar to those found in Chinese
samples and rapidly spread and
CHAGAS DISEASE dominated subsequent unde-
tected community transmission.
Trouncing trypanosomes The other viruses detected had
origins in Europe. Worobey et
T rypanosoma cruzi infection causes Chagas disease in millions of individuals in Latin America, and al. found that early introduc-
intensive drug treatment is frequently unsuccessful. Bustamante et al. demonstrated that high tions into Germany and the
weekly doses of oral benznidazole over 30 weeks, rather than the current treatment of smaller west coast of the United States
twice-daily doses over 2 months, resulted in better clearance of both actively replicating and dor- were extinguished by vigorous
mant trypanosomes in mouse models of Chagas disease. The clearance of dormant parasites was public health efforts, but these
confirmed by light sheet fluorescence microscopy, which allowed the authors to image whole organs and successes were largely unrec-
intact tissues of infected mice. Further studies will determine whether this drug regimen will be successful ognized. Unfortunately, several
in treating patients with Chagas disease. —MN Sci. Transl. Med. 12, eabb7656 (2020). major travel events occurred
in February, including repa-
IMAGE: DAVID M. PHILLIPS/SCIENCE SOURCE GEOPHYSICS that moved in the opposite direc- CORONAVIRUS triations from China, with lax
tion. These regions moved in this public health follow-up. Serial,
Mapping out direction because of inelastic A series of independent introductions trig-
backward motion deformation, which helped to unfortunate events gered the major outbreaks in the
accommodate the overall fault United States and Europe that
Most deformation associated with rupture for the sequence. The The history of how severe acute still hold us in the grip of control
an earthquake is, not surprisingly, observations were possible respiratory syndrome corona- measures. —CA
in the same direction as the fault because of improved radar imag- virus 2 (SARS-CoV-2) spread
rupture. Xu et al. used satellite ing and are likely more common around the planet has been far Science, this issue p. 571, p. 564
imaging to find areas of deforma- than previously believed. —BG from clear. Several narratives
tion associated with the 2019 have been propagated by social PLANT SCIENCE
Ridgecrest earthquake sequence Science, this issue p. 605 media and, in some cases,
Hormone-guided
self-organization

Auxin signals travel through
pathways in developing or
regenerating plant tissues to
guide tissue formation. Hajný
et al. now show that an auxin-
regulated receptor in turn
regulates phosphorylation and
thus subcellular localization of an
auxin transporter. Through this
signaling pathway, auxin builds
the pathways through which it
is transported, guiding develop-
ment as it goes. —PJH

Science, this issue p. 550

MAGNETISM

Lightening the load

Permanent magnets are generally
produced from solid metals or
alloys. Less dense compositions
involving lighter elements tend
to demagnetize well below room
temperature or under modest

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applied external fields. Perlepe to explore exotic topological IN OTHER JOURNALS
et al. now report that chemical phenomena and new phases of
reduction of a low-density chro- quantum matter. —ISO Edited by Caroline Ash
mium-pyrazine network produces and Jesse Smith
a magnet that remains stable Science, this issue p. 600
above 200°C and resists demag- NEURODEVELOPMENT INFLUENZA VIRUS CREDITS: LIU ET AL.; JANROZ/ALAMY STOCK PHOTO
netization with 7500-oersted PANDEMIC PAUSE
coercivity at room temperature. Finding the way through Influenza A virus
The straightforward synthetic Songbirds reclaim a complicated world matrix protein
route to the material shows favored frequencies
promise for broad exploration of As the nervous system devel- Influenza spreads in seasonal
potential applications. —JSY When severe acute respiratory ops, axons grow out from outbreaks that result in hun-
syndrome coronavirus 2 (SARS- immature neurons to build dreds of thousands of deaths
Science, this issue p. 587 CoV-2) pandemic lockdowns connections. The fruit fly, worldwide. The culprit, influenza
were instituted across entire Drosophila melanogaster, is A virus, has occasionally caused
TOPOLOGICAL SYSTEMS countries, human activities used as a model organism for historic pandemics such as
ceased in an unprecedented tracking the development of the 1918 flu pandemic, which
Polaritons with a twist way. Derryberry et al. found the nervous system in bilater- killed tens of millions of people
that the reduction in traffic ally symmetrical animals. In the in 2 years. Despite more than a
The ability to design and sound in the San Francisco Drosophila midline, some axons century of study, we still do not
fabricate optical systems with Bay Area of California to levels will stay on their originating side have a clear picture of many
tunable topological features not seen for half a century led and others will cross the mid- components of the virus, includ-
makes them especially attrac- to a shift in song frequency in line. The secreted protein Slit ing the matrix protein M1, which
tive for developing analogs of white-crowned sparrows (see prevents axons from crossing is one of its most abundant
topological condensed matter the Perspective by Halfwerk). over. Things get complicated, proteins. Selzer et al. provide a
systems, which by themselves This shift was especially however, as Kellermeyer et al. high-resolution structure of M1
tend to be fixed or limited in notable because the frequency reveal with their identification in a single-layered assembly
their tunability. Liu et al. now of human-produced traffic of the protease Tolkin, which using cryo–electron microscopy.
show that the combination of a noise occurs within a range cleaves Slit into fragments. The study offers new insight into
two-dimensional material with a that interferes with the highest Although full-length Slit prohib- the role of the matrix protein in
photonic crystal can be used to performance and most effective its growing axons from crossing maintaining the integrity of the
develop an analogous quantum song. Thus, our “quiet” allowed the midline, the amino-terminal influenza virus and may help
spin Hall system. The strong the birds to quickly fill the most fragment of Slit, which is also in the development of new antivi-
coupling between the monolayer effective song space. —SNV generated by Tolkin, induces rals targeting the matrix layer of
tungsten disulfide excitons with the growing axons to elongate. the virus. —DJ
a nontrivial hexagonal photonic Science, this issue p. 575; Thus, little is left to chance in
crystal gives rise to helical topo- see also p. 523 building the Drosophila nervous PLOS Biol. 18, e3000827 (2020).
logical polaritons observed at system: A negative signal on
up to 200 kelvin. The topological ANTHROPOLOGY one route is itself the root of a GENOMICS
polaritons can be actively tuned positive signal for another route.
by temperature and may further Temporal changes in —PJH Decoding the great ape Y
be manipulated with electric or body temperature
magnetic fields, thereby provid- Development 10.1242/dev.196055 The Y chromosome confers
ing a flexible platform with which For people living in the United maleness in most mammals and
States, normal body tempera- (2020). in other species, including flies
Calculated band structure of a ture (BT) has decreased from
topological polaritonic lattice with 37.0° to 36.4°C over the past 150
odd (brown) or even (blue) spatial years, a decline attributed to the
parity of the bands reduced incidence of infectious
diseases and to improvements
in socioeconomic conditions.
To understand whether this
phenomenon is found in a very
different context, Gurven et al.
analyzed BT data from a group
of indigenous farmers in rural
Bolivia over a 16-year period.
They determined that BT
decreased by 0.5°C in less than
two decades. Better access
to health care contributed to
improved health status but does
not explain the rapid rate of BT
decline. —MSA

Sci. Adv. 10.1126/sciadv.abc6599
(2020).

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Published by AAAS

PESTICIDES temperatures on land can including the backward design
experience complex additional of lessons and courses,
No easy fix season-like variations. The competency assessment
authors conclude that circum- development, and curriculum
E vidence has mounted over the years that neonicotinoid binary exoplanets can remain mapping and planning. —MMc
insecticides used for crop protection have dangerous habitable if they have Earth-like
sublethal effects. Continued used of the chemicals has oceans. —KTS CBE Life Sci. Educ. 10.1187/
led to beneficial insect decline, and many governments cbe.19-11-0259 (2020).
have taken action to ban their use. However, bans have J. Geophys. Res. Planets
not come with systemic changes in agricultural practices, but 10.1029/2020JE006576 (2020). B I O M AT E R I A L S
rather they have prompted replacement by different types of
pesticides, including flupyradifurone and sulfoxaflor. Across E D U C AT I O N It’s all in the inks
published studies, Siviter and Muth found that these com-
pounds have similar modes of action as neonicotinoids Competencies get their For any printing process, the
and similar sublethal impacts on beneficial insects. The chance to shine quality and properties of the
authors argue that sublethal effects should be measured not final product depend on the
just for pollinators but also for non-bee beneficial insects, Transferrable skills, or compe- availability of suitable inks. In
and wider environmental interactions for any proposed tencies, are a critical part of an bioprinting for tissue engineer-
pesticides must be assessed during the approval processes. undergraduate degree in STEM ing, inks need to have the right
—SNV Proc. Biol. Sci. 10.1098/rspb.2020.1265 (2020). (science, technology, engineer- combination of printability as
ing, and mathematics) but well as biological compatibility
Beneficial insects, such as beetle predators of aphids (Coccinella are often an underdeveloped and suitable mechanical prop-
septempunctata is shown here), succumb to the sublethal effects of a facet of curricula. A possible erties for the printed parts. Lee
new generation of pesticides designed to replace banned neonicotinoids. remedy for this would be the et al. developed an extracel-
transformation of a compe- lular matrix–based polymer
and some plants. Studies of this variations in stellar heating over tency framework into a set of through the combination of
chromosome and its evolutionary less than the planet’s orbital measurable learning outcomes. gelatin methacryloyl- and
history can inform upon evolu- period. Wolf et al. performed Using an iterative process, methacryloyl-substituted
tionary lineages and the genes three-dimensional simulations Clemmons et al. did just this recombinant human tropelas-
involved in male fertility. However, of how Earth’s climate would by transforming and validating tin. In addition to providing
the Y chromosome has been differ if it orbited in the habit- the core competencies from elasticity and resilience, tro-
difficult to sequence; because of able zone around a Sun-like star the Vision and Change frame- poelastin provides cell-binding
its high content of repetitive DNA with a smaller stellar compan- work into the BioSkills Guide. motifs and cell-signaling
and low gene number, it is often ion. Even in extreme cases, Compared with other science pathways. Printed vascular-
absent from genomic assemblies. they found that Earth’s oceans competency frameworks, ized tissue constructs were
Cechova et al. generated draft provided enough thermal inertia the BioSkills Guide revealed tested in vitro and in vivo and
sequences of the bonobo and and negative feedback through some gaps and ambiguities, presented endothelium barrier
orangutan Y chromosomes and cloud formation to buffer the likely reflecting areas where function and spontaneous
compared them with previously planet against catastrophic still-evolving competencies in beating of cardiac cells, as
sequenced human, gorilla, and climate variations. However, undergraduate biology merit well as minimal inflammatory
chimpanzee Y chromosomes. By future research. The BioSkills response and in vivo degrada-
comparing the Y chromosomes Guide has potential for a tion. —MSL
of all great ape species, this wide variety of applications, Adv. Mat. 10.1002/adma.202003915
study provides resources for
understanding the evolution of (2020).
this chromosome, which can help
explain population genetic differ-
ences within and between these
species and may aid in conserva-
tion for our endangered closest
relatives. —LMZ

Proc. Natl. Acad. Sci. U.S.A. 117, 26273

(2020).

IMAGE: NASA/JPL-CALTECH EXOPLANETS Planets orbiting binary stars, like the system in this artist rendering, are more likely to be habitable if they have Earth-like oceans.

Oceans protect 30 OCTOBER 2020 • VOL 370 ISSUE 6516 545
circumbinary planets

Exoplanets that orbit a binary
star, known as circumbinary
planets, can experience large

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ALSO IN SCIENCE JOURNALS
Edited by Michael Funk

CORONAVIRUS IMMUNOLOGY STRUCTURAL BIOLOGY HYBRID PEROVSKITES

Factors determining Rethinking metabolic Secrets of a proton Structural secrets of
SARS-CoV-2 endemicity manipulations in MS pumping machine hybrid perovskites

Numerous factors determine Activation of the metabolic Mitochondrial complex I serves The optoelectronic and
whether a respiratory virus will enzyme pyruvate kinase (PK), as a primary entry point for photovoltaic applications of poly-
become endemic and remain which catalyzes a critical step in electrons from the tricarboxylic crystalline hybrid metal halide
in circulation around the world. glycolysis, has been proposed acid cycle into the mitochondrial perovskite films are notable
In a Perspective, Shaman and as a potential treatment for electron transport chain. This because grain boundaries in
Galanti discuss the features that multiple sclerosis (MS). Seki et massive, membrane-embedded most materials cause scattering
might contribute to severe acute al. confirmed that activators of protein complex must couple of charge carriers that decreases
respiratory syndrome coronavi- the PK isoform PKM2 limited quinone reduction to confor- performance. Electron micros-
rus 2 (SARS-CoV-2) endemicity. the differentiation of T helper 17 mational changes across more copy studies of these materials
These include whether people cells, which are thought to be than 150 angstroms within four have been hindered by their
can become reinfected after involved in MS disease, as previ- separate proton pumps. Kampjut rapid structural degradation
recovering from infection, ously reported. However, in a et al. determined five structures under intense electron beams.
whether there will be seasonality mouse model of MS, the authors of complex I in states along the Rothmann et al. now present
in the incidence of infection, and found that PKM2 activators catalytic cycle, a deactive confor- an atomic crystallographic
how SARS-CoV-2 competes with redirected disease pathology mation, and one with the inhibitor structure of formamidinium
other respiratory viruses. The from the spinal cord to the brain rotenone bound. The resolution lead triiodide (FAPbI3) poly-
authors discuss the importance instead of suppressing symp- of some structures was suf- crystalline thin films obtained
of waning immunity and immune toms. These results suggest ficient to see water molecules by low-electron-dose scan-
escape and what can be learned that the therapeutic potential of and to trace putative paths for ning transmission electron
from other endemic respiratory PKM2 activators for MS must be proton transfer within the proton- microscopy with advanced
viruses, including the “common reassessed. —WW pumping membrane domain. The image processing. The crystal
cold” coronaviruses and influ- structures add valuable details structure sustains substoichi-
enza virus. —GKA Sci. Signal. 13, eaay9217 (2020). that provide a basis for generat- ometry in the A-site cation,
ing mechanistic hypotheses for has a nearly perfect crystallo-
Science, this issue p. 527 T CELLS this crucial complex. —MAF graphic alignment between PbI2
impurity phases and the FAPbI3
ANIMAL COGNITION Poised for pathogenicity Science, this issue p. 547 perovskite, and has atomically
clean grain boundaries between
Forgotten ideas from a The production of the cytokine CANCER polycrystalline domains. These
Black zoologist granulocyte-macrophage col- features help to explain the films’
ony-stimulating factor (GM-CSF) Physical traits of cancer surprising regenerative ability,
Charles H. Turner (1867–1923) by T helper cells not only guides their benign grain boundaries
studied animal cognition, and adaptive immune responses but The biological and physical where strain and dislocations
despite an impressive body of can also contribute to the patho- properties of tumors contribute appear mostly absent, and why
work that challenged the main genesis of autoimmune disease. to their growth and to treat- excess lead-iodide precursor can
concepts of animal behavior, Rasouli et al. used single-cell ment outcome. Although intense be counterintuitively beneficial.
intelligence, and personality at RNA sequencing, mass cytom- research efforts have helped —PDS
the time, his work has largely etry, and GM-CSF fate reporter to delineate cancer biology,
been forgotten. As an African mice to identify a distinct subset the physics of cancer has only Science, this issue p. 548
American, Turner was unable of T helper cells in humans and emerged in relatively recent times
to obtain a university position, mice that specialize in sustained as a key area of research. Nia et M I C R O B I O TA
which likely explains why his GM-CSF production but lack key al. reviewed the physical features
work and ideas have not been phenotypic features of other that are common to tumors and Radioprotective bacteria
continued and have indeed T helper lineages. In a murine that limit successful treatment:
been repeated decades later. In model of experimental autoim- solid stresses, interstitial fluid A common symptom of radiation
a Perspective, Galpayage Dona mune encephalomyelitis, these pressure, stiffness (rigidity), and treatment for cancer is gastroin-
and Chittka discuss Turner’s cells were poised to up-regulate architecture and organization of testinal disruption. The damage
work, the challenges he faced as interferon-g within the central tumor constituents. The authors caused can become so severe
an African American then, and nervous system and promote provide a conceptual frame- and debilitating that it interrupts
the racial disparities that con- the development of encephali- work and discuss the origins of treatment. Guo et al. noticed
tinue in research today. —GKA tis, processes that required the these distinct physical traits of that mice surviving experimental
transcription factor T-bet. These cancer and how they enable and radiation exposure had distinc-
Science, this issue p. 530 results provide insight into the synergize with aberrant cancer tive taxonomic representation
identity of GM-CSF–producing biology to fuel cancer initiation, in their gut microbiota. A similar
CD4+ T cells and their function progression, immune evasion, correlation was also observed in
during autoimmune neuroin- and treatment resistance. —PNK a small group of human subjects.
flammation. —CO Further experiments in mice
Science, this issue p. 546 revealed that some strains of
Sci. Immunol. 5, eaba9953 (2020).

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bacteria produced high levels of perfectly associated with conducted a detailed model- a promising route to developing
short-chain fatty acids, which run timing but not with other ing of her ancestry with regard a platform for quantum tech-
seemed to be dampening inflam- traits such as maturity and fat to other Pleistocene human nologies. A successful platform
matory responses and alleviating reserves (see the Perspective genomes. They found evidence requires the interaction of many
the damage caused by reactive by McKinney). Further, they for Denisovan ancestry in qubits in close proximity, as well
oxygen species released by conclude that the region oper- ancient human genomes from as the ability to address each
the radiation. A metabolomics ates as a Mendelian trait, with at least 6000 years before the qubit individually, and, to date,
analysis also implicated a role for assortment dictating run timing Salkhit individual lived and such requirements have run
tryptophan metabolic pathways and associated phenotypes determined that the Denisovan counter to each other. Chen et
in radiation survivorship. —CA being caused by the migration contribution differed from that of al. devised an optical frequency-
environment rather than genet- another ancient Asian individual, domain method with which
Science, this issue p. 549 ics. —SNV as well as from the ancient they were able to simultane-
Denisovan contribution to extant ously address many individual
ANCIENT DOG GENOMICS Science, this issue p. 609; Australasians. This reference rare-earth ion defects (six at this
see also p. 526 point helps us to understand point) with separations all within
Dog domestication was the early history of our species the diffraction limit of the control
multifaceted PROTON MEMBRANES in Eurasia, especially Eastern light. Because the approach is
Eurasia, for which genomic evi- scalable to tens or hundreds of
Dogs were the first domesti- Vacancies enhance proton dence remains scarce. —LMZ defects, it provides the prospect
cated animal, likely originating conductivity of realizing truly large-scale quan-
from human-associated wolves, Science, this issue p. 579 tum processors. —ISO
but their origin remains unclear. Proton-exchange membranes
Bergstrom et al. sequenced (PEMs) allow for the transport of PA L E O G E N O M I C S Science, this issue p. 592
27 ancient dog genomes from protons while acting as electri-
multiple locations near to cal insulators and ensuring that A timeline of cave
and corresponding in time to reactants are kept apart; there- dwellers in sediment
comparable human ancient DNA fore, they are a key component
sites (see the Perspective by in devices such as low-tempera- Two archaic lineages over-
Pavlidis and Somel). By analyz- ture fuel cells. PEMs are typically lapped with modern humans
ing these genomes, along with made from polymers or materi- outside of Africa: the well-
other ancient and modern dog als embedded in a polymer studied Neanderthals and
genomes, the authors found matrix and need to operate in their more mysterious cousins,
that dogs likely arose once from conditions of very high humidity. the Denisovans. Denisovan
a now-extinct wolf population. Starting with an inorganic, lay- remains are rare, being limited
They also found that at least ered material, CdPS3, Qian et al. to Denisovan Cave in Siberia
five different dog populations show that the removal of a small and a putative, undated jaw
~10,000 years before the pres- amount of cadmium introduces from Tibet. However, there is
ent show replacement in Europe vacancies that greatly increase evidence for multiple introgres-
at later dates. Furthermore, the proton conductivity of the sions from Denisovans into
some dog population genetics PEMs (see the Perspective by modern-day humans, especially
are similar to those of humans, Wang and He). The process in Australasian populations.
whereas others differ, inferring works for manganese-based By examining the sediment of
a complex ancestral history for membranes as well, and high Baishiya Karst Cave located on a
humanity’s best friend. —LMZ lithium ion transport was also high plateau in Tibet, Zhang et al.
observed. —MSL identified ancient mitochondrial
Science, this issue p. 557; DNA from Denisovans indicat-
see also p. 522 Science, this issue p. 596; ing their presence at about
see also p. 525 100 thousand, 60 thousand, and
M I G R AT I O N possibly 45 thousand years ago.
HUMAN EVOLUTION This finding provides insight into
Unexpectedly simple the timing and distribution of
DNA analyses of an Denisovans in Asia and extends
Chinook salmon are known to early East Asian the time of occupation of the
return to spawn at two distinct Tibetan plateau by hominins.
times of the year: spring and fall. Ancient, anatomically modern —LMZ
Individuals that return during humans interbred with the
these times have generally been archaic hominins Neanderthals Science, this issue p. 584
referred to as parts of distinct and Denisovans. However,
groups, or ecotypes, with traits the extent of this inter- QUANTUM SYSTEMS
specific to their timing and pre- breeding and how it affects
sumed divergence being caused modern populations is not well Addressing the many and
by the lack of interbreeding. By understood. Massilani et al. the individual
looking at genomes across fish generated genome-wide data
from both runs, Thompson et from a 34,000-year-old female The ability to coherently manipu-
al. found that a single genomic individual from the Salkhit late the quantum state of atomic
region of interest was nearly Valley in eastern Mongolia and defects in solid-state systems is

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RESEARCH

◥ cells. Finally, when normal tissue architecture
is disrupted by cancer growth and invasion,
REVIEW SUMMARY microarchitecture is altered. Stromal and can-
cer cells and extracellular matrix adopt new
CANCER organization. This changes the interactions
between an individual cell and its surrounding
Physical traits of cancer matrix and cells, which affects signaling path-
ways associated with invasion and metastasis.
Hadi T. Nia, Lance L. Munn, Rakesh K. Jain*

BACKGROUND: Historically, cancer has been ing and migrating cells push and stretch solid OUTLOOK: The tumor microenvironment is
considered a disease of the cell, caused by components of the surrounding tissue. Being characterized by both biological and physical
mutations in genes that control proliferation, distinct from fluid pressure and close to zero abnormalities. The growing appreciation of the
differentiation, and death. In recent decades, in most normal tissues, solid stresses are large role of tumor-stromal interactions in cancer
however, the microenvironment surrounding enough to compress blood and lymphatic ves- has led to seminal discoveries that have re-
the cancer cell has gained notoriety as a co- sels in and around tumors, impairing blood sulted in previously unexplored targets and
conspirator in tumor initiation, progression, flow and the delivery of oxygen, drugs, and strategies for treatment. Understanding the
immune evasion, and treatment response. As immune cells. Acting at organ, tissue, and cel- key principles underlying the origins and con-
tumors grow, they disrupt the structure and lular levels, solid stresses activate signaling sequences of the physical traits of cancer will
function of the surrounding tissue via phys- pathways that promote tumorigenesis and be critical for improving treatment. Many of the
ical and biochemical mechanisms. The result- invasiveness and induce treatment resistance. concepts involved are nonintuitive and require
ing physical abnormalities affect both cancer Elevated interstitial fluid pressure is caused deep and broad understanding of both the phys-
cells and their microenvironment and fuel by leakage of plasma from abnormally per- ical and biological aspects of cancer. Therefore, a
tumorigenesis and treatment resistance. The meable tumor blood vessels and insufficient rigorous but accessible description of physical
links between cancer biology and physics have lymphatic drainage. As a result, the interstitial cancer traits will assist research into the phys-
provided opportunities for the discovery of fluid leaks out of the tumor into the peritumor ical sciences of cancer—a highly multidiscipli-
new drugs and treatment strategies. tissue, causing edema and elution of drugs and
growth factors and facilitating invasion and ▪nary area—and help it remain an active and
ADVANCES: Here, we propose four distinct phys- metastasis through flow-induced shear stresses.
ical cancer traits that capture the biomechan- Increased stiffness is caused by matrix depo- progressive subfield of cancer research.
ical abnormalities in tumors: (i) elevated solid sition and remodeling. Traditionally used as
stress, (ii) elevated interstitial fluid pressure, a diagnostic marker, and more recently as a The list of author affiliations is available in the full article online.
(iii) increased stiffness and altered material prognostic factor, increased stiffness activates †Corresponding author. Email: [email protected]
properties, and (iv) altered tissue microarchi- signaling pathways that promote prolifera- Cite this article as H. T. Nia et al., Science 370, eaaz0868
tecture. Solid stresses are created as proliferat- tion, invasiveness, and metastasis of cancer (2020). DOI: 10.1126/science.aaz0868

READ THE FULL ARTICLE AT
https://doi.org/10.1126/science.aaz0868

Solid stress Fluid pressure Stiffness Microarchitecture

kg
kg

Links between cancer physics and biology

Sustaining Deregulating Evading growth Resisting cell Genome Inducing Activating Tumor- Enabling Avoiding immune
proliferative cellular suppressors death instability and angiogenesis invasion and promoting replicative destruction
metastasis inflammation immortality
signaling energetics mutation

Physical traits of cancer. To provide a comprehensive framework for understanding the links between the physics of cancer and signaling pathways in cancer
biology in terms of a small number of underlying principles, we propose four physical traits of cancer that characterize the major physical abnormalities shared by
most if not all tumors.

Nia et al., Science 370, 546 (2020) 30 October 2020 1 of 1

RESEARCH

◥ able water and swell, generating solid stress
that is distinct from fluid pressure (12).
REVIEW
4) Actomyosin-mediated cell contractions.
CANCER Fibroblasts, immune cells, and cancer cells
can all contract matrix elements as they move
Physical traits of cancer around in a tumor or try to repair structural
damage. Cell contraction generates tensile
Hadi T. Nia1,2, Lance L. Munn1, Rakesh K. Jain1,3* forces that contract ECM components (13),
creating tension in some parts of the tumor,
The role of the physical microenvironment in tumor development, progression, metastasis, and treatment which are generally balanced by compression in
is gaining appreciation. The emerging multidisciplinary field of the physical sciences of cancer is now other elements (4). Cancer-associated fibroblasts
embraced by engineers, physicists, cell biologists, developmental biologists, tumor biologists, and (CAFs) that are activated with transforming
oncologists attempting to understand how physical parameters and processes affect cancer progression growth factor–b (TGF-b) become myofibroblasts
and treatment. Discoveries in this field are starting to be translated into new therapeutic strategies and can generate large contractile forces (14).
for cancer. In this Review, we propose four physical traits of tumors that contribute to tumor progression and
treatment resistance: (i) elevated solid stresses (compression and tension), (ii) elevated interstitial fluid The impact of solid stress on cancer cell
pressure, (iii) altered material properties (for example, increased tissue stiffness, which historically biology was first recognized in 1997, when
has been used to detect cancer by palpation), and (iv) altered physical microarchitecture. After defining Helmlinger et al. found that accumulated solid
these physical traits, we discuss their causes, consequences, and how they complement the biological stress inhibits the growth of tumor spheroids
hallmarks of cancer. (3). These stresses are sufficiently large to com-
press and even collapse blood and lymphatic
C ancer is generally considered a disease biological hallmarks of cancer, thus facilitating vessels (6, 7, 15). Vessel compression contrib-
of the cell, caused by mutations in genes cancer cell proliferation and invasion, immune utes to hypoxia (15, 16) and interferes with the
that control cell proliferation, death, me- system evasion, and resistance to therapies. delivery and/or efficacy of chemo-, radio-, and
tabolism, and DNA repair. To create a immunotherapies (17, 18). Solid stress may also
unified conceptual framework for under- Solid stresses and elastic energy have additional, direct effects on tumor biology,
standing the various manifestations of cancer, such as promoting the invasiveness of cancer
Hanahan and Weinberg proposed eight biol- Solid stresses, also known as residual stresses, cells (19) and stimulating tumorigenic path-
ogical hallmarks that delineate the key fea- are the mechanical forces (compressive, ten- ways in colon epithelia (20) (Fig. 3).
tures and properties of cancer cells (1). These sile, and shear) contained in—and transmitted
biological hallmarks are useful for concep- by—solid and elastic elements of the extracel- Cancer and normal cells have mechanosen-
tualizing cancer at the cellular level, but we now lular matrix (ECM) and cells (3). Reported in sitive machinery, such as cell-ECM (21) and
know that the microenvironment surrounding pascals or millimeters of mercury (1 mmHg ≅ cell-cell (22) adhesions and stretch-sensitive
the cancer cell acts as a coconspirator in tumor 133.3 Pa), solid stress values range from <100 Pa ion channels (23), that allows them to respond
initiation and progression. As tumors grow, (0.7 mmHg) in glioblastomas to 10,000 Pa to applied forces. Solid stresses can also act on
they disrupt the surrounding tissue biochem- (75 mmHg) in pancreatic ductal adenocarcino- cells indirectly by deforming ECM components.
ically and physically. They also recruit normal mas (PDACs) (4). Multiple mechanisms, sum- For example, matrix-bound latent TGF-b, in-
cells from the surrounding tissue, which fur- marized in Fig. 2 and discussed below, are active upon synthesis and unable to bind to its
ther alter the matrix and cellular compositions responsible for generating solid stress in tumors. cognate cell surface receptors, can be activated
of the tumor. These perturbations result in by myofibroblast-induced tensile forces on ECM
physical abnormalities associated with both 1) Increased tissue volume caused by cell in- (24). Other examples of ECM sensitivity to
cancer cells and the microenvironment in filtration, cell proliferation, and matrix deposi- tensile forces include the unfolding of fibro-
which they grow that influence tumor biology tion. The added volume pushes and displaces nectin in response to tensile forces (25), the
and response to treatment (2). existing viscoelastic structures inside and out- enzymatic resistance of collagen fibers (26),
side the tumor and gives rise to solid stresses and the tension-regulated interactions of fi-
To provide a more comprehensive concep- in the tumor and the surrounding tissue (4, 5). bronectin with collagen fibers (27).
tual framework for cancer, we propose four ad- As a result, when tumor cells are depleted
ditional traits stemming from the physical through anticancer therapeutics, solid stress is The nucleus is also a mechanosensitive or-
abnormalities of tumors. These are (i) elevated decreased, and blood vessels are decompressed ganelle capable of responding to solid stresses
solid stress, (ii) elevated interstitial fluid pres- (6, 7). through the activity of nuclear pore complexes
sure (IFP) and the resulting fluid flow in the and associated proteins, which modulate the
interstitium, (iii) increased stiffness and al- 2) Concerted displacement of normal tissue nuclear import of transcription factors when
tered material properties, and (iv) altered mi- (8, 9). Some tumors grow as well-circumscribed, the nucleus is deformed (28–30). Nuclear per-
croarchitecture (Fig. 1). As discussed in this nodular masses, in which the tumor remains turbations, such as those generated by cells
Review, these four physical traits are concep- cohesive and pushes the surrounding tissue, migrating through small pores, cause changes
tually distinct but can interact synergistically. generating considerable mechanical stresses. in gene expression and induction of DNA re-
They also enable and exacerbate many of the Other tumors are less cohesive and more in- pair programs (31, 32).
filtrative, interdigitating through the normal
1Steele Laboratories, Department of Radiation Oncology, tissue by finding the path of least resistance or YAP (Yes-associated protein) and TAZ (tran-
Massachusetts General Hospital and Harvard Medical School, by creating space by virtue of cytotoxic and scriptional coactivator with PDZ-binding motif)
Boston, MA 02114, USA. 2Department of Biomedical protease activities. In the latter case, there is have been identified as potent mechanores-
Engineering, Boston University, Boston, MA 02215, USA. less production of solid stress (5, 10). ponsive factors (33) that respond to physical
3Ludwig Center at Harvard, Harvard Medical School, Boston, cues, such as stretching (22, 34) and cell crowd-
MA 02115, USA. 3) Swelling of existing glycosaminoglycan ing (34), by translocating from the cytoplasm
*Corresponding author. Email: [email protected] matrix components such as hyaluronic acid to the nucleus. YAP/TAZ mechanobiology is
(HA) owing to (electro)osmotic water absorp- regulated by filamentous actin (F-actin) dy-
tion (11, 12). These components take up avail- namics through Rho guanosine triphospha-
tases (GTPases), which probe the physical

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RESEARCH | REVIEW

Solid stress Fluid pressure TGF-b (16). In preclinical models of PDAC, lo-
sartan alleviates solid stress and decompresses
kg blood vessels, enhancing chemotherapy and
kg increasing overall survival (16). This strategy is
currently being tested in a randomized clinical
Microarchitecture Stiffness trial (NCT01821729) based on promising re-
sults of a phase 2 trial (40). In another suc-
Fig. 1. Physical traits of cancer. On the basis of the advancements of the past few decades, we suggest cessful PDAC preclinical study, PEGPH20 (a
that the physical traits of cancer can be categorized into four major groups: (i) elevated solid stress, pegylated recombinant human hyaluronidase)
(ii) elevated interstitial pressure, (iii) increased stiffness, and (iv) altered architecture and geometry. Solid that reduced fibrosis in these tumors increased
stresses and fluid pressure are the mechanical stresses (force per unit area) contained in, and transmitted overall survival when combined with chemo-
by, solid and fluid phases of the tumor, respectively. Solid stresses and fluid pressure are reported in pascals therapy (41). Other approaches that have shown
or millimeters of mercury (1 mmHg ≅ 133.3 Pa). Stiffness (elasticity) is defined as the resistance of a material similar potential in preclinical models include
to deformation in response to an applied force, and elastic modulus is reported in pascals. Viscoelasticity inhibiting the vitamin D receptor (42), sonic
defines the resistance of the material to deformation in response to a force applied at a given rate. Most hedgehog signaling (43), and C-X-C motif che-
soft tissues, including tumors, exhibit higher resistance to force (e.g., higher stiffness) when the force mokine receptor 4 signaling (44). Targeting
is applied at high rates. Solid stress, the latent or stored stress in a tissue, should not be confused with the vitamin D receptor is currently being tested
elasticity (stiffness) or viscoelasticity (time-dependent stiffness), which define how much or how fast, in patients (NCT03472833). However, both
respectively, a tissue will deform if a force is applied. A tissue can be stiff (rigid) or soft (compliant), and, PEGPH20 and sonic hedgehog targeting have
independently, it can be under compressive and/or tensile solid stresses (4) or, like most normal tissues, it been unsuccessful in clinical trials (45), high-
can be unstressed. The proposed physical traits characterize most cancers, and their distinct origins and lighting the need for a deeper understanding
consequences make them indispensable to a comprehensive picture of cancer. of these pathways. Alleviating stress using these
approaches may improve response to various
microenvironment via cell-matrix and cell-cell space. Cell competition has recently received treatments, such as immunotherapy (44, 46).
adhesion complexes at the cell surface (35). attention because of its relevance in devel-
Thus, mechanosignaling by YAP and TAZ can opment, where it controls organ size and Interstitial fluid pressure
be modulated by modifiers of actin and Rho eliminates suboptimal cells (37), and in tumor-
GTPases such as cofilin, gelsolin, and F-actin– igenesis, where cancer cells expand into new In most organs, the blood arrives via arteries
capping protein (CAP-Z). In a two-dimensional space by damaging and killing the normal sur- and leaves via veins, and any excess tissue fluid
(2D) epithelial monolayer model of stretch, rounding cells (38). Compressive and tensile is drained by lymphatic vessels. This main-
cells under tensile stresses showed activation stresses, generated from the differential growth tains fluid homeostasis and results in near-
of YAP/TAZ that led to cell proliferation (34) of cell layers, has been suggested to be a me- zero IFP in most normal organs. This balance
and induced cell cycle entry (22). Activation chanical driver of cell competition (39). How is disturbed by abnormalities in tumors, in-
of the YAP/TAZ pathway contributes to tumor cancer cells are able to outcompete the sur- cluding hyperpermeable blood vessels and
malignancy in many ways, including cell pro- rounding normal cells, which experience sim- compression of blood and lymphatic vessels
liferation, cell cycle regulation, overcoming ilar solid stresses at the tumor-host interface, by solid stress. Leaky vessels, combined with
anoikis and mitochondria-induced apoptosis, remains an open question. a compromised drainage system, result in high
inducing cancer stem cell functions, and ac- IFP (Fig. 2), ranging from <1 kPa (7.5 mmHg) in
celerating fibrosis and desmoplasia by activat- Because solid stresses are harbored in matrix brain tumors to 5 kPa (37 mmHg) in renal cell
ing CAFs (36). components, many of the resulting problems carcinomas. IFP is fairly uniform within a tu-
can be reversed by drugs that degrade matrix mor and drops precipitously in the tumor
As cancer growth causes crowding of cells in components and reduce fibrosis. For example, margin, which generates a fluid flow toward
the tissue, there is inevitably competition be- losartan, an angiotensin receptor 1 blocker, re- lymphatic vessels in the surrounding normal
tween cell populations for nutrients and free duces both collagen I and HA by inhibiting tissue, where IFP is close to 0 mmHg. Note
that IFP and solid stress are independent
mechanical stresses with distinct origins and
consequences (47).

High IFP in tumors was first reported in
1950 (48) and then later studied in detail
through experiments and computational models
(49, 50). Elevated fluid pressure drives intersti-
tial flow in the tumor margin, exposing extravas-
cular cells to shear stress. Because flow velocity
and shear stresses depend strongly on the pore
size between cells and matrix components,
shear stresses likely vary widely, even along
individual cell membranes. The shear stresses
affect the biology of cancer and stromal cells in
several ways (51) (Fig. 3), including activation
of fibroblasts (51); modulation of endothelial
sprouting (52), which affects angiogenesis and
lymphangiogenesis (51); induction of matrix
metalloproteinase (MMP) activity and cell mo-
tility (53); and activation of cancer cell mi-
gration (54) and invasion (55). Fluid flow has

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RESEARCH | REVIEW Normal surrounding cells
Cancer cells
Fig. 2. Origins of the physical traits Cancer-associated
of cancer. Physical interactions of fibroblasts
cancer cells with stroma give rise to Extracellular matrix
physical traits of tumors through distinct Adipocytes
and interconnected mechanisms. Leaky
and compressed blood vessels and Immune cells
nonfunctional lymphatics lead to
increased interstitial fluid pressure Endothelial cells
within the tumor and interstitial fluid
flow in the tumor margin. Cellular Interstitial fluid flow
proliferation, matrix deposition, cell con-
traction, and abnormal growth patterns Mechanism Leaky blood Cell proliferation Cell Matrix deposition
lead to compressive and tensile solid vessels contraction
stresses. Matrix deposition and cross-
linking cause increased stiffness in Nonfunctional Compressed Growth pattern Matrix
tumors. Cell contraction, matrix deposi- lymphatics vessels (infiltrative cross-linking
tion, and cross-linking also alter the vs. nodular)
architecture of the tissue. The physical
traits also interact with each other; solid
stresses compress blood and lymphatic
vessels and contribute to increased fluid
pressure in tumors. Tensile solid
stresses result in stretched and aligned
matrix, and through strain-stiffening,
solid stresses also increase tumor stiff-
ness. Fluid flow activates fibroblasts,
which then contribute to increased solid
stresses and stiffness values and alter
ECM architecture.

Physical hallmark Fluid pressure Solid stress Stiffness Microarchitecture

kg
kg

Compressed Flow-induced stiffening Strain Solid stress–induced
vessels & matrix organization stiffening matrix organization

also been shown to induce cell cycle arrest response in multiple ways. High IFP hinders nant from benign breast, head, and neck tumors
through integrin signaling (56). Because im- the convection of drugs from the vasculature (66, 67) and as a prognostic marker in some
mune cells are also responsive to interstitial into the bulk of the tumor (2, 49). Moreover, clinical studies (68).
the steep IFP gradient at the tumor boundary
flow, these fluid forces are likely also involved drives the flow of interstitial fluid from the tu- Therapeutic strategies for correcting the fluid
in regulation of immunity (51). Mechanisms for mor toward the surrounding tissue. This flow abnormalities in tumors have also been devel-
mechanotransduction of flow signals include can promote tumor invasion and growth by fa- oped. One approach is to normalize the leaky
sensors within the focal adhesions (54, 57), the cilitating the transport of growth factors and and tortuous vasculature so that the intralumi-
cell glycocalyx (55), cell-cell junctions (58, 59), cancer cells into the surrounding normal tissue nal pressure operating within microvessels is
ion channels (60), Notch receptor (61), and and peritumor lymphatics (65). The outward not transmitted directly to the surrounding
cilia (62). The resulting signals can up-regulate fluid flow may also facilitate angiogenesis in interstitium. Vascular normalization restores
TGF-b expression and activate YAP/TAZ down- the tumor margin (52) and remove therapeu- abnormal tumor vasculature to a more func-
stream pathways (51, 63, 64). tic agents from the tumor, reducing drug re- tional state closer to that of normal vessels.
tention times (65). IFP has also been proposed Using judicious doses of antiangiogenic thera-
In addition to direct mechanotransduction as a diagnostic marker differentiating malig- py to normalize tumor vasculature (17, 65, 69),
it is possible to increase pericyte coverage,
mechanisms, fluid flow created by IFP gradients

can affect tumor progression and treatment

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RESEARCH | REVIEW

Ang-2 Cytoplasm
Nucleus
PDGF
p53
P iezo1 S1P Rho
Piezo1 p38 Yap
P iezo2 beta-catenin

ROCK MRTF-A

Solid stress mitochondria ATP
fission/fusion
kg vessel
kg compression HIF1- a

Microarchitecture MMP-2

Latent ret MMP-9 Yap Leukocyte
TGF-beta E-cadherin actin beta-catenin Adipose
stromal cell
Stiffness MRTF-A Epithelial

Fluid pressure TGF-beta R1 ERK TAZ TAZ Endothelial
TGF-beta R2 JNK TAZ TAZ Mesenchymal

TGF-beta TAZ TAZ Glioblastoma
Carcinoma
p38 Yap
SMAD 1/5Yap Yap Sarcoma

SMAD 2/3 Yap Neuroblastoma
Yap Activation
Inhibition
Yap Translocation
Yap Cyclic loading

SWI/SNF

F-actin

DIA SKP2 P27 RB
Cyclin D1 - CDK4
RhoA-GTP

ROCK MLC

LARG RhoA GTP

g ly c o c a lyx

GEF-H1 actin
ERK
PAX
BMPRIA

SMAD1/SMAD5 G2/M arrest

integrin actin
FAK
Rho miR-203 HIF1alfa

P iezo1 ROCK
ERK

PI3K PI3K

RA RAR RAR γ
Lamin A TWIST
G3BP2
TWIST aromatase

DDR1 JNK1 JunB

DLL NICD NICD
Notch p53
Rac Actin

TGF-b1 aSMA
GSK-3 β p
Akt p GADD45
p21
G protein

Rb p

HDAC1 p p
eNOS HDAC1

glycocalyx PYK2 NO
Ion

Channel

Fig. 3. Pathways associated with the physical traits of cancer. Physical traits of cancer activate a large cascade of mechanoresponsive pathways in cancer
cells and stromal cells, including endothelial, epithelial, mesenchymal, and immune cells. Pathways such as integrin and YAP/TAZ are responsive to all four physical
traits, whereas many other pathways appear to be more specific.

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