Science

CONTENTS 524 & 577

2 NOVEMBER 2018 • VOLUME 362 • ISSUE 6414 Predicting viral origins

NEWS FEATURES

SPECIAL SECTION IN BRIEF 514 MOMENTS TO SPARE Downloaded from http://science.sciencemag.org/ on November 5, 2018
California’s new earthquake warning
CREDITS (FROM TOP): BABYAN ET AL.; HUMPHREY/SHUTTERSTOCK COMPOSITE 504 News at a glance system delivers just seconds of notice.
MATERIALS Even that is a victory By P. Voosen
IN DEPTH
INTRODUCTION INSIGHTS
507 SEAFLOOR MAPPERS TO
534 Mixing and matching materials COMPETE FOR XPRIZE PERSPECTIVES
Faster, cheaper autonomous systems
REVIEWS could aid in resource extraction and 518 SHIFTING SUMMER RAINS
science By J. Rosen Trace-element records in Chinese caves
536 Composites from renewable and reveal the effects of climate change on
sustainable resources: Challenges and 508 ADVANCES IN FLOW BATTERIES Asian monsoons By D. McGee
innovations A. K. Mohanty et al. PROMISE CHEAP BACKUP POWER
Upstart technology could enable ▶ REPORT P. 580
543 Biological composites— widespread adoption of renewables
complex structures for functional 520 IDENTIFYING POSTURE CELLS
diversity M. Eder et al. By R. F. Service IN THE BRAIN
The parietal cortex represents body
▶ PODCAST 510 MICROBIOME CONSERVANCY STORES posture and other factors in spatial
GLOBAL FECAL SAMPLES awareness By G. Chen
547 Composites with carbon Research could help prevent or
nanotubes and graphene: An outlook treat diseases of the gut ▶ REPORT P. 584
I. A. Kinloch et al.
By T. Rabesandratana 521 CANCER ENZYME AFFECTS
ON THE COVER PARKINSON’S DISEASE
511 LLAMA ANTIBODIES INSPIRE GENE New insights identify a possible
This whimsical photo of SPRAY TO PREVENT ALL FLUS target for slowing neurodegeneration
a coconut turned into Strategy for mutable virus might outdo
a car represents the traditional vaccines By J. Cohen By P. Brundin and R. Wyse
increasing use of natural
materials in commercial ▶ REPORT P. 598 ▶ RESEARCH ARTICLE P. 557
composites, particu-
larly in the automotive 512 EUROPE’S €1 BILLION QUANTUM 523 EVOLVING A PATHOGEN
sector. Coconut fibers FLAGSHIP ANNOUNCES GRANTS TO BE PROTECTIVE
(coir) and powdered Program aims to nudge quantum The deadly fungus Candida albicans
coconut shells can be combined with a variety technology to market By E. Cartlidge can be pushed to protect its mammalian
of polymers to make car parts, including host By C. d’Enfert
door cladding, structural guards, and internal 513 SUSPECT SCIENCE LEADS TO PAUSE
components. For more on the investigation and IN STEM CELL TRIAL ▶ REPORT P. 589
application of biological, hybrid, and carbon- Harvard University finds fraud in
based composite materials, see page 534. 31 papers, casting doubt on study 524 SOURCES OF HUMAN VIRUSES
Photo: Cary and Babs Wolinsky rationale By Jocelyn Kaiser Machine learning predicts the hosts and
vectors of RNA viruses that can infect
518 & 580 humans By M. Woolhouse

SCIENCE sciencemag.org ▶ REPORT P. 577

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CONTENTS 595

2 NOVEMBER 2018 • VOLUME 362 • ISSUE 6414 Snapshot of nucleosomal
transcription

525 DISORDER AT THE BORDER RESEARCH ARTICLES 580 PALEOCLIMATOLOGY Downloaded from http://science.sciencemag.org/ on November 5, 2018
The photoinduced phase transition East Asian hydroclimate modulated by
CREDITS (FROM TOP): KUJIRAI ET AL.; ROBERT NEUBECKER in vanadium oxide involves 557 NEURODEGENERATION the position of the westerlies during
ultrafast loss of coherence Poly(ADP-ribose) drives pathologic Termination I H. Zhang et al.
a-synuclein neurodegeneration in
By A. Cavalleri Parkinson’s disease T.-I. Kam et al. ▶ PERSPECTIVE P. 518

▶ REPORT P. 572 RESEARCH ARTICLE SUMMARY; FOR FULL TEXT: 584 NEUROSCIENCE
dx.doi.org/10.1126/science.aat8407 Efficient cortical coding of 3D posture
POLICY FORUM ▶ PERSPECTIVE P. 521 in freely behaving rats B. Mimica et al.

527 EDITING NATURE: LOCAL ROOTS 558 DRUG DISCOVERY ▶ PERSPECTIVE P. 520
OF GLOBAL GOVERNANCE Defining the human C2H2 zinc finger
Environmental gene editing degrome targeted by thalidomide 589 MICROBIOTA
demands collective oversight analogs through CRBN Q. L. Sievers et al. Experimental evolution of a fungal
pathogen into a gut symbiont
By N. Kofler et al. RESEARCH ARTICLE SUMMARY; FOR FULL TEXT:
dx.doi.org/10.1126/science.aat0572 G. H. W. Tso et al.
BOOKS
559 METALLURGY ▶ PERSPECTIVE P. 523
530 IMPROVING OUTBREAK RESPONSE Extra strengthening and work
Learning from Ebola failures is hardening in gradient nanotwinned 595 STRUCTURAL BIOLOGY
key for crafting better plans metals Z. Cheng et al. Structural basis of the nucleosome
for public health emergencies transition during RNA polymerase II
RESEARCH ARTICLE SUMMARY; FOR FULL TEXT: passage T. Kujirai et al.
By W. F. Pewen dx.doi.org/10.1126/science.aau1925
598 ANTI-FLU THERAPY
531 COLLECTOR’S ITEM OR CULTURAL REPORTS Universal protection against influenza
HERITAGE? infection by a multidomain antibody to
A riveting tale of a smuggled 560 NANOMATERIALS influenza hemagglutinin N. S. Laursen et al.
dinosaur illuminates an enduring A general synthesis approach for
tension in paleontology supported bimetallic nanoparticles via ▶ NEWS STORY P. 511
surface inorganometallic chemistry
By V. M. Arbour 610
K. Ding et al.
LETTERS DEPARTMENTS
564 ORGANIC CHEMISTRY
532 BEYOND HIERARCHICAL Catalytic palladium-oxyallyl 503 EDITORIAL
ONE-ON-ONE MENTORING cycloaddition B. M. Trost et al. How to clean up the Ganges?

By M. C. Horner-Devine et al. 568 QUANTUM OPTICS By Tushaar Shah et al.
Topological protection of biphoton
532 ENGAGING COMMUNITY states A. Blanco-Redondo et al. 610 WORKING LIFE
WITH HUMILITY What are you waiting for?
572 PHYSICS
By J. Delborne et al. Ultrafast disordering of vanadium By R. C. Larson
dimers in photoexcited VO2
533 EVOLUTION OF TEETH IN Science Staff ............................................. 502
SOUTH AMERICA S. Wall et al. New Products............................................ 603
Science Careers ........................................ 605
By D. A. Croft ▶ PERSPECTIVE P. 525

RESEARCH 577 EPIDEMIOLOGY
Predicting reservoir hosts and
IN BRIEF arthropod vectors from evolutionary
signatures in RNA virus genomes
554 From Science and
other journals S. A. Babayan et al.

▶ PERSPECTIVE P. 524

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EDITORIAL

How to clean up the Ganges?

F or millennia, the Ganges River, holy to Hindus, dustrial effluents to the needed standards. And water Tushaar Shah
has provided livelihoods, food, and water for Ne- managers must enhance river flow so that secondary is a senior fellow
pal, India, and Bangladesh. Last month, one of In- treated waste can be safely discharged into Ganga. of the International
dia’s leading environmental activists died after a Water Management
111-day hunger strike, failing to evoke changes to Since 1855, a profusion of barrages and dams has Institute, Colombo,
save India’s most revered river (known as Ganga). diverted water from Ganga and its tributaries for hy- Sri Lanka, and
dropower and canal irrigation. But over the past five is working in
Gujarat, India.
After years of unrelenting abuse, Ganga is now decades, farmers have increasingly turned away from [email protected]

one of the world’s worst polluted rivers. India’s Prime canal irrigation to shallow tube wells. Herein lies a big Chittaranjan Ray
is director of the
Minister Narendra Modi vowed in 2014 to clean Ganga opportunity for cleaning Ganga. During the 1970s, mod- Nebraska Water
Center at the
by 2019, but despite increased funding and much lip elers recommended cranking up the “Ganges water ma- University of
Nebraska, Lincoln,
service, the river is more polluted than before. Mr. chine” to relieve flooding in the eastern parts of the river NE, USA. cray@ Downloaded from http://science.sciencemag.org/ on November 5, 2018
nebraska.edu
Modi needs a new strategy. basin by promoting intensive
Uma Lele
Pressure on Ganga has groundwater-based irrigation is president-elect
of the International
been building for decades. Women worship on polluted bank of during winter and summer Association
of Agricultural
With a tripling of human the Ganges, in Allahabad, India. months. The strategy was Economists,
Milwaukee, WI,
population since 1950 and to draw down basin water USA. umalele1@
gmail.com
rapid urbanization, 50 cities tables in the copious alluvial

along Ganga daily release aquifers. Shallow aquifers

6 billion liters of untreated would then absorb monsoon

sewage into the river, by far floods and snowmelt, and

the largest source of pollu- protect Bihar, North Bengal,

tion. Untreated industrial and Bangladesh from annual

effluents compound the prob- floods. Monsoons would re-

lem, together with run-off plenish aquifers that shallow

of chemical fertilizers and tube wells could then tap into

pesticides. Unfettered dis- for irrigation. This concept

posal of human and animal did not catch on back then,

corpses into Ganga makes it but today, the water machine

unfit even for ritual bathing. is alive and kicking thanks

Barrages and hydroelectric to easy access to credit and

projects on the main stem cheaper drilling technology.

of Ganga and its tributaries “…despite increased funding With over 6.5 million shallow
divert 60% of their waters, and much lip service, the river is tube wells in Nepal, India, and
leaving little mainstream Bangladesh, the Ganga basin

flow, which further concen- more polluted than before.” is one of the most densely
trates pollutants in the river. plumbed aquifer systems in

Earlier governments tried the world. More than 80% of

cleaning Ganga, investing some U.S.$14 billion, mostly in farmers depend on these wells. The water machine would

plants that treat sewage to an acceptable level of pollut- be revved up even more but for the high cost of diesel that

ants before discharge into waterways. Mr. Modi brought a farmers must use to pump groundwater. But affordable

new sense of urgency to the task, allocating U.S.$27 billion electricity or solar pumps could wean farmers from canal

up to 2019. But money alone will not clean the river. Com- irrigation, leaving more water to flow in Ganga and its

plex long-standing issues must be addressed, including tributaries, without adversely affecting hydropower.

PHOTO: RITESH SHUKLA/NURPHOTO/GETTY IMAGES increasing involvement of stakeholders, reducing corrup- The quickest, cheapest, and most effective way for

tion in pollution control agencies, increasing accountabil- Mr. Modi to show a less polluted Ganga by 2019 would

ity and rule enforcement, and inciting behavioral change be operating dams and barrages in the Ganga basin with

among citizens. This requires tackling three interrelated the sole objective of augmenting river flows. This would

challenges, each involving different stakeholders. Munici- be a start to controlling discharge of untreated sew-

palities must curtail discharge of untreated sewage and age and industrial waste, which will take a long time.

rapidly build sewerage infrastructures. Pollution control

authorities must ensure treatment of municipal and in- –Tushaar Shah, Chittaranjan Ray, Uma Lele*

*The views expressed in this editorial are those of the authors and do not necessarily represent the opinions of their institutions. 10.1126/science.aav8261

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NEWS Corrected 1 November 2018. See full text.

“ ”It’s the little spacecraft that could. It did everything
we asked of it, and more.

Jessie Dotson, a NASA project scientist, announcing the demise this week of Kepler,
the prolific exoplanet-hunting satellite, which ran out of fuel after 9 years in space.

IN BRIEF A bid to sequence all species
Edited by Jeffrey Brainard
GENOMICS | The Earth BioGenome Project—
ASTRONOMY an ambitious $4.7 billion, 10-year plan
to sequence the genomes of all of Earth’s
Cosmic law renamed to expand credit 1.5 million known species of animal,
plant, fungus, and protozoan—officially
The change honors Georges Lemaître, an astronomer and priest, as co-discoverer of cosmic expansion. began this week. In addition to provid- Downloaded from http://science.sciencemag.org/ on November 1, 2018
ing insights into evolution, the genomic
H ubble’s Law, a cornerstone of cosmology that describes the ex- data are intended to help conserve and PHOTO: BETTMANN/GETTY IMAGES
pansion of the universe, should instead be called the Hubble- restore biodiversity as well as provide
Lemaître Law, following a vote of more than 4000 members of benefits for agricultural and biomedical
the International Astronomical Union (IAU) announced this research. The Wellcome Sanger Institute
week. The change aims to credit Georges Lemaître, a Belgian in Hinxton, U.K.; BGI in Shenzhen, China;
astronomer and Catholic priest who in 1927 calculated that and 15 other institutions have pledged to
the universe was expanding, 2 years before U.S. astronomer Edwin raise $600 million initially and agreed
Hubble found that galaxies farther from Earth were receding faster. to coordinate their efforts and to work
Some astronomers criticized IAU for not allowing enough debate. with other sequencing projects, to avoid
“The IAU presented the issue as neat and tidy, but it is a much more overlap in species covered, for example.
murky and messy tale,” says Michael Merrifield of the University of Most of these affiliated projects concen-
Nottingham in the United Kingdom, because other researchers could trate on taxonomic groups, such as insects
have a claim. Others argue that IAU has no standing to get involved or fungi, but some focus on the species of
in the history of science and rename physical laws. The vote does not specific countries. The Wellcome Trust, for
change the name of the Hubble constant, the actual expansion rate. example, announced this week plans to
sequence within 10 years all 66,000 known
504 2 NOVEMBER 2018 • VOL 362 ISSUE 6414 eukaryotic species in the United Kingdom.

Scrolls revealed as forged

B I B L I CA L A R C H A EO LO GY | An indepen-
dent analysis of their ink revealed that five
fragments of text claimed to be pieces of
the Dead Sea Scrolls are modern forgeries,
the Museum of the Bible in Washington,
D.C., announced last week. Scholars had
long questioned the authenticity of these
and the 11 other fragments in the museum’s
collection. The texts were bought on the
antiquities market by the Green family, the
evangelical billionaires who have bankrolled
the museum (Science, 20 October 2017,
p. 295). Its administrators say they will
replace the known fakes in the museum’s
Dead Sea Scrolls display with other
fragments in its collection, with labels
saying that their authenticity, too, has
been questioned.

Canada introduces carbon tax

C L I M AT E C H A N G E | Canada announced
last week it will implement a tax on carbon
emissions in the four provinces that do
not already have either a tax or cap-and-
trade system of their own—Manitoba, New

sciencemag.org SCIENCE

Published by AAAS

Corrected 1 November 2018. See full text.

Brunswick, Ontario, and Saskatchewan. employees and that there was no evi- have an extensively drug resistant (XDR) Downloaded from http://science.sciencemag.org/ on November 1, 2018
The federal levy will come into effect on dence of gender discrimination, “wrongful form of the lung disease. Bedaquiline
1 April 2019 at CA$20 per ton, rising to exploitation of scientific work,” or misuse (sold as Sirturo) came to market in 2012
CA$50 per ton in 2022, Canadian Prime of grant monies by Stratton and other primarily to treat multidrug-resistant
Minister Justin Trudeau said. The govern- senior institute managers. But the lawyer’s (MDR) TB—a form that doesn’t respond
ment expects the tax to raise CA$2.36 report faulted the institute for a paucity of to the most common TB drugs but usually
billion next year, but under a measure female scientists—seven of the institute’s remains treatable by other medications.
unique among countries that have imple- 33 faculty members are women—and lack About 600,000 people each year acquire
mented a carbon tax, it will return 90% of of transparency in its processes for firing MDR TB, and about 6% of those fall
that revenue directly to taxpayers in the employees. The probe responded to a into the XDR category. Their TB doesn’t
four provinces, providing them an incen- 170-page April complaint by a woman who respond to the second tier of drugs and
tive to reduce their personal emissions was terminated; she also referred to a joint typically produces a mortality rate of 60%.
from burning fossil fuels. The size of the statement of concern from several other At the 49th Union World Conference on
refund is based on each province’s energy employees. In a statement, Stratton apolo- Lung Health held last week in The Hague,
mix—ranging from an average of CA$248 gized for “failures in people management” Netherlands, researchers reported that
per household in New Brunswick to and added he is “personally committed to” bedaquiline-containing regimens cured
CA$598 per household in Saskatchewan— righting the gender imbalance among “our 80% of a group of 181 TB drug–resistant
and will increase with carbon prices. scientific leaders.” Jeremy Farrar, director patients, 64% of whom had XDR. Only
Ontario and Saskatchewan are challenging of the Wellcome Trust in London, the char- three people in the group died.
the federal tax in court. ity that funds the institute, also apologized
in a statement that the institute failed to Hungary forces university move
Genomics lab leaders cleared recognize and act on diversity and inclu-
sion issues sooner. H I G H E R E D U CAT I O N | The Central
WO R K P L AC E | The Wellcome Sanger European University (CEU) in Budapest,
Institute, the world-renowned genom- Toughest TB cases routinely cured under pressure from Hungary’s right-wing
ics center in Hinxton, U.K., last week government, will send incoming students
cleared its director of allegations of PUBLIC HEALTH | A clinical trial from to a new campus in Vienna starting
bullying and gender discrimination after Belarus has provided what some tuber- next year. The private university, founded
an investigation led by an outside attor- culosis (TB) experts say is the most in 1991 by American-Hungarian billionaire
ney, Thomas Kibling. He concluded that compelling evidence that the drug beda- philanthropist George Soros and based in
director Michael Stratton had not bullied quiline can help cure most people who Budapest since 1993, grants U.S.-accredited

Only a few scientists PA L E OA N T H R O P O L O GY
have squeezed into a
South African cave rich Virtual tour
in hominin bones. reveals fossil cave

PHOTO: ROBERT CLARK/CONTRIBUTOR/GETTY IMAGES O nly a handful of people have
entered the Dinaledi chamber
in the Rising Star cave in South
Africa, where hundreds of bones
of a mysterious early hominin
called Homo naledi were discovered in
2015. To access it, researchers must
squeeze through a chute only 18 centi-
meters wide. But now, anyone with
a smartphone can explore the fossil
chamber. The Perot Museum of Nature
and Science in Dallas, Texas, and the
University of the Witwatersrand in
Johannesburg, South Africa, developed
a virtual reality tour, which opened
in May for visitors to the museum.
To expand the exhibit’s reach, the
museum and the university last week
released the tour in a freely down-
loadable app format, compatible with
Google Cardboard, a virtual reality
headset that can be made at home.
The tour is available in English, Spanish,
isiZulu, Setswana, and Sesotho.

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Corrected 1 November 2018. See full text.
NEWS | IN BRIEF

graduate degrees in environmental science, TMT board now faces no legal obstacles to Downloaded from http://science.sciencemag.org/ on November 1, 2018
math, and other fields. In 2017, the govern- restarting construction, though it may still
ment enacted a law requiring international face protesters on the mountain. PHOTO: JASMINA WIEMANN
universities to have a campus in the coun-
try where they are officially chartered. CEU Dinosaurs began colored eggs
says its collaboration with Bard College in
Annandale-on-Hudson, New York, fulfills PA L EO N TO LO GY | Birds were not the first
the requirements. Hungary’s government, to lay colored eggs: Dinosaur eggshells
however, has declined to sign the required came in a panoply of hues and speckle pat-
agreeement. The university said in its terns, researchers report in the
25 October announcement that current 1 November issue of Nature. The authors
students can remain in Budapest to finish argue that eggshell coloration likely had a
their degrees and that it will “maintain single evolutionary origin, in the carnivo-
as much research and educational activity rous dinosaurs called theropods that gave
in Budapest as possible.” rise to modern birds. The researchers, led
by Jasmina Wiemann of Yale University,
Iran brings capital charges used spectroscopic analysis of fossils to
identify pigments in eggs of 15 species of
I N T E R N AT I O N A L A F FA I R S | Prosecutors dinosaurs and prehistoric birds, reveal-
in Iran have charged four conservation- ing their probable original colors. As with
ists with “sowing corruption on Earth”—a modern birds, the dinosaurs’ tinted shells
crime punishable by death. The envi- likely camouflaged their eggs from preda-
ronmentalists, with the Persian Wildlife tors, while distinctive speckling patterns
Heritage Foundation in Tehran, were may have helped parents distinguish their
arrested on suspicion of espionage own eggs from those of cuckoolike dino-
in January. Iran’s Revolutionary Guards saurian nest parasites, Wiemann says.
accused them of using camera traps—
intended for remotely monitoring rare Tests of fossilized dinosaur eggs (top eggshell) show
Asiatic cheetahs and other wildlife—to they had colors like those of modern bird eggs.
eavesdrop on the nation’s ballistic missile
program. Two of the accused serve on China allows rhino, tiger trade
International Union for Conservation
of Nature (IUCN) panels that recommend W I L D L I F E C O N S E RVAT I O N | In a setback
whether to add or remove species from for conservationists, China this week said it
IUCN’s Red List of Threatened Species. will legalize the use of tiger and rhinoceros
Taher Ghadirian and Houman Jowkar bones and tissues “in medical research and
are members of the cat specialist group, healing,” as long as the material comes
and Ghadirian is also part of the bear from farmed animals. The move ends a ban
specialist group. Many observers view the that had been in place since 1993. Many
detainees as pawns in a power struggle Chinese believe tiger and rhino parts have
between the hardline Revolutionary medicinal properties, despite a lack of sci-
Guards and Iranian President Hassan entific evidence. Conservationists fear the
Rouhani’s relatively moderate admin- new policy will ease the ability of poachers
istration, which in a review last spring to smuggle parts from wild animals into
determined that the spying accusation the Chinese market, further imperiling the
is baseless but has been powerless endangered species.
to secure the conservationists’ release.
SCIENCEMAG.ORG/NEWS
Court OKs Hawaiian telescope Read more news from Science online.

ASTRONOMY | The Supreme Court of the
State of Hawaii ruled this week that the
Thirty Meter Telescope (TMT) project
should be granted a permit for construction
on Mauna Kea. The TMT, to be one of the
world’s largest optical telescopes, is opposed
by some native Hawaiian groups because
the mountain is a sacred site. The project’s
original permit was revoked in 2015 on
procedural grounds because opponents had
not been given opportunities to object. The
state’s supreme court dismissed another
challenge, to the University of Hawaii’s sub-
lease of land for the project, in August. The

sciencemag.org SCIENCE

Published by AAAS

IN DEPTH

The Swiss team tests a Downloaded from http://science.sciencemag.org/ on November 1, 2018
laser mapping submersible

in Lake Annecy in France.

MARINE GEOLOGY

Seafloor mappers to compete for XPRIZE

Faster, cheaper autonomous systems could aid in resource extraction and science

By Julia Rosen titions to spur innovation, and in 2015, it two new volcanoes, one of which is bigger

turned to the problem of mapping the ocean than Mount Vesuvius,” she says.

N ext week, a small yellow and white– floor, says contest director Jyotika Virmani. Sharper pictures of the ocean floor could
striped boat will slip out of port in Ka- The catalyst was the disappearance of Malay- help companies look for resources such as
lamata, Greece, and motor away from sia Airlines Flight 370 somewhere over the oil. (The energy company Shell is the prize’s
shore. The vessel won’t carry a captain Indian Ocean, and the stark realization that sponsor.) But researchers want a clearer
or crew, just an array of electronics recovery teams knew little about what lay be- view, too. For example, Dave Clague, a

that will tell it where to go, and when low the surface of the search area. “Instead geologist at the Monterey Bay Aquarium

to drop the torpedo-shaped pod lodged in of the airplane, unfortunately, they did find Research Institute in Moss Landing, Cali-

its stern. Once released, the sonar- fornia, studies volcanic activity

equipped vehicle will descend sev- along midocean ridges—submarine

eral kilometers into the frigid abyss Race to the bottom mountain chains that generate new
of the Hellenic Trench, the deepest ocean crust—by identifying lava
part of the Mediterranean Sea, and The eight teams competing for the ocean mapping XPRIZE use a mix of flows. But scientists have fine-scale
map the sea floor with pinging pulses uncrewed surface vehicles and autonomous underwater vehicles (AUVs). maps for only a tiny fraction of the

of sound. The team behind the effort TEAM NAME COUNTRY SURFACE OPS NUMBER OF AUVS 65,000-kilometer-long system, limit-

is the first of eight competing over Arggonauts Germany Five ships Five ing their understanding of how new

CREDITS: (PHOTO) XPRIZE; (DATA) XPRIZE TEAMS the next few months in the finals of Blue Devil Ocean United States Two aerial Two crust forms and what happens to it as
the $7 million Shell Ocean Discovery Engineering drones 20 it moves away from the ridge.
XPRIZE. “I’m not sure if we are crazy
or not, but we decided to go first,” says CFIS Switzerland None Biologists also need better maps, to
manage fisheries and identify deep-

Rochelle Wigley, a marine geologist GEBCO-Nippon International One ship One sea habitats. They have already dis-

at the University of New Hampshire Foundation alumni covered new colonies of cold-water

in Durham, who leads the XPRIZE Kuroshio Japan One ship Two corals just by looking for structures
team of the Japanese Nippon Foun- PISCES Portugal rising from the sea floor, says Craig
dation and the General Bathymetric One ship, two One Brown, a mapping expert at Nova
Chart of the Oceans (GEBCO), an acoustic beacons Scotia Community College in Hali-

international organization. Team Tao United One ship Five fax, Canada. “They usually have quite
Kingdom dramatic topography,” he says.
XPRIZE, a nonprofit based in

Culver City, California, runs compe- Texas A&M United States One ship One So far, just 9% of the sea floor has

SCIENCE sciencemag.org Corrected 1 November 2018. See full text. 2 NOVEMBER 2018 • VOL 362 ISSUE 6414 507

Published by AAAS

NEWS | IN DEPTH

been mapped in detail with modern sonar from shore. Instead of sonar, they will use la- ENERGY

technology, Wigley says, and only 18% of the sers, which can bounce light off the sea floor Advances in
flow batteries
world’s ocean bottom has been surveyed at because they are at such close range. promise cheap
backup power
all, often at resolution so coarse that jumbo Team Tao will also use a swarm approach,
Upstart technology could
jets—and volcanoes—would have no trouble launching five custom-built AUVs from an enable widespread adoption
of renewables
hiding. The rest—four-fifths of the two- autonomous catamaran it calls the “vend-
By Robert F. Service
thirds of the planet covered by water—is ing machine.” Eventually, the system will
B atteries already power electronics,
virtually unknown. As usual, the limitations carry two dozen subsea drones, says team tools, and cars; soon, they could help
sustain the entire electric grid. With
are money and time. The research vessels leader Hua Khee Chan, an engineer at New- the rise of wind and solar power, en-
ergy companies are looking for ways
that do high-resolution mapping cost up to castle University in the United Kingdom, al- to keep electrons flowing when the
sun doesn’t shine and the wind ebbs. Giant
$100,000 a day to operate. And they move so lowing half to work while the others charge. devices called flow batteries, using tanks
of electrolytes capable of storing enough
slowly that it would take centuries for them Each AUV will follow a simple vertical path, electricity to power thousands of homes for
many hours, could be the answer. But most
to chart the world’s oceans, Virmani says. enabling it to sample the temperature and flow batteries rely on vanadium, a some-
what rare and expensive metal, and alterna-
Satellites can also map the sea floor, by salinity of the water column as it descends. tives are short-lived and toxic.

measuring slight variations in the ocean Chan says it’s “extra data that we get for free Last week, researchers reported over-
coming many of these drawbacks with a
surface caused by the gravitational pull of while it’s traveling.” Both Chan and Jackson potentially cheap, long-lived, and safe flow
battery. The work is part of a wave of ad-
massive seafloor features. But the resolu- say they aim to produce their AUVs for less vances generating optimism that a new
generation of flow batteries will soon serve
tion is crude. In recent years, researchers than $25,000 a pop—a bargain compared as a backstop for the deployment of wind
and solar power on a grand scale. “There
have turned to autonomous underwater ve- with the sophisticated models used today, is lots of progress in this field right now,”
says Ulrich Schubert, a chemist at Friedrich
hicles (AUVs). They follow preprogrammed which can cost $1 million or more. Schiller University in Jena, Germany. Downloaded from http://science.sciencemag.org/ on November 1, 2018

paths using inertial navigation systems that Cheaper, more flexible systems could help Lithium-ion batteries—the sort in laptops
and Teslas—have a head start in grid-scale
precisely track their speed and direction, researchers rapidly fill the gaps in seafloor applications. Lithium batteries already bank
backup power for hospitals, office parks,
and carry miniature multibeam sonars. By maps—and enable repeat surveys to moni- and even towns. But they don’t scale up well
to the larger sizes needed to provide backup
cruising close to the ocean bottom, they can tor changes over time. Clague would like to power for cities, says Michael Perry, asso-
ciate director for electrochemical energy
detect contours in the sea- measure how much lava is systems at United Technologies Research
Center in East Hartford, Connecticut.
bed smaller than a meter— “… you go into the produced during a single
eruption on a midocean That’s where flow batteries come in. They
a vast improvement over ridge, which gives clues store electrical charge in tanks of liquid
electrolyte that is pumped through elec-
the 50-meter resolution of ocean and things trodes to extract the electrons; the spent
electrolyte returns to the tank. When a so-
a typical ship-based system are not like math.” about magma generation lar panel or turbine provides electrons, the
working in the deep ocean, in the mantle. Repeat map- pumps push spent electrolyte back through
says Clague, who is not in- Nuno Cruz, University of Porto ping could also track move- the electrodes, where the electrolyte is re-
charged and returned to the holding tank
volved in the XPRIZE con- ment along offshore faults

test. But the AUVs are still slow. Efforts to that generate earthquakes, and in seafloor

add batteries and extend diving time only sediments after major weather events.

bulk up the AUV, requiring bigger ships to As XPRIZE’s sponsor, Shell reserves first

launch them, “which kind of defeats the rights to negotiate with each team for use of

purpose,” Clague says. its technology, which it could use for oil and

XPRIZE hopes its competition will spark gas exploration or to monitor production

faster, cheaper autonomous systems. Start- wells and pipelines. Companies hoping to

ing from shore, the eight finalists must map mine the sea floor for minerals are also eager

between 250 and 500 square kilometers in to get a better look. But Wigley says mapping

24 hours, at depths down to 4000 meters could also aid in marine protection. “If we

and resolutions of 5 meters or better. They understand the sea floor better, we can man-

must also carry instruments to collect im- age where it’s happening better and under-

ages of 10 interesting features and find a stand the impacts better.”

trophy stashed on the sea floor. The techni- For now, that’s a long way off, and most

cal challenges include building instruments teams are just scrambling to prepare for the

to withstand enormous pressure, balancing competition in Greece. A Portuguese team

battery life against speed, and making the still hasn’t tested its acoustic positioning

robots smart enough to carry out the whole system, which relies on a constellation of

operation without human guidance. “Every- floating beacons, in deep water. “From the

thing is hard,” says Martin Brooke, an engi- math, it should work,” says team leader

neer at Duke University in Durham, North Nuno Cruz, an engineer at the University

Carolina, and leader of its XPRIZE team. of Porto in Portugal. “But you go into the

Brooke’s group—mostly engineering ocean and things are not like math.” Some

students—will try to gain time by using teams already know they won’t win, but

heavy-lift aerial drones to carry buoys that they are fine with that. Most entered for

will lower tethered mapping pods into the the challenge, not the purse, and XPRIZE

ocean. Most teams use an autonomous is pleased with the progress they’ve made,

surface vessel to save their AUV’s precious Virmani says. “We’ve already shifted the

power and to serve as a communication hub. field.” j

The Swiss CFIS team, led by Toby Jackson,

a financial trader–turned–inventor, will send Julia Rosen is a journalist based in

20 lightweight, 3D-printed AUVs directly Portland, Oregon.

508 2 NOVEMBER 2018 • VOL 362 ISSUE 6414 Corrected 1 November 2018. See full text. sciencemag.org SCIENCE

Published by AAAS

(see graphic, right). Scaling up the batteries Tanked up Energy storage
to store more power simply requires bigger
tanks of electrolytes. Because flow batteries store charge in tanks of electrolytes, Energy
they can be scaled up as a backup source of grid power. A new generation
Vanadium has become a popular electro- design relies on ferrocyanide to capture and release electrons.
lyte component because the metal charges
and discharges reliably for thousands of +–
cycles. Rongke Power, in Dalian, China,
for example, is building the world’s larg- Ammonium
est vanadium flow battery, which should
come online in 2020. The battery will store Ferrocyanide Electrolyte Viologen derivative
800 megawatt-hours of energy, enough to reservoir
power thousands of homes. The market for During discharge, During charging,
flow batteries—led by vanadium cells and ferrocyanide Electrode electrons reverse course.
zinc-bromine, another variety—could grow (green) loses elec- Ammonium ions (center)
to nearly $1 billion annually over the next trons, which travel Circulation pump travel back and forth to Downloaded from http://science.sciencemag.org/ on November 1, 2018
5 years, according to the market research through a circuit to balance charges.
firm MarketsandMarkets. a viologen-based
electrolyte (orange).
But the price of vanadium has risen in
recent years, and experts worry that if va- Commercial flow batteries, such as this zinc-bromine system from Redflow, are helping back up renewables.
nadium demand skyrockets, prices will, too.
CREDITS: (PHOTO) REDFLOW LIMITED; (GRAPHIC) C. BICKEL/SCIENCE A leading alternative replaces vanadium ammonium that allows at least twice as It’s too early to say which flow battery
with organic compounds that also grab and much ferrocyanide to dissolve, doubling the chemistry—if any—will support the renew-
release electrons. Organic molecules can be battery’s capacity. The resulting battery is able grid of the future. Another contender
precisely tailored to meet designers’ needs, not as energy-dense as a vanadium flow bat- uses electrolytes made from metal-
says Tianbiao Liu, a flow battery expert at tery. But in last week’s issue of Joule, Liu and containing organic compounds called
Utah State University in Logan. But organ- his colleagues reported that their iron-based polyoxometalates, which store far more
ics tend to degrade and need replacement organic flow battery shows no signs of deg- energy in the same volume than the com-
after a few months, and some compounds radation after 1000 charge-discharge cycles, petition. In the 10 October issue of Nature
work only with powerful acidic or basic equivalent to about 3 years of operation. And Chemistry, for example, researchers led by
electrolytes that can eat away at the pumps because the electrolytes are neutral pH and Leroy Cronin, a chemist at the University of
and prove dangerous if their tanks leak. water-based, a leak likely wouldn’t produce Glasgow in the United Kingdom, reported
environmental damage. a polyoxometalate flow battery that stores
Researchers are now in the midst of “a up to 40 times as much charge as vana-
second wave of progress” in organic flow “Overall, that’s an excellent piece of dium cells of the same volume. The down-
batteries, Schubert says. In July, a group led work,” says Qing Wang, a materials scien- side for now is that these electrolytes are
by Harvard University materials scientist tist at the National University of Singapore. highly viscous and thus more challenging
Michael Aziz reported in Joule that they had Still, he and others caution that the battery to pump through the battery, Cronin says.
devised a long-lived organic molecule that is sluggish to charge and discharge. Liu “Today, no one flow battery fills all the
loses only 3% of its charge-carrying capac- says he and his colleagues plan to test other needs,” Schubert says. That means there’s
ity per year. Although that’s still not stable electrolyte additives, among other fixes, to still plenty of room for innovation. j
enough, it was a big jump from previous or- boost conductivity.
ganic flow cell batteries that lost a similar
amount every day, Liu says.

Iron, which is cheap and good at grab-
bing and giving up electrons, is another
promising alternative. A Portland, Oregon,
company called EES, for example, sells such
batteries. But EES’s batteries require elec-
trolytes operating at a pH between one and
four, with acidity similar to vinegar’s.

Now, Liu and his colleagues have come up
with a flow battery that operates at neutral
pH. They started with an iron-containing
electrolyte, ferrocyanide, that has been stud-
ied in the past. But in previous ferrocyanide
batteries, the electrolyte was dissolved in
water containing sodium or potassium salts,
which provide positively charged ions that
move through the cell to balance the electron
movement during charging and discharging.
Ferrocyanide isn’t very soluble in those salt
solutions, limiting the electrical storage ca-
pacity of the battery.

So Liu and his colleagues replaced the
salts with a nitrogen-based compound called

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Published by AAAS

Researchers distribute plastic bowls to collect fecal
samples from Hadza people near Lake Eyasi in Tanzania.

MICROBIOLOGY studied the microbiome of the Hadza, a tra- Downloaded from http://science.sciencemag.org/ on November 1, 2018
ditional people in Tanzania. “Keeping a bio-
Microbiome conservancy bank is already expecting that diversity loss
stores global fecal samples is an inevitable process,” she says.

Research could help prevent or treat diseases of the gut GMC’s biobank now houses about 11,000
strains, from about 40 people in seven
By Tania Rabesandratana ments not just for gut ailments, but for other countries. Its budget will support visits PHOTOS: CHRISTOPHER CORZETT
disorders linked to the microbiome—such until 2021 to about 34 countries in total—
W hether in villages on the coast as asthma, allergy, obesity, and diabetes. from the Arctic to Africa, Asia, Oceania, and
of Ghana or in the mountains of “I’m 100% confident that there are relevant South America. After that, organizers hope
Rwanda, asking for people’s poop medical applications for hundreds of strains to find several million dollars per year to
is a good icebreaker, Mathieu we’ve screened and characterized,” he says. expand the research and fund local science.
Groussin says. “Everybody laughs,”
says Groussin, a microbiologist at Gathering material from human subjects For now, the focus is on gathering strains.
the Massachusetts Institute of Technology and importing it to the United States for On collecting trips, Groussin retrieves the
(MIT) in Cambridge. “Especially when we posterity raises ethical and legal complica- filled plastic bowls the morning after
stress that we need the whole fecal sample tions, however. And the project itself repre- distributing them—or, in places with high
and show them the big bowl.” sents a pessimistic outlook, says Stephanie fiber diets, within the hour. He then pro-
Schnorr, a biological anthropologist at the cesses the samples in a makeshift lab in the
He’s asking on behalf of the Global Micro- University of Nevada in Las Vegas who has back of a car. Portions of the stool are fixed
biome Conservancy (GMC), an effort to iden- and dried for DNA sequencing and lipid
tify and preserve gut bacteria from different Stool samples are put into small tubes and content measurement. The rest is divided
peoples around the world. Most microbiome transported to the United States at –190°C. into small tubes, preserved in glycerol, and
research has focused on Western, urban pop- shipped back to Cambridge in containers at
ulations, which typically eat processed foods –190°C. There, bacterial strains are isolated,
and use antibiotics. The few studies of tradi- using growth media that mimic the condi-
tional peoples have found a far more diverse tions of the gut, and preserved in perpetuity
gut microbiome that appears to be linked to in large freezers.
the absence of certain diseases.
The team is already uncovering novel
But as traditional societies change their strains. The 7000 strains in GMC’s library
lifestyles, that biodiversity is under threat, that came from North American peoples in-
says Eric Alm, an MIT microbiologist who co- clude only five previously unknown genera.
founded GMC in 2016 with Groussin and two But the 4000 strains from Africa and the Arc-
other MIT postdocs. “Strains that coevolved tic have already yielded 55 unknown genera.
with humans are currently disappearing,” he
says. Later this month, Groussin plans to ex- Genomic data on the bacteria revealed
pand the growing conservatory with samples another contrast between populations. In
from Nigerian communities affected by oil September, at a human microbiome sym-
pollution near the Niger River delta. posium in Heidelberg, Germany, Groussin
said GMC found preliminary evidence that
Rescuing and preserving the microbes, so-called horizontal gene transfers between
Alm says, could pave the way for new treat- the strains living within one person are
frequent enough to change the gut micro-
biome’s function during a lifetime. These
gene transfers are more frequent in indus-
trialized populations, they found, possibly
as a result of higher environmental pres-
sures, such as antibiotic use.

Developing nations that have a history
of exploitation can be wary of the effort.
In Rwanda, for example, MIT researchers
worked with John Rusine, director of the
National Reference Library’s biology lab
in Kigali, to gain permission to transport
stool samples to the United States. Rusine
says he spent several months convincing
the library’s head to allow it. “Without his
signature, we couldn’t ship the samples out
of the country.” Each country keeps backup
samples, and GMC trained local technicians
to extract DNA. “Just keeping samples has
no meaning if there is no further research
here,” Rusine says.

510 2 NOVEMBER 2018 • VOL 362 ISSUE 6414 sciencemag.org SCIENCE

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One way to ensure broad buy-in is to store BIOMEDICINE
samples in a territory perceived as “neu-
tral, stable, safe, where their rights will be Llama antibodies inspire gene
respected,” says Maria Gloria Dominguez- spray to prevent all flus
Bello, a microbiologist at Rutgers University
in New Brunswick, New Jersey. Dominguez- Strategy for mutable virus might outdo traditional vaccines
Bello leads an initiative to build an inter-
national storage facility modeled after By Jon Cohen tein, hemagglutinin, from two other flu
the Svalbard Global Seed Vault, an under-
ground cold storage building on a remote strains. They then harvested four antibod-
Norwegian island that safeguards plant di-
versity for future generations. Just as in the F our llama antibodies and a harmless ies that each neutralized many flu strains.
seed vault, researchers, institutions, or gov- virus: This outlandish recipe could Ultimately, the team was able to engineer
ernments could make deposits in the mi- be the basis of a nasal spray designed a gene that expressed a protein made up of
crobiota vault, retrieve samples, and grant to foil infection from all strains of in- nanobodies derived from all four antibod-
others access to them. fluenza. The spray, containing a virus ies. “It’s very easy to link the domains to-

So far, the microbiota vault is just an engineered to make a protein derived gether into one single molecule,” Kolkman
idea, supported by a dozen volunteer sci-
entists; it has no planned home yet, and from the llama antibodies, has passed its says. They spliced the gene into a benign
Dominguez-Bello says she is seeking a few
hundred million dollars to endow the proj- first animal test, protecting mice from ev- adenovirus-associated virus (AAV) that’s Downloaded from http://science.sciencemag.org/ on November 1, 2018
ect and get it started.
ery known flu strain that infects humans, a used in gene therapy experiments.
Who owns the preserved microbiome
samples—and any scientific advances made research team reports on p. 598. Test tube studies showed the four-in-one
using them—remains a legal puzzle. Micro-
organisms do fall under the Convention on Although the strategy must go through antibody prevented infection by 60 differ-
Biological Diversity, a 1992 international
treaty ratified by all United Nations member more testing before human trials can begin, ent influenza viruses from both the type A
states except the United States. But it’s not
clear whether the convention applies to mi- researchers who have struggled to develop and B groups that infect people. “It’s been
crobes that come from the human body.
a “universal” vaccine against the highly quite hard to find an antibody that neu-
The treaty intends to ensure that any R&D
results or benefits arising from genetic re- mutable flu virus say it merits serious at- tralizes both A and B,” says Ian Wilson, a
sources are shared with the government or
community that provided them in the first tention. The nasal spray structural biologist at the
place. GMC is trying to abide by that spirit: In
each country it visits, it has drawn up agree- could prove a boon to the Scripps Research Institute
ments stipulating that the stool samples and
cultured bacteria strains remain the property elderly, who typically suffer in San Diego, California,
of individual donors, and can only be used for
noncommercial purposes. most from flu and get only who helped work out how

But the very idea of preserving cells for fu- weak protection from ex- the nanobodies bound to
ture studies can be problematic, Schnorr cau-
tions. For example, in her 2014 study of the isting vaccines. And unlike the virus.
Hadza, Schnorr used samples only in the ex-
act way her study’s consent forms described. traditional influenza vac- Mice given the synthetic
She is skeptical that consent can be meaning-
ful when scientists themselves don’t know cines, which are tailormade antibody—delivered either
what questions they may ask in the future.
each flu season to match by squirting the doctored
Kieran O’Doherty, a social scientist at the
University of Guelph in Canada who has the viruses in circulation, virus into their noses of
studied the ethics of microbiome research,
thinks scientists should do more than ar- it could be stockpiled as the mice or by infusing the
chive the diversity of the human micro-
biome; they should look for ways to pre- protection against a flu protein directly into their
serve it, by helping traditional peoples
retain their sovereignty and natural re- pandemic. “This is a great circulation—had signifi-
sources. O’Doherty compares biobanking to
small-scale efforts to fight climate change. story and shows the power cantly higher survival rates
“It’s a good idea to use different light bulbs
or drive a different car, but we need higher- of antibody engineering,” than untreated rodents
level political action,” he says. “To many
scientists that’s activism, and they’re not says immunologist Antonio A flu-fighting antibody targets four when injected with a variety
comfortable with that.” j
Lanzavecchia, a leading flu sites (colored areas) on the virus’s of influenza strains. Wilson,

vaccine researcher at the hemagglutinin surface protein. who has published more

Institute for Research in than 50 papers on influ-

Biomedicine in Bellinzona, Switzerland. enza antibodies, says he’s never seen one

Antibody engineer Joost Kolkman at Jans- with greater breadth and potency. Because

IMAGE: XUEYONG ZHU AND IAN WILSON, SCRIPPS RESEARCH INSTITUTE sen Infectious Diseases in Beerse, Belgium, AAVs can persist for months, the strategy

and his colleagues thought an unusual class could offer extended production. “Hope-

of antibodies made by llamas and their camel fully it would last the entire flu season in

cousins might serve as a weapon against flu. humans,” Wilson says.

These antibodies are unusually small be- Immunologist James Crowe, an influenza

cause they lack the “light” peptide chain that antibody specialist and vaccine developer at

normally bulks up each arm of the Y-shaped Vanderbilt University in Nashville, cautions

proteins. Researchers can further pare down that human immune systems may see the

the remaining “heavy” chains to create so- llama-derived proteins as foreign and de-

called nanobodies, able to reach into crevices velop antibodies against them. He also notes

of viruses that their full-size counterparts that although AAV-based treatments are be-

can’t touch (Science, 11 May, p. 594). ing tested for life-threatening diseases, giv-

To create nanobodies against the flu, the ing the virus as a flu preventive would face

Janssen group injected llamas with a vac- more intense scrutiny from regulators. “The

cine containing three different influenza bar for putting AAV in a healthy individual

viruses, as well as the viral surface pro- is going to be very high,” Crowe says. j

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Quantum computers made of superconducting
circuits could outperform classical computers.

PHYSICS quantum communication, among them an ef- Downloaded from http://science.sciencemag.org/ on November 1, 2018
fort to develop a blueprint for a quantum in-
Europe’s €1 billion quantum ternet. Two more will plunge into the race for
flagship announces grants quantum supremacy, which means executing
a specific algorithm that the best classical
Program aims to nudge quantum technology to market computers can’t handle.

By Edwin Cartlidge encryptions for banks and governments. Google aims to reach that milestone in PHOTO: IBM RESEARCH/FLICKR/CC BY-ND
Basic research in quantum mechanics has the coming months using quantum bits, or
T he first phase of Europe’s decadelong, qubits, made in superconducting circuits,
billion-euro program to turn its quan- flourished in Europe. But China is spending says John Martinis, the company’s head of
tum technology research into commer- billions to commercialize quantum technol- quantum hardware in Santa Barbara, Cali-
cial products has come into focus. At ogy, including a satellite to send quantum- fornia. Yet Thomas Monz of the University of
an event held in Vienna on 29 October, encrypted messages through space, launched Innsbruck in Austria, who coordinates one of
the European Union announced that in 2016—a first step toward a quantum inter- the European consortia, says his group’s bid
the first €132 million of its quantum flagship net. Meanwhile, the U.S. Congress is consid- for quantum supremacy, which uses trapped
initiative will be split between 20 continent- ering a $1.3 billion quantum initiative, and ions as qubits, is based on an algorithm that
wide consortia over the next 3 years to de- U.S. companies including Google, IBM, Intel, will be more “meaningful” than Google’s.
velop new kinds of quantum sensors, com- and Microsoft have already spent hundreds
munications, and computers. of millions of dollars to try to build a quan- A full-scale quantum computer is decades
tum computer that could outstrip conven- off, however. Among the consortia develop-
Backers hope the investment will keep Eu- tional machines on certain tasks. ing more tangible quantum devices are
rope from being overtaken in a potent new a Dutch-led group that intends to make a
area of technology. “It’s important to start an Such investment has been scarce in Eu- portable and easy-to-use optical clock that
applications sector to allow industry to grow rope, where companies without the huge could help telecom companies end their
in Europe,” says Ian Walmsley, of the Univer- cash reserves of U.S. tech firms have been re- dependence on potentially unreliable GPS
sity of Oxford in the United Kingdom, who luctant to take risks. The quantum flagship— signals. A group led by the Fraunhofer
is also a member of the steering group that the third EU flagship research program after Institute for Applied Solid State Physics in
formulated the flagship. “No doubt it’s grow- ones on graphene and the human brain—is Freiburg, Germany, is working on a room-
ing elsewhere in the world.” But it remains intended to compensate. Without such sup- temperature device to supply the spin-
uncertain how the rest of the flagship will be port, says flagship spokesperson Tommaso polarized molecules needed for magnetic
paid for, and whether it will inject life into a Calarco of the Jülich research center in Ger- resonance imaging machines.
fledgling European quantum industry. many, “the ideas that were developed and are
still being developed in Europe could be con- The grants amount to a fraction of the
Physicists have begun to find commercial verted into companies and jobs elsewhere.” initiative’s €1 billion commitment. Calarco
applications for the strange laws of quantum says the next funding round could combine
mechanics, which allow a subatomic particle The program was announced in 2016, and calls for fresh proposals with continued
to be in two states at the same time and a grant proposals from 140 consortia—each a support for existing projects. But the source
measurement on one particle to instantly af- mixture of academics and industrialists— of the money is in question. Funding is sup-
fect another, distant particle. For example, were received earlier this year, then whittled posed to be split 50-50 between the Euro-
Swiss company ID Quantique, set up in 2001, down to the 20 winners across five catego- pean Commission and member states, as in
sells equipment exploiting the quantum ries. Seven winners will pursue basic science other flagships. But in the quantum initia-
properties of photons to create uncrackable while many others will develop commercial tive, member states can spend their share
prototypes. Four of the projects focus on on national programs that merely share the
same aims. To avoid this, Calarco is hop-
ing that when the budget for the next EU
research framework is decided next year, it
will contain all of the remaining €850 mil-
lion the flagship needs.

An additional uncertainty is how Brexit—
the United Kingdom’s departure from the
European Union in 2019—will affect the
flagship. It could remove a key funding
source, although the United Kingdom could
strike a deal like Switzerland, which pays to
participate in EU research frameworks. But
Brexit’s effects on grantees will be delayed:
The U.K. groups in the winning consortia
will participate for the full 3-year initial pe-
riod. “We don’t know what form Brexit will
take,” Calarco says. “So we have 3 years to
sort this out.” j

Edwin Cartlidge is a journalist in Rome.

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CARDIOLOGY

Suspect science leads to pause in stem cell trial

Harvard University finds fraud in 31 papers, casting doubt on study rationale

By Jocelyn Kaiser fits from c-kit+ cells as a heart disease treat- Goff says that when the CONCERT-HF Downloaded from http://science.sciencemag.org/ on November 1, 2018
ment. Also in 2014, Harvard and Brigham trial was approved, reviewers were aware
IMAGE: SPL/SCIENCE SOURCE T he saga of one of the biggest scien- and Women’s revealed they had begun of concerns about Anversa’s work. But eight
tific fraud cases in the past decade a scientific misconduct investigation of other labs had published 11 studies support-
has reached a turning point. In mid- Anversa’s work (Science, 18 July 2014, ing the c-kit+ cell treatment in animal mod-
October, Harvard University officials p. 254). Anversa has blamed problematic els of heart disease. Scientists no longer
disclosed that they have called for papers on another lab member. He lost a think the cells engraft in the heart and dif-
the retraction of 31 papers from car- lawsuit claiming the investigation was mis- ferentiate into cardiac cells. Instead, many
diac researcher Piero Anversa, who ran a handled and left Harvard and Brigham and think the cells secrete some “paracrine fac-
Harvard Medical School lab studying the Women’s in 2015. Last year, Brigham and tor” that promotes heart tissue growth.
potential of stem cells to repair the heart. Women’s agreed to pay $10 million to settle
And this week, federal officials paused charges that Anversa and two colleagues Further concerns arose this month when
a related clinical study, explaining that fraudulently obtained federal funding. Harvard and Brigham and Women’s recom-
the pending retractions “have raised con- mended that 31 papers from the Anversa
cerns about the scientific foundations of The now-paused clinical trial explored using stem lab be retracted because they “included fal-
this trial.” cells to repair damage to the heart. sified and/or fabricated data.” (Harvard and
Brigham and Women’s also told Anversa in
Anversa’s research has long drawn con- The CONCERT-HF trial, led by cardio- a 3 October letter that he “committed re-
troversy. Some critics of his work say stud- logist Roberto Bolli of the University of Lou- search misconduct” in eight published or
ies like the now-halted trial should never isville in Kentucky, began to enroll patients submitted papers and a grant proposal, ac-
have started, given long-standing ques- with heart failure 3 years ago. The study is cording to The New York Times.) The news
tions about how—and whether—the cells testing four possible treatments: an injec- prompted NHLBI to convene the trial’s
Anversa studied might repair heart tissue. tion in the heart of c-kit+ cells derived from safety board, which recommended that
“The problem is that if you don’t know how a patient’s own heart tissue, a combination the study pause for a review. NHLBI also
something works, then you don’t really have of c-kit+ cells and mesenchymal stem cells expects to examine the list of 31 papers to
a road map of what to address to make it from the patient’s bone marrow, mesenchy- ensure the trial is scientifically sound “out
better,” says Deepak Srivastava, a pediatric mal stem cells alone, or a placebo. The trial of an abundance of caution,” Goff says.
cardiologist and president of the Gladstone has recruited 125 of a planned 144 partici-
Institutes in San Francisco, California. pants, Goff says. Blood stem cells and heart He could not say how long the review
tissue have been collected from 117 of them, will take, but promises it will be done “in
But other researchers defend the push and 90 have received treatment. No safety an expeditious manner,” particularly be-
into the clinic. Many labs other than the Har- issues related to the treatment have arisen, cause patients have donated tissue and
vard group contributed to the basic research but one person died after a heart biopsy await treatment. About half of patients
supporting the study, called CONCERT-HF, during early safety tests. with chronic heart failure die within
says David Goff, director of the Division 5 years of diagnosis, he notes.
of Cardiovascular Sciences at the National
Heart, Lung, and Blood Institute (NHLBI) Despite the cloud over Anversa’s re-
in Bethesda, Maryland. NHLBI, which search, some researchers think the trial
funds the study at several U.S. sites, is paus- should be completed. “There’s plenty of rea-
ing the trial to review it simply because “it’s son to believe that there’s still promise,” says
the prudent thing to do,” he says. cardiologist Christopher Granger of Duke
University in Durham, North Carolina. Bolli,
Anversa, formerly of Harvard Medical a longtime Anversa collaborator, points
School and Harvard-affiliated Brigham to “overwhelming evidence” from animal
and Women’s Hospital in Boston, rose to studies that c-kit+ cells somehow promote
prominence by showing that, contrary to heart tissue growth. “The controversy [over
the received wisdom, the heart can rapidly Anversa’s work] does not really change the
regenerate muscle. He also reported that validity of using c-kit+ cells,” Bolli says.
heart tissue contains stemlike cells known
as c-kit+ cells that can rejuvenate heart Another trial, based in Florida, planned
muscle in mice. If true, the cells could form to begin to treat infants born with a cer-
the basis of a treatment for heart failure, tain heart defect with c-kit+ cells this
caused by weakened heart muscle. month; the status of the trial was unclear
at press time.
But several labs could not replicate
Anversa’s work. One Anversa paper was Meanwhile, NHLBI hopes to clarify just
retracted in 2014, and a 2011 paper in The what c-kit+ cells do and how much promise
Lancet drew an “expression of concern” they hold. It is funding 14 preclinical grants
from the journal. That paper reported on a to study the cells, Goff says. j
small clinical trial that found modest bene-
With reporting by Jennifer Couzin-Frankel.

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FF EE AATT UU RR EE SS By Paul Voosen

MOMENTS TO SPARE he shaking woke Thomas Heaton
California’s new earthquake on a quiet winter morning in Pasa-
warning system delivers just seconds dena, California. The streets were
of notice. Even that is a victory empty, with sunrise hours away.
As Heaton lay in bed next to his
wife, waves vibrated through Downloaded from http://science.sciencemag.org/ on November 5, 2018
their house. Ten seconds. Fifteen.
ILLUSTRATION: ROBERTO CIGNA
T Twenty. As a seismologist, Heaton
514 2 NOVEMBER 2018 • VOL 362 ISSUE 6414 had spent his career studying seis-
mic waves like these. By feel and duration,
he guessed this quake was big, maybe a
magnitude 6.5, and close, under west Los
Angeles. Plenty dangerous. An aftershock
rolled through. He was needed. “I’ve got to
get to work,” he told his wife.

At the time, in 1994, Heaton was the lead
scientist at the earthquake field office of
the U.S. Geological Survey (USGS) in Pasa-
dena. He drove to the office in darkness,
imagining the fires, collapsed bridges, and
crumbled buildings closer to the epicenter.
At the office, seismic readings partially
validated his gut: “I was right about the
magnitude and approximate distance,” he
says—though not the location. The quake
had struck farther north, under the neigh-
borhood of Reseda, on a previously un-
known fault. The Northridge quake, as it
came to be known, killed 57 and caused
many billions of dollars in damage. There
had been no warning, no sirens sending
people into the streets. Heaton recalled
how he had guessed the size of the earth-
quake when the first, gentle waves reached
his bedroom. There must be a way, he
thought, to translate his gut check into a
short but useful warning.

After decades of work, Heaton’s dreams
have taken form. Last month, USGS un-
veiled ShakeAlert, the West Coast’s earth-
quake early warning system. If all goes as
planned, a dense network of seismometers
in California, Oregon, and Washington will
detect the first, weak waves of an earth-
quake and relay a rapid warning of ground
shaking to come. To start, those warnings
will go to first responders, power compa-
nies, and transit agencies. But in the next
couple of years, alerts could roll out to the
public to provide at least a few seconds
of warning. Not much time, but enough
to “drop, cover, and hold on,” says Doug
Given, a geophysicist in Pasadena who is
leading the USGS effort.

For years, ShakeAlert was an academic
side project of California seismologists,
especially the gravelly voiced Heaton, now
at the California Institute of Technology
(Caltech) in Pasadena, and Richard Allen,
his soft-spoken counterpart at the Univer-
sity of California (UC), Berkeley. They were
inspired by warning systems in Mexico,

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Japan, Taiwan, and Chile, among others, As a graduate student at Caltech he expe- that could save lives. And at the time it ap-

which emphasize detecting earthquakes at rienced his first earthquake, an aftershock peared poised for a breakthrough.

the source and warning distant cities be- of the San Fernando quake in 1971. Dur- At their most basic, earthquakes result

fore the seismic waves arrive. Many people ing that disaster, emergency workers took when the strain built up between two

thought such a system would be useless 3 hours to figure out where the heavy dam- locked chunks of Earth’s crust becomes

in fault-riddled California, where earth- age was. Seismologists were little help. too much to bear and the slabs of rock slip

quakes seem to erupt underfoot anywhere. Heaton had three children, so he took a past each other along a fault. The larger

But Heaton and Allen persevered, deploy- job with Exxon. He lasted less than a year, the slip area, the bigger the earthquake.

ing a pilot system in 2012. but while there he learned that Japan was As the rupture starts, it tosses off pressure

Now, politicians are offering their sup- already using early earthquake warnings (P) and shear (S) waves. P waves percuss

port. Last year, some $13 million in annual to shut down bullet trains. “At that point, the rock like a drumstick, traveling quickly

funding flowed in from the federal govern- I got very excited,” Heaton says in his through incompressible material. S waves,

ment, along with $10 million more for sen- Caltech office, where gas mains buckled by though more powerful, struggle through

sor upgrades; California kicked in another earthquakes serve as table stands. the rock because of their sashaying motion

$10 million. In his state-of-the-city speech He laid out his idea for a U.S. system in and lag well behind.

last year, Los Angeles Mayor Eric Garcetti a 1985 paper in Science. Because seismic The classical view had been that noth-

pledged: “By the end of 2018, we will de- waves travel far more slowly than electri- ing about the first waves from a rupture

ploy an earthquake early warning system cal signals, a “seismic computerized alert indicates how it will grow, reflecting an

to every corner of this city—in schools, at network” could detect an earthquake at inherently chaotic, unpredictable system.

businesses, even on your smartphone.” its source and relay a warning of ground But in the 1990s, lab-built models and Downloaded from http://science.sciencemag.org/ on November 5, 2018

This year’s version doesn’t quite mea- shaking to cities far from the epicenter. some data on actual earthquakes sug-

sure up to that promise. Only half of the Automated systems could act immediately gested that a nucleation phase—a brief

system’s 1675 seismic stations have been to prevent chemical spills, electrical fires, period of subtle slipping at the quake’s

installed. The technology to rapidly push and other catastrophes. Such a system start—could predict the size of the ensu-

alerts to mobile phones is not mature. And would do little to protect San Francisco ing rupture. If that were true, forecasting

the public has yet to be trained in the ultimate magnitude of an earth-

how to respond to such alerts, which quake from only a few seconds of P

are sure to include false alarms. “You’re not going to get much time. waves might be possible. That ability
The system’s scientific ambitions could power a potent early warning

have also been humbled. The sci- If it’s going to be dangerous, we won’t system—a possibility that Yutaka
entists developing ShakeAlert once Nakamura, an earthquake engineer
promised it could warn of strong, know that till the last seconds.” at a private company in Japan, had

violent shaking from a distant earth- Thomas Heaton, California Institute of Technology already begun to pursue to improve
quake far in advance. That pitch bullet train warnings.

stemmed especially from Allen, Hea- Allen and Kanamori built on

ton’s friendly rival, who believed the final from an earthquake like the one in 1906, Nakamura’s work in a 2003 Science paper.

magnitude of an earthquake was deter- which was centered near the city. But it In records from 53 California earthquakes,

mined by its first few seconds of rupture. could give minutes of warning for great the largest a magnitude 7.3, they found a

If so, the system could catch an earthquake quakes that start far from populated re- correlation between the time the initial P

rupturing on a remote section of the San gions. It was a simple model with many wave took to complete one cycle, called t,

Andreas fault and give Los Angeles 1 min- assumptions—including, critically, an im- and the resulting magnitude. That rela-

ute or more of warning of severe shaking. mediate detection of an earthquake’s mag- tionship became the core of an algorithm

But over 15 years of development, reality nitude. “We can do it in 10 years,” Heaton Allen developed called ElarmS. It led him

has intruded: Faults fracture in complex, promised anyone who asked. to argue, in a 2005 Nature paper, that

unpredictable ways. The current incarna- It took longer. But as he climbed the earthquakes are deterministic, their fate

tion of ShakeAlert might offer 10 seconds ranks at USGS, Heaton updated South- structured by their start, contrary to the

of warning for a severe event—if you’re ern California’s network of seismometers conventional wisdom. “That paper,” he

lucky, Heaton says. “We’re back to the sim- toward the always-connected compat- notes, “was very controversial.”

ple ideas and just making the engineering ibility needed for early warning. He also Heaton, though, doubted a chaotic sys-

part of this problem work,” he says. “We’re formed an alliance with Hiroo Kanamori, tem such as an earthquake would surren-

just trying to get it born.” a decorated Caltech seismologist. Oth- der its secrets to a simple equation. He

ers in the field had spent years fruitlessly recalled how his gut feeling and knowledge

THE SON OF A MATHEMATICIAN at Rutgers debating whether earthquakes can be of past events had called out the North-

University in New Brunswick, New Jersey, predicted. Kanamori saw a better use for ridge quake. He started to develop code to

Heaton, born in 1951, grew up on the stable seismologists’ talents: developing a warn- re-create that intuition. As with ElarmS,

ground of the East Coast. Dyslexia, which ing system for earthquakes already under- the code relied on P waves from the first

made molecular structures a jumble, way. By the early 2000s, Allen, then an few seconds of a quake. But instead of us-

pushed him out of chemistry into phys- ambitious postdoc, had joined their effort. ing t to leap to a final magnitude, the sys-

ics, but he didn’t find his calling in the Like Heaton, Allen was a transplant tem compared the features of the initial

Cold War tasks of the time, either. “They from stable terrain, namely, the United waves with those of past quakes to create a

had enough nuclear weapons to blow up Kingdom. He, too, came to Caltech dissat- digital gut check. Heaton called the project

the entire solar system and they didn’t isfied with sterile debates, in his case about Virtual Seismologist.

need any more,” he says. Instead he was Earth’s internal structure. Early warning, Despite the ongoing debate, USGS began

drawn to study Earth’s own convulsions. it seemed, was the rare scientific discipline to finance Heaton, Allen, and other teams

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to work on the algorithms that make up the ture Detector (FinDer), which updates its recorded within 25 kilometers of the hypo-

core of ShakeAlert. warnings as an earthquake progresses. center of earthquakes in the United States,

FinDer, despite its late start, proved vital Japan, and elsewhere showed that the small

WHEN A MAGNITUDE-9.1 EARTHQUAKE struck to showing that ShakeAlert could handle a and large quakes looked identical at the

70 kilometers off Japan on 11 March 2011, Tohoku-size strike. “And really, if we can’t start. The determinism of the nucleation

the country’s warning system was little do big earthquakes,” Heaton says, “we’re phase, it seemed, was a ghost.

help for people in the path of the torrential missing the point.” Meier and Heaton, along with Pablo

tsunami that swamped the coast; nearly Ampuero, another Caltech seismologist,

16,000 died. But the system did alert more A KLAXON SOUNDED eight times, followed have found that as an earthquake devel-

than 50 million people and halt bullet by an insistent robotic voice: “Earth- ops, it does drop a hint about its ultimate

trains and elevators in many regions be- quake. Earthquake.” Heaton, seated at his strength. In a database of 116 earthquakes

fore the shaking began. It also served as desk, had a map of Southern California on greater than magnitude 7 created by a for-

a wake-up call for U.S. researchers to push screen. A simulated earthquake had just mer postdoc, Lingling Ye, now at Sun Yat-

for their own system. “That was the tip- struck at the southern end of the state, by sen University in Guangzhou, China, they

ping point,” Allen says. the Salton Sea, with an estimated magni- found that once the rupture starts to slow,

At a 2-day emergency summit at UC tude of 7. The quake posed little threat to the median earthquake ends up no more

Berkeley a month later, the ShakeAlert team Pasadena, 250 kilometers to the north, and than doubling in strength. “At some point

won a $6.5 million commitment from the so ShakeAlert warned of only light shak- you see it slowing down, and then you know

Gordon and Betty Moore Foundation in Palo ing. But the rupture didn’t stop there, and after that it’s all downhill,” Ampuero says.

Alto, California, to build a prototype. USGS FinDer stayed on the case. A gray line be- Heaton believes that effect, which they call Downloaded from http://science.sciencemag.org/ on November 5, 2018

was sold, too, and agreed to run the system. gan to extend toward Los Angeles, as did weak rupture predictability, is the only

The funders accepted that ShakeAlert need expanding rings of yellow and red: the pattern they’ll be able to tease out. But it

not be perfect; the Japanese public had warning P waves and damaging S waves. emerges late and has little predictive value

appreciated the Tohoku warning despite “Now it’s getting closer,” Heaton said. “And for individual earthquakes. There’s no sign

its flaws. “They just had to make sure it bigger as it goes.” of a clear connecting thread from the start

worked reasonably well,” Hea- to the end of an earthquake.

ton says. And that meant solv- Faced with the mounting

ing the problems that Tohoku “After working on this for over a decade, here evidence that determinism
had exposed. isn’t holding up, Allen, too, is

Despite the warning’s suc- it was in action and I was on the receiving end.” settling for weak predictabil-
cess, it failed to alert Tokyo ity, something his own recent
residents, far south of the Richard Allen, University of California, Berkeley work has supported. That

quake, who were blindsided happens in science: Careers

when the ground began to shake. The prob- “Earthquake. Earthquake. Moderate are made by staking out either side of a

lem was that the system had located the shaking expected in 42 seconds,” the voice data-poor claim, and then a middle ground

earthquake to a single point. It then cal- warned. The estimated magnitude had emerges. Yet even though most seismo-

culated how the shaking at that point, the gone up to 7.8—a 16-fold leap in energy. logists now agree that the start of an earth-

hypocenter, would affect more distant loca- The rupture continued, and ShakeAlert quake does not determine its end, many

tions. For earthquakes of magnitude 6.5 or upped its warning again: “Strong shak- still think its early stages might somehow

smaller, which rupture for only a few sec- ing expected in 23 seconds. Earthquake. influence whether the rupture can grow by

onds, that approach is reasonable. But the Earthquake.” Finally, 7 seconds before jumping faults or sections of locked rock.

Tohoku fault rupture grew toward Tokyo, the damaging waves arrived, ShakeAlert The earthquake’s start may not drive all ac-

extending to some 400 kilometers over gave its final warning: “Very strong shak- tion, but it may still be a prologue that—in

more than 3 minutes. “One thing we did ing expected.” The klaxon fired rapidly. some way still not evident in the data—

not expect is that really long fault rupture,” And then silence. “You’re not going to get informs the rest of its story.

says Masumi Yamada, a seismologist at much time,” Heaton says. “If it’s going to be

Kyoto University in Japan who studied with dangerous, we won’t know that till the IN SEPTEMBER, while Allen was riding a Bay

Heaton. As a result, the alert under- last seconds.” Area Rapid Transit train near San Fran-

estimated the quake’s magnitude and extent. Heaton says he still wishes that some cisco, his rail car ground to a halt. The

The algorithms developed for ShakeAlert signal buried in the first moments of an conductor’s voice came on the intercom.

had the same shortcoming. “We realized re- earthquake could reveal more. But even A magnitude-3.3 quake had struck 40 kilo-

ally quickly that if there was a major earth- before Tohoku, the grand promise of pre- meters north of Berkeley, and the train

quake along the southern San Andreas dicting an earthquake’s final magnitude system, following protocol, had stopped

fault, we wouldn’t expect shaking in Los from its first moments had begun to fall for safety. “I can’t believe it: We have seen

Angeles because it was so far away,” says apart. In records for earthquakes with Yosemite, San Francisco, and now we have

Maren Böse, a seismologist at ETH Zurich magnitudes above 7, “We started see- been in an earthquake!” one family of tour-

in Switzerland who had also worked with ing a saturation effect,” says Gilead Wur- ists said. The unplanned stop delighted

Heaton. But while Yamada was at Caltech, man, one of Allen’s former students at UC Allen, too. “After working on this for over a

Heaton worked with her to develop a way to Berkeley. “You’d start to underestimate the decade, here it was in action and I was on

track the growth of a rupture in real time, magnitude.” the receiving end.”

by measuring the shaking along its path. Heaton’s recent work, conducted espe- Over the past year, Given has pushed the

Böse, Heaton, and others then refined that cially with Men-Andrin Meier, a seismol- ShakeAlert team to meld its unruly com-

technique. Virtual Seismologist yielded to ogy fellow at Caltech, has only solidified peting algorithms into a cohesive whole.

an algorithm called the Finite-Fault Rup- doubts. A 2016 comparison of P waves First, a fast-estimating code called EPIC—

516 2 NOVEMBER 2018 • VOL 362 ISSUE 6414 sciencemag.org SCIENCE

Published by AAAS

consisting primarily of Allen’s ElarmS— On the alert Washington
generates an initial magnitude, treating the
quake as a point source. But if EPIC sees ShakeAlert, the first U.S. earthquake early Oregon
a quake lasting more than a few seconds— warning system, went live in October. It detects
and therefore larger than magnitude 6.5— incipient earthquakes to provide seconds
FinDer takes the lead, tracking the rupture of warning to critical infrastructure and,
from there and updating the magnitude. eventually, the public. For now, the sensor
The refinements will continue. “It’s been network is densest in Southern California, but
kind of a closed club through this year,” it will expand into the Pacific Northwest.
Given says, but the agency is now soliciting
other researchers to improve the code. Installed seismic Cascadia subduction zone Idaho
stations In the Pacific Northwest, the
New technologies will sharpen the Stations needing biggest earthquake hazard Nevada Utah
warnings, too. GPS sensors, though slower upgrade comes from the plunging,
than seismometers, can capture even shak- offshore Cascadia fault.
ing strong enough to max out conventional Planned seismic
instruments, enabling the system to cope stations San Andreas fault
better with the biggest earthquakes. And The San Andreas fault
Heaton expects artificial intelligence, espe- ruptured most famously California Downloaded from http://science.sciencemag.org/ on November 5, 2018
cially neural networks, will in the next few in the 7.8-magnitude
years be able to discern P waves, an earth- San Francisco Arizona
quake’s first whisper, from seismic noise earthquake of 1906.
earlier than the existing algorithms. At
first, Heaton was skeptical of the technol- A race against time
ogy. “But then it dawned on me that this
other neural network was in many ways Warnings rely on fast detection of an earthquake’s first
more capable than this neural network,”
he says, pointing at his head. pressure (P) waves, which travel faster than the damaging Early warning
outpaces S waves
Any warning system is only as good as shear (S) waves that a quake also emits. After using Power
its messaging, and how ShakeAlert will
best reach the general public remains P waves to estimate an earthquake’s size Cities and
uncertain. “The technology for doing residential
rapid massive alerting doesn’t exist in and location, the system can relay centers
the United States,” Given says. The cellu-
lar messaging system that handles child electronic warnings ahead of
abduction or severe weather alerts wasn’t
designed to relay warnings in seconds— the oncoming S waves. Transit
more like minutes. Los Angeles will begin
to test an alternative, using notifica- Sensor station Fault
tions on a smartphone app, but the P wave
fear is that such a system could First P waves
easily overload. detected Earthquake
alert center
USGS has set one important
parameter: Instead of waiting un- Dilation Land Damaging
til a risk is severe, ShakeAlert will Compression surface S waves
skew toward more alerts, sounding
GRAPHIC: C. BICKEL/SCIENCE an alarm once a location is at risk of Fault Growing threat
“light shaking.” That will increase the
warning time—but it also will mean Rupture The P waves from an
that, if the rupture grows, the pre- surface earthquake’s nucleation
diction could change to severe shak- site only weakly predict
ing only seconds before hitting. And Nucleation its overall magnitude,
the public might grow complacent site which depends on the total
about those alarms and fail to re- area of rupture, or slip.
spond to the rare mild threat that, ShakeAlert will update its
in a moment, turns severe. warnings as an earthquake
propagates along a fault.
The faults riddling Heaton’s ad-
opted state guarantee that soon, Hypocenter
ShakeAlert will get its first high-
profile test. “It’s a little terrifying,”
he says. “The world will be watching.
Here’s your chance to sing in front of
everybody. You just hope you don’t—”
And Heaton’s gravelly voice broke into
a croak that echoed down the hall. j

SCIENCE sciencemag.org

Published by AAAS

INSIGHTS

PERSPECTIVES

C L I M AT E EASM and jet stream variations on rainfall Downloaded from http://science.sciencemag.org/ on November 1, 2018
patterns over China. Through examination
Shifting summer rains of trace elements in Chinese stalagmites (a
proxy for local precipitation amount) and
Trace-element records in Chinese caves reveal the climate modeling experiments, they show
effects of climate change on Asian monsoons that cooling episodes in the North Atlantic
shifted the summer jet stream south, delay-
By David McGee latitude jet stream, which appears to gov- ing the onset of monsoon rains in northeast- PHOTO: HUMPHERY/SHUTTERSTOCK
ern the monsoon’s northward march each ern China and increasing rainfall in central
M ost of China’s water supply de- spring and summer (1). To investigate the China. The finding demonstrates that local
pends on rainfall from the East monsoon’s sensitivity and dynamics, many rainfall in the EASM regions can vary in op-
Asian summer monsoon (EASM), scientists have turned to examining its past position to monsoon strength, and it high-
a seasonal progression of rains that changes recorded in natural archives. Al- lights the importance of future high-latitude
begins along the southern coast in though past climates are not a direct analog warming in determining precipitation pat-
spring, then sweeps north, reaching of the 21st-century climate, they offer vital terns in China.
northeastern China in midsummer (see the tests of the ability to describe monsoon be-
photo). Projections of the EASM’s response havior through theories and numerical mod- Central to investigations of the EASM’s
to future climate change are complicated els. On page 580 of this issue, Zhang et al. (2) history are records of the oxygen isotope
by its complex interaction with the mid- provide new insight into the impact of past
Department of Earth, Atmospheric, and Planetary Sciences,
Massachusetts Institute of Technology, Cambridge, MA, USA.
Email: [email protected]

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Published by AAAS

In south-central China, monsoon flooding typically d18O, weak monsoon intervals.

occurs in early summer before rains progress Zhang et al. investigate this tripole pattern

northward, as in this June 2016 flood in Jiujiang. with climate modeling experiments designed

to mimic changes in Northern Hemisphere

set by changes in the composition or frac- temperatures during the last deglaciation.

tion of water vapor transported into the The authors found precipitation changes

EASM region from India, where there is consistent with the tripole pattern that ap-

preferential rainout (removal from the at- pear to derive from the impact of high-

mosphere by precipitation) of water vapor latitude temperatures on the seasonal shifts

with heavy oxygen isotopes (5). In this in- of the jet stream (a narrow band of strong

terpretation, d18O records from Chinese sta- winds around 5 to 7 miles above Earth’s sur-

lagmites provide information about remote face that blow from west to east). In response

atmospheric circulation, but not rainfall to cooling of the Northern Hemisphere’s high

over China itself. latitudes in the model, the steeper pole-to-

Key to testing both interpretations are equator temperature gradient slows the jet

independent reconstructions of local rain- stream’s seasonal migration north of the

fall changes in the EASM region during Tibetan plateau, delaying the summertime

periods with high-amplitude oxygen iso- incursion of tropical moisture into northeast-

tope changes. Zhang et al. do precisely that ern China and increasing summer rainfall

and provide important support for a newly near the cave site in central China. Downloaded from http://science.sciencemag.org/ on November 1, 2018

emerging interpretive framework for the This finding of antiphased regional rain-

canonical Chinese cave records. The study fall patterns in China, and of the key role of

presents measurements of trace

impurities in the calcium car-

bonate lattice—substitutions of East Asian summer monsoon rainfall
magnesium and strontium for
calcium—in two stalagmites from In response to warmer high-latitude temperatures, an earlier
central China that span the tran- northward shift of the jet stream in summer (red arrows) draws more
sition from the peak of the last ice water vapor into northeastern China (blue arrow, blue ellipse)
and shortens the rainy season in central China (blue dashed ellipse).

age to the beginning of the cur-

rent interglacial period, between

21,000 and 10,000 years ago.

These trace-element variations

are interpreted to reflect changes

in the rate with which infiltrating

waters passed through the rock

above the cave, which should

track local precipitation. Oxygen

isotopes in these samples record

the same pronounced variations N
as other Chinese stalagmites

during the last deglaciation:

high d18O values during periods

composition of rainfall recorded in stalag- of abrupt cooling of the Northern Hemi- the jet stream’s position in producing them,
mites from Chinese caves (3). Because of
their precise chronological control, con- sphere, interpreted as representing a “weak makes several important contributions to
tinuous coverage of the last 640,000 years,
and high temporal resolution, these isotope monsoon” and/or low summer rainfall over our understanding of the past and future
records excel on the “x axis” (time) in ways
that are essentially unparalleled in paleo- the cave site, and low d18O values when the of the EASM. That local precipitation varies
climate research. A key limitation of these
records, however, is in the “y axis” (oxygen Northern Hemisphere warmed. in opposition to oxygen isotope values dem-
isotope ratio) because the interpretation
of oxygen isotope variations remains un- Surprisingly, the trace-element records onstrates that d18O values cannot be inter-
certain. It was initially argued that these
variations (expressed as the 18O/16O ratio, or from these stalagmites indicate rapid infil- preted simply as a proxy for the abundance
d18O) reflect changes in the contribution of
18O-depleted summer rains to total annual tration of waters during cold periods when of summer rainfall at this and other sites in
rainfall outside of the caves. This implies
that low d18O values mean more summer oxygen isotopes point to a “weak monsoon.” the EASM region. But it also appears incor-
rainfall at the cave site (4). At the opposite
extreme, others have argued that d18O val- The data suggest locally wet conditions at rect to conclude that oxygen isotope records
ues in EASM rainfall have no relationship
with local rainfall amounts and are instead these times, and dry conditions during low- have no relationship to local rainfall in

d18O “strong monsoon” intervals. Combining China and only reflect upstream processes:

this new record with other recent precipita- The data of Zhang et al. suggest that low-

tion reconstructions [e.g., (6)], Zhang et al. d18O intervals are marked by a consistent

GRAPHIC: N. DESAI/SCIENCE propose that strong monsoon intervals are pattern of higher precipitation in both the

marked by a tripole pattern of precipita- south and northeast of China, and reduced

tion anomalies consisting of drying in cen- precipitation in central China.

tral China and wet conditions to the south The results of Zhang et al. also demon-

and northeast. Opposite responses—drying strate the importance of current and future

in the northeast and south, and wet condi- warming of the Northern Hemisphere’s

tions in central China—occur during high- high latitudes for regional rainfall patterns

SCIENCE sciencemag.org 2 NOVEMBER 2018 • VOL 362 ISSUE 6414 519

Published by AAAS

INSIGHTS | PERSPECTIVES

in China (see the figure). The tripole pat- NEUROPHYSIOLOGY
tern evident in the paleoclimate data is very
similar to the spatial pattern of interannual Identifying posture cells
rainfall variability in China over recent de- in the brain
cades (7), suggesting the robustness of this
behavior across different climate states The parietal cortex represents body posture and other
and forcings (physical factors that affect factors in spatial awareness
climate). In isolation, the polar-amplified
Northern Hemisphere warming projected By Guifen Chen pects of the animal’s posture, that is, the Downloaded from http://science.sciencemag.org/ on November 1, 2018
over the coming decades would suggest that relative position of different parts of its
droughts in central China may be a consis- F or an animal to successfully feed, body, implying that these posture cells
tent feature of the 21st century. mate, and avoid danger, its brain could be one of the building blocks for co-
must integrate incoming information ordinate transformation in the brain.
Several mysteries remain for future inves- from many sensory modalities, com-
tigation, however. The relationship between bine the information with previously The parietal cortex has reciprocal con-
high-latitude temperatures, the jet stream’s stored knowledge about the world, nections to frontal motor areas as well as
seasonal shifts, and the EASM proposed by and then send appropriate output com- to almost all sensory areas in the mam-
Zhang et al. predicts that other processes mands to the muscles. The information malian brain (see the figure). It is thus ex-
that influence Earth’s pole-to-equator tem- in this process is highly spatial in nature, pected to play a role in multiple cognitive
perature gradients, including ice ages and but it is not anchored to any one coordi- functions such as multisensory integration,
changes in the tilt of Earth’s axis, should nate reference frame. For example, sensory movement planning, working memory,
have pronounced effects on the EASM. Yet, data from a fingertip tell the animal about and spatial navigation. Recordings from
oxygen isotope records from Chinese caves a point in space, but exactly which point in the parietal cortex of head-fixed monkeys
show almost no variability on the char- space depends on the position of the finger revealed cells sensitive to light at specific
acteristic time scales of ice age cycles or relative to the wrist and arm it is attached positions on the retina, with responses fur-
changes in axial tilt. Longer records will to, as well as on the actual location of the ther modulated by the position of the eyes,
be essential for testing whether the glacial- animal in the world. Similarly, for the in- position of the head, and even by limb posi-
interglacial variability in EASM rainfall ap- formation on the retina, the point depends tion (2–5). These experiments also revealed
parent in other paleoclimate records (8, 9) on depth of field, position of the eye within cells related to quick eye movement, grasp-
is also present in infiltration proxies in sta- the socket, position of the head relative ing, and reaching. Such complex responses
lagmites, but is somehow masked in oxygen to the body, and location of the animal in hinted that within the parietal cortex, some
isotope records. Indeed, the data of Zhang et the world. To integrate this highly spatial form of spatial transformation might occur
al. intriguingly suggest an overall reduction information, the brain needs to transform between the various reference frames of the
in rainfall in central China over the deglaci- between coordinate systems. On page 584 receptors (for example, eyes) and effectors
ation, a finding that requires further testing. of this issue, Mimica et al. (1) demonstrate (for example, hands) (6).
Recently developed infiltration proxies in- how the posterior parietal cortex (PPC) in
volving calcium and strontium isotopes (10, the brains of rats represents different as- Building on this, Mimica et al. recorded
11) offer valuable new tools for these efforts. single neurons from the PPC and frontal
In addition, modeling experiments that sep- motor cortex (M2) of freely moving rats
arate low- versus high-latitude influences
on the monsoon, and experiments directly Posture cells in the PPC-M2 network
simulating the oxygen isotope composi-
tion of rainfall (5, 12), will be necessary to Posture cells have been discovered in the PPC-M2 network. PPC neurons in rodents have reciprocal
fully unpack the processes driving monsoon connections to various cortical areas, including visual, auditory, primary somatosensory, and prefrontal cortices,
variations and to decode the foundational as well as the secondary motor and retrosplenial cortices, thus supporting a series of cognitive functions.
records of past climate changes preserved in
Chinese stalagmites. j Back posture Head posture

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ACKNOWLEDGMENTS
I thank G. Roe for helpful discussion and acknowledge funding
related to this topic from NSF EAR-1434138.

10.1126/science.aav5280

520 2 NOVEMBER 2018 • VOL 362 ISSUE 6414 sciencemag.org SCIENCE

Published by AAAS

while tracking reflective markers attached regions are then coupled to the superior N E U R O D E G E N E R AT I O N

to various parts of the rodent’s body. They colliculus, which contains cells tuned to, Cancer enzyme
affects
found that slightly more than half of the and likely driving, the rotational move- Parkinson’s
disease
populations in PPC and M2 were tuned to ment of the head in three-dimensional
New insights identify
postural features (including head, neck, space (11). This suggests that PPC-M2 net- a possible target for slowing
neurodegeneration
and back positions), with some of the cells work activity could be the driving force for
By Patrik Brundin1 and Richard Wyse2
responding to the conjunctive postures of the downstream postural changes. If that
P arkinson’s disease (PD) is a progres-
multiple body parts. The authors also dem- is the case, how do the postural signals in sive neurodegenerative disease char-
acterized by rigidity, tremor, and
onstrated that they could reliably decode the PPC and M2 become translated into slowness of movement, as well as a
wide range of debilitating nonmotor
the activity of the neuron population in rotation signals in the superior colliculus? symptoms (1). The neuropathology
is characterized by loss of midbrain dopa-
these regions so as to predict postures. A Where does the transformation happen, mine–producing neurons and the occur-
rence of intraneuronal protein aggregates,
posture signal of this kind and what is the nature of largely comprising the protein a-synuclein,
that are distributed widely throughout the
would be a key component feedback between the dif- nervous system. Current treatments are
focused on alleviating the impaired move-
of the transformation be- “The parietal cortex ferent regions? ment, and there is no therapy that slows
tween reference frames Further, can the posture PD progression. With almost 7 million pa-
tients worldwide, finding ways to prevent
because it would enable, has reciprocal cells support other complex
for example, conversion cognitive functions in the The addition of PAR (bottom) accelerates pathogenic
from a head-centered co- connections to… PPC, such as spatial mem- a-synuclein fibrillization.

ordinate frame to a body- almost all sensory ory and navigation? To per- Downloaded from http://science.sciencemag.org/ on November 1, 2018
form such functions, there
centered coordinate frame. must be a transformation

Previously, PPC cells in areas in the

rodents were shown to spe- mammalian brain.” from body-centric (egocen-
cifically encode simple lo- tric) to world-centric (allo-

comotion behaviors, such centric) coordinates, such

as left and right turns and forward runs (7); that information is expressed in a manner

and a more complex series of locomotion invariant to the animal’s location, and an-

behaviors, for example, running straight chored to the external environment. Allocen-

followed by a right turn (8). Responses of tric signals have been reliably observed in

these cells could be highly dependent on the the hippocampus, which is connected to the

given task, such as leftward movement in PPC via the retrosplenial cortex. And indeed,

a maze versus in an open field (9), or they cells in the PPC have been found to encode

could be related to working memory, for ex- not just egocentric body movements (left or

ample, remembering which of two paths to right turns), but also a direction signal ex-

choose when approaching a T junction to pressed in both egocentric and allocentric

reach a reward (10). However, it is possible reference frames (12). Thus, the transforma-

that in all of these cases, the animal was tion between egocentric and allocentric ref-

simply exhibiting very different postures at erence frames presumably happens in either

different points in the activity being under- the PPC or retrosplenial cortex (13, 14). But

taken, for example, turning its head to the how? And what role do PPC posture cells

right prior to making a right turn, or turn- play in the process? Future experiments will

ing in a very different manner during the be needed to reconcile the newly found pos-

maze task compared to the open-field task. ture cells in the PPC-M2 network by Mimica

Indeed, Mimica et al. disambiguated loco- et al. with previous work on the PPC in ro-

motion from posture and found posture to dents and primates, so as to establish how

be far more correlated with PPC cellular ac- these cells support the complex cognitive

tivity, thus providing a more consistent and functions of the PPC. j

PHOTOS: T. I. KAM ET AL. (2) simpler explanation for the phenomenon of REFERENCES AND NOTES
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10. C. D. Harvey et al., Nature 484, 62 (2012).
11. J.J.Wilson et al., Curr. Biol. 28, 1744 (2018).
12. A.A.Wilber et al., J. Neurosci. 34, 5431 (2014).
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rons precedes that in M2 neurons. These

ACKNOWLEDGMENTS

G.C. thanks D. Manson for helpful discussion and comments.

Neuroscience, Physiology and Pharmacology, University 10.1126/science.aav3819
College London, London, UK. Email: [email protected]

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INSIGHTS | PERSPECTIVES

long-term neurodegeneration in PD Vicious cycle of PARP activity in PD to the GLP1R agonist are no longer
and slow disease progression are vi- able to trigger the transformation
tal goals. On page 557 of this issue, PARP1 produces PAR, which accelerates the fibrillization of a-synuclein of neighboring supportive cells, a
Kam et al. (2) describe a new mo- and triggers parthanatos, a PARP-dependent form of cell death. This form of glial cell called astrocytes,
lecular pathway that could explain may contribute to the progressive neurodegeneration observed in PD. into a neurotoxic form (13). To-
why a-synuclein aggregates form in gether, one can potentially consider
Native a-synuclein

PD. Moreover, their findings sug- PAR and a-synuclein simultaneously targeting pathologi-

gest a pharmacological approach to interact cal a-synuclein toxicity by means of

slowing PD progression. Vicious Pathological Cell death by two dissimilar approaches: PARP
Kam et al. show that fibrillar ag- cycle a-synuclein parthanatos inhibition to reduce the assembly
of a-synuclein into toxic aggre-
gregates of a-synuclein created in fbrils NOS activation gates, and concomitant activation
a test tube can activate the DNA DNA damage of GLP1R to prevent microglia-me-
damage repair protein, poly(ADP- diated activation of astrocytes.
ribose) (PAR) polymerase-1 (PARP1), PARP1
which in turn triggers generation Therefore, in the future, combi-
of PAR. Even in a test tube, PAR di- ADP-ribose PAR nation therapies could be used in
rectly binds to and accelerates the clinical neuroprotection trials for
fibrillization of recombinant a-sy- Nicotinamide adenine Nicotinamide enhanced therapeutic gain beyond
nuclein into highly pathogenic fibrils using a single neuroprotective
dinucleotide (oxidized form)

(see the image), as part of a vicious agent. Clearly, further research is Downloaded from http://science.sciencemag.org/ on November 1, 2018

cycle (described by the authors as “forward- logical diseases—for example, Alzheimer’s needed to define the interrelationship be-

feeding”) (see the figure). When such a-sy- disease, stroke, traumatic brain injury, and tween PARP inhibitors and GLP1R agonists

nuclein fibrils are added to cell cultures or multiple sclerosis—and so PARP inhibitors in their capacities to dampen a-synuclein

injected into the brains of mice, they are have been suggested as potential therapeu- responses and to unravel whether their ef-

particularly potent at causing intracellular tics for these diseases (7, 8). fects are additive. In addition to these two

accumulation of a-synuclein and neuronal Several drugs are currently being re- approaches, several other strategies to tar-

death, via activation of nitric oxide synthase positioned as possible disease-modifying get a-synuclein pathology—for example, by

(NOS) and induction of DNA damage, which agents in PD (9). A coordinated drug- using immunotherapy against a-synuclein

activates PARP1. Kam et al. show that dele- repurposing initiative, the international aggregates and small molecules to prevent

tion of the PARP1 gene or pharmacological Linked Clinical Trials initiative, has over a-synuclein aggregation—are either al-

inhibition of PARP1 activity, both in cell cul- the past 6 years initiated many clinical ready in trials or about to enter the clinical

tures and mice, prevents a-synuclein aggre- trials aimed at disease modification (10). arena (14). Identification of clinically ef-

gates from propagating between neurons Since 2012, PARP inhibitors (such as olapa- fective neuroprotectants for PD has been a

and causing neuronal death by parthana- rib, ABT-888, BMN-673, rucaparib, and struggle for many years, but given the dis-

tos, which is PARP-dependent cell death, a niraparib) have been considered by this covery of several potentially relevant mo-

form of programmed cell death that differs initiative (11). Although there has been lecular disease mechanisms, hopeful times

from both apoptosis and necrosis (3). The great interest in PARP1 as a therapeutic lie ahead. j

authors also present evidence for increased target, concerns about possible safety and REFERENCES AND NOTES
PAR levels in the cerebrospinal fluid of PD tolerability issues, especially in conjunc-
patients as well as in the region containing tion with chronic treatment that would 1. W. Poewe et al., Nat. Rev. Dis. Primers. 3, 17013 (2017).
degenerating dopamine neurons. be necessary to treat PD, have previously 2. T.-I. Kam et al., Science 362, eaat8407 (2018).
weighed against moving into clinical trials. 3. S.A.Andrabi,T. M. Dawson,V. L. Dawson, Ann. N.Y.Acad.
PARP inhibitors have been developed as Notably, the study of Kam et al. suggests
chemotherapeutic agents and are currently that relatively low doses of PARP inhibitors Sci. 1147, 233 (2008).
used to treat several forms of cancer, in- might be sufficient to attenuate elevated 4. Y. Lee et al., Nat. Neurosci. 16, 1392 (2013).
cluding BRCA-mutated breast cancer, as PAR levels in the brain to achieve clinical 5. A. S. Mandir et al., Proc. Natl.Acad. Sci. U.S.A. 96, 5774
well as chronic lymphocytic leukemia. The benefit. Furthermore, target engagement
rationale for using a PARP inhibitor is that could be assessed by measuring PAR lev- (1999).
some cancer cells are particularly vulner- els in cerebrospinal fluid, which could help 6. S. Lehmann,A. C. Costa, I. Celardo, S. H.Y. Loh, L. M.
able to loss of PARP1 activity because they guide appropriate dosing.
rely heavily on the enzyme for DNA repair Martins, Cell Death Dis. 7, e2166 (2016).
and thus to maintain the ability to divide. The first trial to be completed under 7. N.A. Berger et al., Br.J. Pharmacol. 175, 192 (2018).
As a direct result of the current findings the Linked Clinical Trials initiative was 8. S. Martire, L. Mosca, M. d’Erme, Mech.Ageing Dev. 146–
by Kam et al., and supported by earlier published in 2017 and suggested that ex-
studies in neurotoxin-induced and genetic enatide, a glucagon-like peptide 1 receptor 148, 53 (2015).
9. D.Athauda,T. Foltynie, CNS Drugs 32, 747 (2018).
10. P. Brundin, R. K.Wyse, Eur.J. Neurosci. 10.1111/ejn.14175

(2018).
11. P. Brundin et al.,J. Parkinsons Dis. 3, 231 (2013).
12. D.Athauda et al., Lancet. 390, 1664 (2017).
13. S. P.Yun et al., Nat. Med. 24, 931 (2018).
14. P. Brundin, K. D. Dave,J. H. Kordower, Exp. Neurol. 298, 225

(2017).

animal models of PD (4–6), it should be (GLP1R) agonist used to treat type 2 dia- ACKNOWLEDGMENTS GRAPHIC: N. DESAI/SCIENCE
possible to consider PARP inhibitors for betes, slowed PD progression (12). Notably, P.B. has received commercial support as a consultant for
repurposing as potential neuroprotective several of the authors who contributed to Renovo Neural, Roche,Teva, Lundbeck A/S,AbbVie, Neuroderm,
therapeutics in PD patients. Parthanatos the study by Kam et al. recently reported Fujifilm Cellular Dynamics, Living Cell Technologies, ClearView
potentially also contributes to other neuro- that GLP1R agonism inhibits a-synuclein Healthcare, FCB Health, IOS Press Partners, and Capital
toxicity. They demonstrated that a GLP1R Technologies. P.B. has received commercial support from
1Van Andel Research Institute, Center for Neurodegenerative agonist reduces the activation of brain- Renovo, Roche,Teva, and Lundbeck A/S. P.B. has ownership
Science, 333 Bostwick Avenue NE, Grand Rapids, MI 49503, resident macrophages, called microglia, interests in Acousort AB, and P.B. and R.W. are on the steering
USA. 2The Cure Parkinson’s Trust, 120 Baker Street, London when they are exposed to a-synuclein ag- committee of the NILO-PD trial.
W1U 6TU, UK. Email: [email protected] gregates. Consequently, microglia exposed
10.1126/science.aav3986

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MICROBIOLOGY

Evolving a pathogen to be protective

The deadly fungus Candida albicans can be pushed to protect its mammalian host

By Christophe d’Enfert is critical for disseminated infections (3). of the yeast-to-hypha switch. None of these Downloaded from http://science.sciencemag.org/ on November 1, 2018
Yeasts contribute to C. albicans dissemina- mutations were observed in a collection of
T he yeast Candida albicans is a com- tion in the bloodstream and adhesion to 182 genome-sequenced C. albicans isolates,
ponent of the human oro-gastrointes- tissues, whereas the filamentous form con- including commensal isolates (5). Other loss-
tinal and genital microbiota where it tributes to tissue invasion and escape from of-function FLO8 mutations occurred rarely
can exist in a commensal state without phagocytic cells in the host immune system. and were never found at homozygosity, sug-
causing pathological infection. Yet, it It was shown previously that strains with gesting that they are not selected.
is one of the main fungal pathogens defects in the yeast-to-hypha transition have
of humans, responsible for superficial infec- an increased ability to colonize the GI tract A possible explanation for this paradox
tions as well as disseminated, often deadly, of antibiotic-treated mice (4). However, the lies in the additional observation by Tso et al.
infections (1). As the focus of recent research observation that serial passage of C. albi- that filamentation-defective variants are less
has been on understanding what makes cans in the GI tract of such mice leads to the fit than the wild type upon GI colonization of
C. albicans such a harmful pathogen, we mice that have not received antibiotics and
know little about the commensal state and
whether the interaction of C. albicans with Evolving a fungal pathogen into a beneficial commensal
the healthy human host has some recipro-
cally beneficial (mutualistic) components. Evolved C. albicans differ from their parental C. albicans isolates by their ability to colonize the GI tract in
Exploring this aspect has been hampered, the presence or absence of an intact microbiota, cause systemic infection, and induce trained immunity toward
in part, by the observation that most labora- other bacterial and fungal pathogens (shown by arrow thickness). This shift toward a mutualistic interaction
tory animals (including mice) are not natu- results from the loss of a virulence attribute—filamentation—as well as other changes, possibly of the cell wall.
ral hosts of C. albicans, and persistence of
C. albicans in the gastrointestinal (GI) tract C. albicans Macrophage
of these animals requires antibiotic-induced isolate
dysregulation of the microbiota (dysbio- Natural
sis). By contrast, when allowed to reach the killer cell
bloodstream, C. albicans behaves as a highly
virulent pathogen of mice. On page 589 of Trained immunity
this issue, Tso et al. (2) report how they have
taken advantage of this dichotomy in C. albi- GI colonization Dysbiosed GI colonization Disseminated infection
cans–mouse interactions to evolve this fun-
gal pathogen into a genuine commensal that Protection
protects the host from other pathogens and
might pave the way to a universal vaccine. Evolved Bacterial
C. albicans and fungal
Through serial passage of a C. albicans iso- pathogens
late in the GI tract of antibiotic-treated mice,
GRAPHIC: KELLIE HOLOSKI/SCIENCE Tso et al. obtained variants with increased emergence of hypha-defective variants with thus have an intact microbiota, such as in
fitness upon commensalism but decreased increased fitness for this compartment was healthy human hosts. Perhaps the filamen-
fitness upon blood-borne infection. Impor- unknown and is somewhat puzzling. tation program is required for establishing
tantly, colonization of the GI tract or injec- a commensal equilibrium with other com-
tion in the bloodstream of several of these C. albicans is primarily a commensal, and ponents of the microbiota, but this is disad-
variants protected mice against virulent C. its involvement in disease is occasional, with vantageous when the microbiota is reduced,
albicans but also protected them from infec- superficial infections resulting from local leading to the emergence of filamentation-
tion with the filamentous fungus Aspergillus dysbiosis and disseminated infections usually defective variants. One important conclusion
fumigatus and the bacterial pathogens Pseu- associated with broad-spectrum antibiotic is that C. albicans has exploited an attribute
domonas aeruginosa and Staphylococcus au- treatment, alteration of epithelial barriers, of commensalism for pathogenesis.
reus (see the figure). and induced or pathological immunosup-
pression. Notably, the ability of C. albicans to What could be the hypha-specific factors
One of the notable observations of Tso form hyphae is considered a hallmark of this that are important for C. albicans survival
et al. is that GI-tract evolved variants dis- species and is frequently used in clinics to dis- in the microbiota? Hypha-associated pro-
play defects in one of the key attributes of tinguish C. albicans from other yeast species. teins that are expressed predominantly
C. albicans virulence: the yeast-to-hypha Indeed, most C. albicans isolates form hy- during hyphal growth have various func-
transition. The reversible switch between phae, albeit with different efficiency. Hence, tions, including cell wall proteins that
the yeast and hyphal (filamentous) forms one would expect that, if hyphal forma- are involved in the interaction with host
tion is disadvantageous for commensalism, cells and proteins, the cytolytic peptide
Institut Pasteur, INRA, Unité Biologie et Pathogénicité this would have been lost during evolution. toxin candidalysin, and secreted aspartyl
Fongiques, 25 rue du Docteur Roux, Paris, France. Similarly, most of the variants obtained by proteases (3, 6). Moreover, hypha adopt
Email: [email protected] Tso et al. carry loss-of-function mutations a metabolism that differs from those of
in FLO8, a C. albicans gene that encodes a yeasts (7). Future research should elucidate
transcription factor key to the progression whether hyphal formation is indeed nec-

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INSIGHTS | PERSPECTIVES

essary for C. albicans commensalism in a INFECTIOUS DISEASE Downloaded from http://science.sciencemag.org/ on November 1, 2018
host with an intact microbiota and, in this
event, which of the above factors contrib- Sources of human viruses
ute to commensalism.
Machine learning predicts the hosts and vectors of RNA
Another key observation of Tso et al. is that viruses that can infect humans
priming of mice by the C. albicans variants
led to cross-protection against different fun- By Mark Woolhouse little of the basic biology of a new virus, it is PHOTO: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES, NATIONAL INSTITUTES OF HEALTH/SCIENCE SOURCE
gal and bacterial pathogens. This is rapidly now relatively straightforward to obtain its
established, independent of adaptative im- M ost emerging infectious diseases are genome sequence (6). The study of Babayan
munity, relatively short-lived, and requires caused by RNA viruses (1). Many of et al. suggests that sequence data can give
cytokine production. These are hallmarks these that are newly found in hu- us a rapid prediction of reservoir host type,
of “trained immunity,” a recently described mans have a natural mammal or whether the virus is vector-borne, and, if so,
property that allows enhanced innate im- bird reservoir; some are transmitted the vector type.
mune cell responses when pathogens are re- by arthropod vectors, such as mos-
encountered (8). Colonization of the GI tract quitos (2). If we do not know the reservoir Babayan et al. assembled a dataset of more
by C. albicans is known to protect against host and/or vector, it is harder to identify than 500 genomes of single-stranded RNA
subsequent injury and infection (9), and a individuals and populations at greatest risk viruses linked to information on known res-
role of the gut fungal microbiome (mycobi- of infection and to design an effective pub- ervoir and vector species. Their first analysis
ome) in shaping immunity has started to be lic health response. On page 577 of this issue, was based on the “phylogenetic neighbor-
unraveled (10, 11). Yet, the variants identified Babayan et al. (3) report their efforts to pre- hood,” a cluster of closely related viruses.
by Tso et al. showed increased cross-protec- dict the reservoir hosts and vectors of human This approach predicted vector-borne trans-
tion compared to the parental C. albicans RNA viruses by applying machine-learning mission with 95% accuracy but correctly pre-
isolate as well as C. albicans mutants defec- algorithms to virus genome sequence data. dicted the type of vector (mosquito, midge,
tive in the yeast-to-hypha switch. This sug- sandfly, or tick) and the reservoir host type
gests that passage through the gut has led More than 200 species of RNA virus are (as one of 11 broad taxonomic groups within
to changes, besides loss of filamentation, known to be capable of infecting humans, mammals and birds) only 67% and 58% of
that contribute to triggering trained immu- and two or three new species are discov- the time, respectively. These results reflect
nity. These changes may affect the fungal cell ered every year (2). Some of these, such as the ways in which these traits are distributed
wall. Indeed, b-glucans, the main component severe acute respiratory syndrome (SARS) among virus taxa. RNA viruses switch be-
of the cell wall skeleton, are strong induc- coronavirus (4), posed an immediate epi- tween hosts quite easily. By contrast, vector-
ers of trained immunity (12), and intestinal demic threat; others, such as mammalian borne transmission is a much more conserved
stimulation with mannans, the glycans that 2 bornavirus (5), remain restricted to small trait; few genera have both vector-borne and
decorate cell wall proteins, protects against numbers of cases. Although we may know non–vector-borne species, although there
disease susceptibility, yet in a manner that may be within-genus differences in the type
may be distinct from trained immunity (9). Usher Institute at Ashworth Laboratories, of vector used.
University of Edinburgh, Edinburgh EH9 3FL, UK.
Understanding the exact nature of these Email: [email protected] Babayan et al. then used machine learn-
changes represents a prerequisite to the de- ing to improve their predictions. More than
velopment of the universal vaccine that Tso
et al. propose based on the cross-protection
properties of the C. albicans variants. Even
though the prospects for a universal vaccine
might seem hypothetical, one could antici-
pate that further exploration of the mecha-
nisms by which the variants protect against
different fungal infections may lead to new
preventive approaches against these infec-
tions. Such approaches are greatly needed be-
cause fungal infections are responsible for up
to a million deaths per year worldwide, and
resistance to antifungals is rising (1, 13). j

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MERS (Middle East respiratory syndrome) genetic material in a sample) makes it con- PHYSICS Downloaded from http://science.sciencemag.org/ on November 1, 2018
coronavirus first emerged in 2012 and causes siderably more feasible (10).
severe acute respiratory illness. Disorder at
A collection of virus sequences from ani- the border
4000 genomic traits (such as amino acid bias mal reservoirs would be especially valuable
or codon pair bias) were deployed in training, if it could be used to predict whether a virus The photoinduced phase
optimization, and validation algorithms. This is capable of infecting humans, even before transition in vanadium
markedly improved the predictions of vector any human cases are detected (11). Babayan oxide involves ultrafast loss
type (to 91% accuracy) and host type (to 72% et al. did not look for predictors of human of coherence
accuracy). Although the genomic traits them- infectivity, and it is not clear whether their
selves show strong phylogenetic signals, this approach would predict preadaptation to By Andrea Cavalleri1,2
result suggests that they also contain infor- a potential new host as well as it predicts
mation not (or not easily) captured by analy- adaptation to an established reservoir host. H ow does an ensemble of closely
ses based on relatedness alone. packed atoms rearrange when a
More focused approaches may be solid undergoes a morphological
The algorithms can be used to predict un- needed. For example, a key determinant change? Do the atoms follow a com-
known natural reservoirs or vectors. For ex- of host range is cell receptor usage; host mon, synchronized path, or do they
ample, they predict that Bas-Congo tibrovirus switching has been linked to a virus gain- move independently into their new
is transmitted by midges from an artiodactyl ing cell entry via a phylogenetically con- positions? These elusively simple questions
(even-toed ungulates) reservoir and that two served host receptor (12). Cell receptor underpin many key problems in modern
species of ebolavirus—Bundibugyo and Taï usage also determines tissue tropism, and condensed-matter physics and also affect
Forest—have primate reservoirs. These as- this is associated in turn with both patho- fields as far removed as soft-matter re-
signations should be regarded as hypotheses genicity and transmissibility, two traits that search and biological sciences. On page 572
to be tested empirically. Some predictions are highly relevant to the level of threat to of this issue, Wall et al. (1) use the Linac
may be helpful in confirming or challenging human health. Predicting cell receptor us- Coherent Light Source x-ray free-electron
current understanding. For example, they age directly from virus genome sequences laser (2) to provide decisive new informa-
predict that Crimean-Congo hemorrhagic is beyond our current capabilities, but un- tion on the nature of a structural phase
fever virus is not vector-borne, although it is deniably the genome does contain the in-
thought to be transmitted by ticks. formation. As our knowledge of viral cell “…immediately after
receptors improves and the number and photoexcitation, different
Babayan et al. propose that their method- diversity of virus genome sequences accu- dimers become uncorrelated
ology could also be used for rapid assessment mulates, machine-learning approaches ap- at short distances…”
of emerging viruses of which we have no plied to protein-protein interactions (13)
prior knowledge [a scenario that the World may provide a way forward. transition. They study the time evolution
Health Organization calls “Disease X” (7)]. In of the monoclinic phase of crystalline va-
the early stages of a public health emergency, Currently, our ability to predict human nadium dioxide (VO ) after it is destabi-
knowledge of reservoir host and/or vector infectivity among RNA viruses is limited
species could be vital for effective outbreak to (mostly weak) ecological correlates (14), 2
management. In this situation, the stakes are and the value of massive investment in vi-
higher and greater caution is appropriate. It rus discovery and sequencing programs is lized with light (3–5). Previous studies have
is helpful that the in silico predictions are as- hotly debated (9, 15). This debate is timely, assumed that this photoinduced structural
signed a confidence level and that the next however, given that databases are grow- transition proceeds coherently, that is, as
best possibilities are identified: 95% confi- ing fast and analytical methods are evolv- a concerted structural rearrangement in
dence in a particular vector type is more use- ing rapidly. The study of Babayan et al. which all atoms move at once (6, 7). Wall
ful than 60% confidence in a choice of three is a valuable step forward and hopefully et al. turn this notion on its head and find
different host types. However, even if the res- presages further advances in our ability to a prompt increase in disorder immediately
ervoir host and/or vector are predicted with extract information of public health value after photoexcitation, long before the ma-
high confidence, the taxonomic resolution directly from virus genome sequences. j terial heats.
is currently insufficient; we need to identify
species rather than broadly defined “types” REFERENCES To understand the nature of the problem,
such as sandflies or rodents. Even then, em- it is helpful to recall the idea of crystal sym-
pirical confirmation would still be necessary. 1. S. S. Morse et al., Lancet 380, 1956 (2012). metry, which physicists define as a collec-
2. M. E.J.Woolhouse, L. Brierley, Sci. Data 5, 180017 (2018). tion of mathematical operations that leave
Could confidence and resolution of the 3. S.A. Babayan et al., Science 362, 577 (2018). a unit cell unchanged. For example, a cu-
predictions be improved in the future? 4. J. S. M. Peiris et al., Lancet 361, 1319 (2003). bic crystal is invariant against all rotations
Methodological advances may help; Ba- 5. B. Hoffman et al., N. Engl.J. Med. 373, 154 (2015).
bayan et al. found variation in the per- 6. M. E.J.Woolhouse et al., Sci.Transl. Med. 7, 307rv5 (2015). 1Department of Physics, University of Oxford, Oxford, UK. 2Max
formance of different machine-learning 7. World Health Organization, A Research and Development Planck Institute for the Structure and Dynamics of Matter,
algorithms. However, the key requirement Hamburg, Germany. Email: [email protected]
is for more and better-quality data, and Blueprint for Action to Prevent Epidemics (2018); www.
here there is much still to do. It is likely who.int/blueprint/en/.
that we currently know of only a small frac- 8. J. L. Geoghegan, E. C. Holmes, R. Soc. Open Biol. 7, 170189
tion of RNA viruses of mammals and birds (2017).
(8). Finding and sequencing this hidden 9. D. Carroll et al., Science 359, 872 (2018).
diversity of viruses would be an enormous 10. P. Simmonds et al., Nat. Rev. Microbiol. 15, 161 (2014).
undertaking (9), but the advent of metage- 11. G.T. Keusch et al., Sustaining Global Surveillance and
nomics (techniques for sequencing all the Response to Emerging Zoonotic Diseases (National
Academies Press, 2009).
12. M. E.J.Woolhouse,J. L.Ashworth, Biochemist 39, 8 (2017).
13. B. Kim et al., J. Bioinf. Comp. Biol. 15, 1650024 (2017).
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at right angles, because a cube is indistin- consider instead a situation in which the magnetic case of the figure if the spin di-
guishable if looked at from the top, from moments at each site do not necessarily rection and size are substituted with the
the bottom, or from any one of its sides. disappear when crossing T , but rather be- contracted or elongated bonds of different
Similarly, the cube is also invariant against amplitudes. The authors differentiated the
reflections about a number of planes, for ex- c two possibilities of a displacive and of an
ample, those that bisect the edges. However, order-disorder transition by measuring not
if a phase transition takes place that dis- come uncorrelated near the transition. That only the dynamical changes in the Bragg
torts the unit cell—for example, one of the is, the size and angle of a moment at one peaks after photoexcitation, but also those
edges becomes longer—the material loses a site do not influence the size and angles of x-ray photons scattered in the weak “halo”
subset of these symmetry elements. spins only a short distance away. Also in this between peaks. As the cations acquired
limit, which is that of an “order-disorder” the high-temperature symmetry, a large
A phase transition is in fact about ac- transition, the diffraction peak disap- increase in the diffuse scattering was also
quiring or losing elements of symmetry, pears when the transition temperature is detected, indicating an ultrafast order-
but how does this proceed microscopi- crossed (see the figure, bottom). Hence, disorder transition.
cally? Instead of the geometric parameters one cannot tell apart a displacive and an
of a unit cell, let us consider, for graphic order-disorder transition by looking at the The reason why this disordering happens
simplicity, a magnetic material in which Bragg scattering alone. However, in the so fast is that immediately after photo-
displacive case, the diffraction peak disap- excitation, different dimers become uncor-
pears because the individual spins are not related at short distances and start to move
independently. This loss of correlation is a
Symmetry changes can be in lockstep at all sites, or incoherent defining feature of the high-temperature Downloaded from http://science.sciencemag.org/ on November 1, 2018
state of VO , in which the frequency of
Two ways in which a phase transition can proceed are illustrated for an antiferromagnetic spin system and
its diffraction pattern (measured as angle u) as a function of temperature T. 2

Displacive transitions the molecular vibration is independent of
the wavelength at short length scales. A
The ordering of spins uniformly decreases at each site with increasing temperature in a cooperative fashion, and wavelength-independent frequency in a
difraction peaks simply decrease in intensity. chain of atoms implies that if a single bond
is “plucked” at one site in the crystal, no
T sound wave is launched, but the vibration
remains localized. Thus, photoexcited low-
Order-disorder transitions temperature VO acquires the essence of the

The decrease in spin order occurs independently at each site. Difraction peaks decrease in amplitude with 2
temperature, but x-rays are also refected incoherently into a difuse background.
high-temperature phase, that is, nonpropa-
T gating short-wavelength sound waves, even
before the atoms have had time to rear-
spin moments point either up or down at there to scatter the light, whereas in the range completely. A photoinduced structur-
neighboring sites. The classical theory of order-disorder case, it disappears because al transition is then not only about atomic
phase transitions is based on a so-called of a lack of constructive interference at the positions, but also about their oscillation
mean-field approach. It is assumed that Bragg angle. In the order-disorder case, frequencies and correlation lengths.
fluctuations of local order occur uniformly the x-rays are still scattered by the nonzero
over long length scales. It follows that the local moments, but in a more incoherent The most important implication of these
order must be finite everywhere below the manner to other diffraction angles. measurements is that the much-publicized
transition temperature T and zero every- molecular movie, the idea that atomic po-
In the VO structural transition discussed sitions as a function of time provide a com-
c 2 plete picture of the microscopic physics,
becomes a slippery concept of limited va-
where above it. In this view, x-ray diffrac- by Wall et al., the increase in symmetry lidity. The experiments reported here show
tion from an antiferromagnet would show between the low- and high-temperature the crucial importance of diffuse and in-
a diffraction peak for all temperatures phases involves the disappearance of V4+ elastic x-ray scattering in dynamical expe-
below T and no peak for all temperatures dimers, which in the low-temperature riments. No transition can be understood
phase are arranged in chains with alter- without a complete measurement of elastic
c nate elongated and contracted bonds. and inelastic components of the scattered
Such an antiferrodistortive transition can signal. More generally, the work of Wall et
above it (see the figure, top). This type of be thought of in the same terms as the al. shows that x-ray free-electron lasers are
transition is termed “displacive.” opening up far more avenues of research
than what was envisaged when these light
However, let us relax the constraint on sources were being planned, forcing us
the correlation length of the order and to reevaluate many old notions taken for
granted up until now. j

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1. S.Wall et al., Science 362, 572 (2018).
2. P. Emma et al., Nat. Photon. 4, 641 (2010).
3. A. Cavalleri et al., Phys. Rev. Lett. 87, 237401 (2001).
4. V. R. Morrison et al., Science 346, 445 (2014).
5. P. Baum et al., Science 318, 788 (2007).
6. A. Cavalleri et al., Phys. Rev. B 70, 161102 (2004).
7. C. Kübler et al., Phys. Rev. Lett. 99, 116401 (2007).

10.1126/science.aav2019

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POLICY FORUM deemed current ecological risk-assessment
frameworks as adequate to predict poten-
TECHNOLOGY GOVERNANCE tial ecological impacts of gene-drive release
but recommended new guidelines to safe-
Editing nature: Local roots guard gene-drive research and encourage
of global governance public discourse (4). In fact, several na-
tional and regional reports echo in their
Environmental gene editing demands collective oversight calls for improved fora that can support
meaningful public debate (7, 8); however,
By Natalie Kofler, James P. Collins, Jennifer Kuzma, Emma Marris, Kevin Esvelt, most frameworks for regulatory decision-
Michael Paul Nelson, Andrew Newhouse, Lynn J. Rothschild, Vivian S. Vigliotti, making continue to largely preference sci-
Misha Semenov, Rowan Jacobsen, James E. Dahlman, Shannon Prince, ence-based knowledge and technical risk
Adalgisa Caccone, Timothy Brown, Oswald J. Schmitz assessments over ethical and societal con-
siderations. At the international level, the
T he end of malaria. Restored island hab- potentially reach every member of a species. Convention on Biological Diversity (CBD) Downloaded from http://science.sciencemag.org/ on November 5, 2018
itats. Resiliency for species threatened Villages in Burkina Faso are weighing the re- has enlisted an expert technical panel to,
by climate change. Many envisioned lease of gene drive–bearing mosquitoes that in part, update its Cartagena Protocol (of
environmental applications of newly could suppress malaria. Nantucket Island which the United States is not a party) that
developed gene-editing techniques residents in the United States are consider- oversees transboundary transport of living
such as CRISPR might provide pro- ing the release of genetically engineered modified organisms to accommodate gene
found benefits for ecosystems and society. white-footed mice to deplete Lyme disease drive–bearing organisms (9). The Interna-
But depending on the type and scale of the reservoirs. New Zealand communities are tional Union for the Conservation of Nature
edit, gene-edited organisms intentionally discussing the possibility of using genetic (IUCN) is also developing policy to address
released into the environment could also methods to eliminate exotic predators. the release of gene-edited organisms (3).
deliver off-target mutations, evolutionary Although the CBD and the IUCN offer fora
resistance, ecological disturbance, and ex- But what if a gene drive designed to sup- to engage diverse public feedback, a role
tinctions. Hence, there are ongoing conver- press an invasive species escaped its release largely fulfilled by civil society groups, none
sations about the responsible application of site and spread to a native population? Or if of these agencies currently use the broad
CRISPR, especially relative to the limitations a coral species gene edited to better adapt to and open deliberative process we advocate.
of current global governance structures to environmental stressors dominated reef eco-
safeguard its use [(1, 2); see table S1]. Largely systems at the expense of a diversity of natu- In the absence of widely agreed-upon
missing from these conversations is attention rally evolving coral species and the fish that governance guidelines or support for more
to local communities in decision-making. depend on them (see the photo)? The gravity optimal deliberative processes, the develop-
Most policy discussions are instead occurring of these potential outcomes begs the ques- ers of a technology seeking consent to re-
at the national or international level (3, 4), tion: Should humans even be meddling with lease a gene-edited organism may also serve
even though local communities will be the the DNA of wild organisms? The absence of as a community’s source of expertise and
first to feel the context-dependent impacts of generally agreed on answers can be used to information (10, 11). Such an advice-and-
any release. To be fully representative, there- support calls for moratoria on developing consent relationship raises the possibility of
fore, local inputs and perspectives must also and releasing genetically altered organisms, a real or apparent conflict of interest. Ide-
be considered. As laboratories around the especially those with gene drives (6). ally, in these cases, governance plans should
world develop and perfect gene-editing tech- incorporate expertise and perspectives that
niques with unprecedented capacity to alter However, the promising benefits of envi- are independent, transparent, inclusive,
wild species and, by extension, the ecological ronmental gene editing cannot be dismissed and based on balanced deliberations.
and cultural systems of which they are a part, (4). Gene drives may provide a long-sought-
we outline our vision for locally based, glob- after tool to control vectors of infectious Each decision to release a gene-edited or-
ally informed governance. disease and save millions of human lives. ganism has specific considerations that de-
Projects to conserve ecosystems or promote pend on the organism altered, the scope and
GENETICALLY ENGINEERING NATURE species resilience are often intended to repair intent of the alteration, the ecosystem(s)
CRISPR gene editing and other related ge- human-inflicted environmental damage. Put affected, consequences for human health,
netic technologies are groundbreaking in simply, either using this technology irrespon- and the value systems of communities af-
their ability to precisely and inexpensively sibly or not using it at all could prove damag- fected by such a decision. Underlying all of
alter the genome of any species (5). CRISPR- ing to humans, our welfare, and our planet. this are differing views about what is con-
based gene drives hold particular import sidered “natural” and to what degree hu-
because they are designed to rapidly spread National, regional, and international gov- mans should intervene in ecosystems (12).
genetic changes—including detrimental ernmental agencies are working to clarify Different societal views about the human
traits such as infertility—through popula- how existing research policy, field-testing relationship to nature will therefore shape
tions of sexually reproducing organisms, to frameworks, and risk-assessment guide- decision-making. Local community knowl-
lines apply to environmental gene editing, edge and perspectives must therefore be en-
See supplementary materials for author affiliations. enacting some existing rules, and seeking gaged to address these context-dependent,
Email: [email protected] to update and create new policies to ad- value-based considerations.
dress this technology. For example, the U.S.
National Academies of Sciences, Engineer- A special emphasis on local communities is
ing, and Medicine’s report on gene drives also a matter of justice because the first and
most closely affected individuals deserve a
strong voice in the decision-making process.
This is additionally a matter of urgency. Com-
munities, technologists, and governments

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INSIGHTS | POLICY FORUM

will require methods to make responsible those who have previously been overlooked; tors would also strive to cultivate certain vir-
and informed decisions about environmental deliberative procedures should build on tues in participants. These decisions involve
applications to keep pace with rapid progress frameworks demonstrated to promote inclu- complexity and uncertainty and are moti-
in gene-editing technologies. sive and democratic deliberation (14, 15). vated by concern for both human and non-
human well-being; thus, deliberants must
Compounding this challenge is that these The needs of ecosystems could also be be encouraged to think in interdisciplinary
decisions cannot be made in isolation. Or- given voice to inform deliberative out- ways, act with humility, and be mindful of
ganisms released into local environments comes through custodial human proxies. their membership in an interdependent,
may cross regional and even international Inspired by legislative precedent set by planetary community. To incentivize virtue-
borders. Hence, respect for and consider- New Zealand, in which the Whanganui based participation, the coordinating body
ation of local knowledge and value systems River was granted legal “personhood,” hu- must function in a manner that upholds ex-
are necessary, but insufficient, to anticipate man representatives, nominated by both treme transparency and trustworthiness with
the potentially ramifying global implications an international body like the IUCN and deliberative outcomes that carry authority.
of environmental release of gene-edited or- the local community, would be responsible Accordingly, an outright refusal to either par-
ganisms. What is needed is an approach that for upholding the health and interests of ticipate in or heed the outcomes of the delib-
places great weight on local perspectives the ecosystems in question (16). Proposed erative process could mark certain agents as
within a larger global vision. gene-editing strategies would be placed untrustworthy, an outcome likely not in line
in the larger context of alternative ap- with their strategy for long-term success.
INTEGRATED DELIBERATION proaches to address the public health or
We propose a coordinating body that can environmental issue in question. Each deliberative process would yield a
convene communities, technology develop-
ers, and governmental and nongovernmental Coral reef ecosystems are estimated to support over 25% of all marine fish worldwide and to contribute over Downloaded from http://science.sciencemag.org/ on November 5, 2018
organizations in ways that ensure inclusive US$1 trillion in economic, social, and cultural value globally. CRISPR-based strategies have been proposed as
deliberations. Such a body would serve as a a means to protect coral from bleaching. Corals genetically engineered to be more resilient to heat stress and ocean
neutral third party to help inform decision- acidification could be used to help conserve the Great Barrier Reef (shown above), a UNESCO world heritage site.
making that is free from conflicts of interest
and locally based. This organization would (i) To promote equitable representation, neu- standardized report that summarizes con- PHOTO: DANIELA DIRSCHERL/GETTY IMAGES
establish a deliberation framework that inte- tral and informed facilitators would bring cerns raised, areas where consensus was
grates diverse expertise and worldviews, in- history to the table, reveal existing power reached, and recommendations as to whether
cluding participants that represent impacted structures, and foster relationships be- or how a gene-edited organism should be de-
communities; (ii) facilitate deliberation to tween groups that hold disparate ideological veloped for environmental release. Reports
produce standardized reports and deliver stances. Deliberants would be encouraged to could also accommodate a recommendation
recommendations; (iii) establish informa- observe and reflect on their values—how they of “maybe, but not yet” and stipulate ecologi-
tion-sharing protocols to connect delibera- value nature, how they perceive risk, their cal, technical, and ethical considerations that
tions around the world; and (iv) report on level of trust in technology, and their motives require further study, reflection, and consid-
the outcomes of deliberation to inform global and agendas—with full transparency. Ques- eration. Ultimate control over the delibera-
governance of gene editing. tioning what is “natural” and to what degree tive process would be shared by nominated
ecosystems should be restored will also re- local leaders, but the coordinating body
Characterizing what defines an affected quire exploration to ensure an appropriate would provide frameworks for deliberation
“local” community will be an important part ethical basis for decision-making. and provide support throughout the process.
of this process and will depend on the nature
of the technology and how it is predicted to In following with recent proposals for To allow deliberative outcomes to have
interact with the environment. For example, more meaningful deliberation over socially immediacy, while not being encumbered by
if a self-propagating gene drive is under de- complex environmental issues (17), facilita- what will likely be a long-drawn-out process
liberation to counter malaria transmission,
then representatives from much of sub-Saha-
ran Africa would deserve a voice. For cases
where a technology is more limited in scope
or designed to have more limited spread, pre-
dictive models could be used to define the
communities most likely to be affected and
relative riskiness of the alteration. In line
with frameworks for responsible innovation,
evaluation would ideally begin as early as
possible, so that deliberation shapes the de-
velopment of the application in question (13).

The integrated deliberation framework
must incorporate expertise from fields such
as genetics, philosophy, ecology, economics,
law, and risk assessment, as well as repre-
sentatives of diverse stakeholder groups, and
members of affected communities. Histori-
cally marginalized voices (indigenous com-
munities, ethnic minorities, women, and
children) must be included. Network analy-
sis could identify affected parties, especially

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to update national and international regu- ments to deliberative design. Organizational gene-editing governance on a global scale. Downloaded from http://science.sciencemag.org/ on November 5, 2018
latory policy, a certification model for inte- procedures could be built on models used by
grated deliberation could be one way to lend existing international organizations. For ex- The success of this approach will depend
immediate authority and impact. In this vein, ample, the Intergovernmental Science-Policy
any project that successfully passes through Platform on Biodiversity and Ecosystem Ser- on inputs and expertise from diverse world-
the deliberative framework could be given vices has developed protocols to integrate
a seal of completion to alert regulatory bod- normative inputs into science-based policy views and disciplines. Important questions
ies and the general public that informed and (18), and effective measures for global coordi-
inclusive deliberation steered the develop- nation of diverse stakeholders and expertise remain to be answered: How can delibera-
ment of that specific technological applica- could be garnered from the IUCN.
tion. This is not to deny that new regulatory tive procedures effectively weigh local ben-
policies need to be in place to cope with Second, an online registry for all projects
this technology, but a certification approach intending to release genetically engineered efits with more-widespread global risks?
could address concerns about environmental organisms into the environment must be
applications in a timely way, while providing created. Currently, no central database ex- How would transfer of control for the de-
incentive for developers to participate. ists for environmental gene-editing appli-
cations or for decision-making outcomes liberations to local leaders take place? What
FROM VISION TO ACTION associated with their deployment, and this
Our proposed environmental gene edit- potentially puts the global community at structures are in place to guarantee histori-
ing coordinating body could be jointly risk. Third, a communications task force
supported by several intergovernmental needs to create an online space that allows cally marginalized voices are heeded in de-
organizations. Similar to how the Intergov- communities, technology developers, and
ernmental Panel on Climate Change falls policy-makers from around the world to liberation? What institutional procedures
under the joint sponsorship of the World share information resources, discuss issues
Meteorological Organization and the United faced, and provide expertise. The communi- and evaluation mechanisms are needed to
Nations Environment Programme (UNEP), cations team would also oversee an annual
this new initiative could receive shared sup- summit and the publication of annual re- ensure accountability? Through the collec-
port from several concerned organizations, ports to share lessons learned and promote
such as the World Health Organization tive creation of this new governance model,
(WHO), UNEP, or the IUCN. Falling under “Put simply, either using this
the auspices of existing intergovernmental technology irresponsibly the first that proposes a connection be-
organizations would serve to hasten the or not using it at all could
development of the coordinating body, so prove damaging...” tween local needs and global frameworks
it can meet the rapid development of gene-
editing technologies. Joint support would continued conversation on concerns raised. and expertise, our world may realize this
also lend immediate accountability and au- Finally, leveraging the experience and
thority, while ensuring that environmental technology’s most profound benefit—the
and human health concerns are equally up- infrastructure of its support organiza-
held in deliberative procedures. tions (for example, perhaps the WHO and opportunity to inspire a more healthy and
UNEP), a global coordination task force
A trust fund built on contributions by would be charged with coordinating mul- just future for all who share our planet. j
concerned governments, nongovernmen- tiple communities, nations, and regions to
tal organizations, and intergovernmental ensure successful deliberative outcomes. As REFERENCES AND NOTES
organizations and managed in a manner a hypothetical example, genetic strategies 1. S.Jasanoff,J. B. Hurlbut, Nature 555, 435 (2018).
consistent with International Public Sec- to eliminate invasive possums from New 2. L. Montoliu et al., CRISPR J. 1, 128 (2018).
tor Accounting Standards could provide Zealand must include representatives from 3. IUCN, Development of an IUCN policy on synthetic
financial support. Our hope is that govern- Australia, the country likely to be affected biology; https://www.iucn.org/theme/science-and-
ments from around the world and global should animals be transported outside knowledge/our-work/culture-science-and-knowledge/
health and environmental organizations the intended range. Similarly, the African synthetic-biology-and-biodiversity-conservation/
will financially support this organization, Union is currently deliberating appropriate development-iucn-policy-synthetic-biology.
because in the absence of global guidelines, governance of gene drive–bearing mosqui- 4. The National Academies of Sciences, Engineering, and
improper use of this technology could prove toes to combat malaria on a regional scale. Medicine, Gene Drives on the Horizon: Advancing Science,
costlier than any up-front investments that The global coordination team would estab- Navigating Uncertainty, and Aligning Research with Public
ensure its responsible use. lish mechanisms to provide integrated de- Values (National Academy Press,Washington, DC, 2016).
liberation services for regional and national 5. A.J. Piaggio et al., Trends Ecol. Evol. 32, 97 (2017).
An interdisciplinary leadership commit- decision-making. Coordination would serve 6. ETC Group, Reckless driving: Gene drives and the
tee diverse in gender, age, geography, and to minimize geopolitical threats and ensure end of nature (2016); www.etcgroup.org/content/
worldviews and whose members are not that the rights of affected communities are reckless-driving-gene-drives-and-end-nature.
direct beneficiaries of any decision-making upheld at all levels of decision-making. 7. Australian Academy of Science, Synthetic gene drives in
process, would need to oversee the following Moreover, the new avenues forged for open Australia: Implications of emerging technologies
essential next steps. First, a task force must communication by the coordinating body (2017); www.science.org.au/support/analysis/reports/
be established to design the integrated delib- will enable deliberative outcomes to shape synthetic-gene-drives-australia-implications-emerging-
erative framework. This task force would also technologies.
be charged with defining the scope and type 8. New Partnership for Africa’s Development,
of edits to be covered, convening deliberative Gene drives for malaria control and elimination
processes, and overseeing iterative improve- in Africa (2018); www.nepad.org/publication/
gene-drives-malaria-control-and-elimination-africa.
9. CBD, Portal on synthetic biology; https://bch.cbd.int/
synbio/.

10. C. Emerson, S.James, K. Littler, F. Randazzo, Science 358,
1135 (2017).

11. I. Swetlitz,“In a remote West African villiage, a revolu-
tionary genetic experiment is on its way—if residents
agree to it,”STAT News, 14 March 2017; www.statnews.
com/2017/03/14/malaria-mosquitoes-burkina-faso/.

12. G. E. Kaebnick, Hastings Cent. Rep. 47, S60 (2017).
13. R. Owen et al., in Responsible Innovation: Managing the

Responsible Emergence of Science and Innovation in
Society, R. Owen,J. Bessant, M. Heintz, Eds. (Wiley, 2013), pp.
27–50.
14. S. Burall, Nature 555, 438 (2018).
15. C. P. Neuhaus, Hastings Cent. Rep. 48, 25 (2018).
16. E. L. O’Donnell,J.Talbot-Jones, Ecol. Soc. 23, 7 (2018).
17. M. Ferkany, K. P.Whyte, J.Agric. Environ. Ethics 25, 419
(2012).
18. S. Díaz et al., Science 359, 270 (2018).

ACKNOWLEDGMENTS

Authors thank the Yale Institute for Biospheric Studies, the Yale
Interdisciplinary Center for Bioethics, and the Franke Program in
Science and the Humanities for funding the 2017 Editing Nature
Summit, which informed this manuscript.We are grateful for
the help and support of J. and M. R.Vigliotti, I. Papangeli, G.
Kaebnick, M. E.Tucker, L. Stevenson, C.A. Kroop,A. Miller, and
our dearly remembered friend and colleague Calestous Juma.

SUPPLEMENTARY MATERIALS

www.sciencemag.org/content/362/6414/527/suppl/DC1

10.1126/science.aat4612

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An Ebola treatment
center sits empty in
Freetown, Sierra Leone,
in November 2016.

BOOKS et al.

PUBLIC HEALTH of 11 U.S.-built Ebola treatment units is an Downloaded from http://science.sciencemag.org/ on November 1, 2018
emblematic example: Just two units were
Improving outbreak response ever occupied because they were no longer
needed by the time they were completed.
Learning from Ebola failures is key for crafting better plans
for public health emergencies Lags in detection and mobilization and de-
lays in the establishment of best clinical prac-
By William F. Pewen 2014. Before his death, physicians struggled tice proved costly. Failures synergized: When
the Sierra Leone Ministry of Health and San-
to reconcile ethical questions: Should they itation counted only laboratory-confirmed
Ebola deaths, yet had just two phlebotomists
“K nowing is not enough; we must apply. use a new experimental treatment? If he in the field collecting blood samples, cases
Willing is not enough; we must do.” subsequently perished, would the attempt were underreported. Meanwhile, response
This observation, made many years be viewed by the public as a noble failure was compromised by a deficit of collabora-
ago by Johann von Goethe, might well or the exploitation of yet another African tion: 43% of the authors’ survey respondents
have been said about the West African life? Would offering him a new treatment be reported data hoarding.

Ebola outbreak of 2014–2016, when equitable? Could a patient without Khan’s Sabeti and Salahi provide a set of prin-
ciples to improve outbreak response. They
neither advanced technology nor training provide truly informed propose a foundation of universal ethical
standards coupled with increased account-
humanitarian intent was suffi- consent to receive such a therapy? ability. They note that cooperation could be
incentivized, from eliminating stigma and
cient to avert a major health crisis. The authors deftly weave sur- discomfort in implementing quarantine to
reforming data sharing and patent systems
In Outbreak Culture, geneti- veys, interviews, and retrospec- in order to promote collaboration.

cist Pardis Sabeti joins journalist tives on previous outbreaks into Most provocative is the authors’ vision of
a system of global readiness—one that com-
Lara Salahi to examine the epi- a concise depiction of the Ebola bines a military-styled response and cen-
tralized governance. Given that substantial
demic from the perspective of the epidemic, with particular focus compliance issues exist even under existing
World Health Organization health regula-
clinical workers, researchers, and on human behaviors that exacer- tions, could such an integrated authority gain
the support of national governments and the
health agency personnel who ex- Outbreak Culture bated the course of the outbreak. cooperation of local populations? In an era of PHOTO: OLIVIA ACLAND/BARCROFT IMAGES/BARCROFT MEDIA/GETTY IMAGES
perienced it firsthand. They note Pardis Sabeti and They describe the negative im- increasing nationalism and waning support
in particular three factors that fos- pacts of the egregious quarantine of international efforts, the bar to achieve
ter a culture that can compromise Lara Salahi in Liberia and acknowledge the such an ambitious vision appears high.
outbreak response: (i) fear; (ii) the Harvard University contribution of local burial prac-
Press, 2018. 275 pp. Yet in a time when it can be easier to se-
quence a virus than to obtain a clinical sam-
instinct to protect oneself, others, tices to viral transmission, but ple or share genomic data, changing outbreak
culture demands systems innovations and
or institutions; and (iii) the desire to exploit. they also remind readers how poorly health policy commitments. As Sabeti’s colleague
Nathan Yozwiak notes, “The limitations are
The book focuses on what happens when care workers returning to the United States human, they’re not technical anymore.” j

these motives collide, indicting poor policies, were treated and how inadequately the coun- 10.1126/science.aav2473

ineffective decision-making, and bad actors. try responded to a mere handful of cases.

An illustrative prologue depicts the tragic Accountability proved a critical problem

death of Sheikh Humarr Khan, the physician in the Ebola response. Funds often flowed

director of the Kenema Government Hospital directly to individuals, fostering corruption:

who succumbed to Ebola infection in July of Less than 2% were directed to the pressing

needs of local responders.

The reviewer is visiting associate professor and interim chair Sabeti and Salahi present a wealth of
of the Department of Health, Nursing and Nutrition at the evidence supporting the imperative that
University of the District of Columbia, Washington, DC, USA. outbreak response must operate in a coor-
Email: [email protected] dinated, real-time manner. The construction

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INSIGHTS

PA L E O N T O L O GY

Collector’s item or cultural heritage?

A riveting tale of a smuggled dinosaur illuminates an enduring tension in paleontology

By Victoria M. Arbour bones” and “fossil reptiles.” After more than a The Dinosaur Artist
Obsession, Betrayal,
year of work cleaning the bones and fabricat- and the Quest for Earth’s
Ultimate Trophy
W hen a dinosaur is named as a de- ing an armature to mount them together, the Paige Williams
fendant in a court case, it is all but skeleton went up for auction in 2011. When Hachette Books, 2018.
ensured that headlines will fol- the Mongolian government raised concerns 432 pp.
low. So it was in 2013, when the over the sale of the skeleton, it kickstarted a
U.S. government sought to seize a multiyear investigation that would ultimately Mongolian fossils have contributed greatly
to our understanding of dinosaur evolution;
smuggled dinosaur skeleton in a see the Tarbosaurus seized and returned to however, most have been excavated by for-
eign teams of paleontologists who receive the
case entitled United States v. One Tyranno- Ulaanbaatar. Prokopi would lose his house credit and fame for these discoveries. As such,
the tale of the smuggled Tarbosaurus raises
saurus Bataar Skeleton. In The Dinosaur Art- and face time in jail for smuggling fossils.
some uncomfortable questions for
ist, journalist Paige Williams tells the story of I must admit that I came away from The academic paleontologists who, like
myself, take part in foreign expedi-
Eric Prokopi—the man who purchased, pre- Dinosaur Artist with respect for Prokopi’s tions. Are our efforts just another Downloaded from http://science.sciencemag.org/ on November 1, 2018
form of western colonialism? Have
pared, and attempted to sell the Tarbosaurus passion for fossils, if not for his methods. In a those of us who study Mongolian
fossils truly done all we can to help
in question—and reveals how the skeleton world where full-time positions for academic grow capacity for research and pub-
lic engagement within that country?
made its way out of, and ultimately back to, paleontologists are extremely rare, and where
Although the heart of Williams’s
Mongolia. Throughout the book, tale is Prokopi’s story, I found in-
spiration in Mongolian paleontolo-
she folds together multiple stories gist Bolor Minjin’s quest to bring
the Tarbosaurus home and to re-
to illuminate the history of fossil boot paleontological research and
education in her home country.
hunting, revealing how fossils wind She raised the alarm over the sale
of the Tarbosaurus and, with the
up as precious objects of national nonprofit Institute for the Study
of Mongolian Dinosaurs that she
and cultural heritage or coveted founded, has helped repatriate numerous
Mongolian skeletons that had been smug-
collector’s items. gled out of the country. Each summer, she
leads a team that travels across the Mon-
Tarbosaurus bataar was a close golian countryside in a 40-foot mobile mu-
seum, bringing dinosaurs directly to her
relative of Tyrannosaurus rex that fellow Mongolians. But the resources for
building education and research from the
roamed the humid floodplains of ground up in Mongolia pale in comparison
with the sums involved in the sale of smug-
Mongolia during the Late Creta- gled dinosaurs, and Minjin faces a constant
uphill battle.
ceous, toward the end of the age Ultimately, The Dinosaur Artist is a com-
pelling, nuanced look at the surprisingly
of dinosaurs. Some Tarbosaurus complex politics that surround fossil col-
lecting. It should be required reading for
skeletons have been excavated by both professional paleontologists and fos-
sil enthusiasts and is a gripping read for
teams of paleontologists and can anyone interested in the interplay between
culture, history, and science. j
be found in museums, where they
10.1126/science.aav2020
are used for research and public

display. Others enter a not-so-

secret underground trade in fossils The smuggled Tarbosaurus was eventually returned to Mongolia.

illegally exported from Central Asia

and are sold piecemeal at gem and mineral obtaining such a position requires that one

shows, on eBay, or through private dealers. have the time and money to pursue a gradu-

Fossils sold to private hands are effec- ate degree, he forged his own path.

tively lost to science. Specimens in the pub- The Dinosaur Artist puts into stark

lic trust, such as accredited museums, can relief the way wealth, privilege, and na-

be examined over and over again by pale- tionality shape who gets to participate

ontologists now and in the future; private in paleontology and reveals how shifting

PHOTO: BYAMBASUREN BYAMBA-OCHIR/AFP/GETTY IMAGES collections do not have the same mandates norms complicate the legacy of revered

to care for fossils in perpetuity. For this rea- paleontologists of the past. Mary Anning,

son, many countries, including Mongolia, a 19th-century English fossil hunter who

make it illegal to excavate or export scien- struggled to be taken seriously as a con-

tifically important fossils without a permit. tributor to science (despite making numer-

Prokopi built a living by selling fossils ous important discoveries), is now lauded

he scoured from beaches and waterways in as an unsung hero of our discipline, for

Florida, starting when he was just a teenager. example. But, as Williams reveals, she also

The Tarbosaurus was his biggest acquisition sold her fossils to make a living. Similarly,

yet, shipped to America via a dealer based Roy Chapman Andrews, who led the first

in England in crates labeled “broken fossil American paleontological expedition to

Mongolia, inspired many of today’s promi-

The reviewer is curator of paleontology, Royal BC Museum, nent paleontologists. But, like Anning, he
Victoria, BC, Canada. Email: [email protected] also sold some of his finds.

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LETTERS

Edited by Jennifer Sills participants access to resources, support, REFERENCES Downloaded from http://science.sciencemag.org/ on November 5, 2018
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Beyond hierarchical ing setting. Evidence suggests that peer 1. B. R. Ragins,J. L. Cotton,J. S. Miller, Acad. Manage.J. 43, 6 PHOTO: KLAUS VEDFELT/GETTY IMAGES
one-on-one mentoring mentoring is most effective with groups (2000).
of five to eight participants who are all at
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mentoring” (5 October, p. 22) demonstrates tary fields of expertise, and share social Acad. Med.J.Assoc.Am. Med. Coll. 88, 1 (2013).
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these relationships are not strong, they wisdom and perspectives to share as well century clinician, educator and scientist”(2016); https://
can hinder or even harm mentees (1, 2). as areas in which they need advice. Peer academicaffairs.ucsf.edu/ccfl/media/lectures/Race%20
The unequal power dynamic of a senior mentoring provides an opportunity to col- Matters%20Slides.pdf.
mentor (typically one who is male and laboratively problem solve, share ideas and 5. K.A. Rockquemore,“When it comes to mentoring, the
white) and junior mentee can be especially perspectives, and develop community and more the merrier”Chron. High. Educ. (2014); https://
problematic for individuals belonging thus serves as a mechanism for developing chroniclevitae.com/news/326-when-it-comes-to-
to systematically marginalized identity independence and career self-efficacy (11). mentoring-the-more-the-merrier.
groups (such as women, people of color, 6. K. E. Kram, Mentoring at Work: Developmental
and individuals with disabilities) and can Peer mentoring becomes especially Relationships in Organizational Life (Scott Foresman,
exacerbate a sense of isolation for the men- important as mentees mature and develop Glenview, IL, 1985).
tee (3). Furthermore, mentees, more than into independent scientists. Through 7. R. DeCastro, D. Sambuco, P.A. Ubel,A. Stewart, R.Jagsi,
mentors, say that mentoring relationships peer mentoring, individuals participate in Acad. Med. 88, 4 (2013).
should directly address cultural diversity reciprocal and interactive relationships in 8. A. Darwin, E. Palmer, Higher Educ. Res. Dev. 28, 2 (2009).
(4). A mentoring network, including peer which they have the opportunity to develop 9. M. C. Horner-Devine, C. Margherio, S.J. Mizumori,J.W.
mentoring, can address the shortfalls of not only their own problem-solving skills Yen,“Peer Mentoring Circles: A strategy for thriving in
traditional one-on-one mentoring. and career self-efficacy but also their science,” BioMed Central Blog (2017); https://blogs.
confidence and skills as mentors. Peer biomedcentral.com/bmcblog/2017/05/18/peer-
A mentoring network with multiple mentoring can be a component of a pro- mentoring-circles-a-strategy-for-thriving-in-science/.
modes of mentoring (5) dismantles the fessional development program (12) or a 10. E. Daniell, Every Other Thursday: Stories and Strategies
guru mentor myth, which suggests that one stand-alone activity (10). Those looking for from Successful Women Scientists (Yale, Cambridge, MA,
senior mentor is a necessary and sufficient the mentoring so valued by contributors to 2006).
source of mentoring. Instead, a mentoring the NextGen Voices survey might consider 11. L. R. Fraga,“Comment: Mentoring for institutional gain”in
network framework centers on the mentees giving peer mentoring a try. ATruly Diverse Faculty: New Dialogues in American Higher
and what they need and desire to thrive Education, S.A. Fryberg, E.J. Martinez, Eds. (Palgrave
in their career; it then meets their varied M. Claire Horner-Devine,1,2* Torie Macmillan, New York, 2014), pp. 257–264.
needs through a host of mentoring rela- Gonsalves,1 Cara Margherio,3 Sheri J. 12. J.W.Yen, M. C. Horner-Devine, C. Margherio, S.J.
tionships (6, 7). Peer mentoring can serve Mizumori,4 Joyce W. Yen1 Mizumori, Neuron 94, 3 (2017).
as an important node in an individual’s
broader mentoring network and reduce the 1ADVANCE Center for Institutional Change, 10.1126/science.aav7656
reliance on hierarchical relationships (8). University of Washington, Seattle, WA 98195, USA.
2 Counterspace Consulting, Seattle, WA 98103, Engaging community
Peer mentoring is a truly horizontal USA. 3Center for Evaluation and Research for STEM
mentoring experience (9) that offers Equity, University of Washington, Seattle, WA 98195, with humility
USA. 4Department of Psychology, University of
Washington, Seattle, WA 98195, USA. In his Policy Forum “Building an evi-
*Corresponding author. Email: [email protected] dence base for stakeholder engagement”
(10 August, p. 554), J. V. Lavery rightly
proposes additional reporting and evidence
collection to understand best practices for
community and stakeholder engagement.
However, we are concerned that he framed
stakeholder engagement too narrowly.

Lavery’s proposed consumer model
for engagement replicates the individual

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INSIGHTS

Peer mentoring can provide support, facilitate radiation of modern kangaroos” (A. M. C. Downloaded from http://science.sciencemag.org/ on November 5, 2018
collaborative problem solving, and build confidence. Couzens and G. J. Prideaux, 5 October, p.
72), P. D. Polly discusses the evolution of
focus of human subject research in an high molar teeth in Australian kangaroos
arena where stakeholders’ interests and and wallabies. He cites evidence that,
power are often collective. His refer- in South America, mammals developed
ence to the human-centered design these high-crowned teeth in the context of
that informed Apple tech products for humid forests. However, this has not been
purchase by individual consumers fails determined with certainty.
to capture the complexity and challenges
that communities and stakeholders face Opinions have oscillated in recent
when confronted with large-scale techni- years regarding the context and causes
cal interventions that affect the shared of the high-crowned molars [so-called
environment. Lavery’s avoidance of the “precocious hypsodonty” (1)] exhibited
term “public” in favor of this consumer by late Eocene and early Oligocene South
model contrasts with important research American mammals. Several lines of
and practice in the pursuit of more evidence, including fossilized plant tissue,
democratic visions for the governance of mammals, and stable isotopes, suggest
science and technology (1, 2). that high-crowned teeth developed in the
context of relatively arid and open habitats
Although Lavery cites the potential (2–5). Curiously, these habitats seem to
for community and stakeholder engage- have been dominated by palms rather than
ment to increase the success of science grasses (4) and thus were neither true
programs, he does not explore stakehold- grasslands nor analogous to most mod-
ers’ role in defining what would count as ern South American open habitats. The
success. For community and stakeholder discrepancy is reminiscent of the ancient
engagement to matter and serve as more South American mammal communities
than just window dressing, scientists themselves, which were not analogous to
and funders need to relinquish some those found there today (6).
of their power and authority by allow-
ing stakeholders—including historically As Polly explains, geographically isolated
marginalized groups that are tradition- Cenozoic mammal species, such as those
ally excluded from governance spaces—to of Australia and South America, are well
influence problem framings, program suited for independently documenting how
goals, and other key decisions (3, 4). mammalian herbivores have responded to
Communities and stakeholders should changing climates and other factors over
help identify the desired goals of a science millions of years. In South America, unlike
program instead of serving as a means in Australia, the relationship between
to achieve the program sponsor’s prede- aridity and the evolution of high molars
termined ends (5, 6). For community and broadly parallels that seen in the Northern
stakeholder engagement to take a more Hemisphere (4, 7); it just happened to take
central role in science programs, scientists place some 15 to 20 million years earlier (2).
and funders will have to embrace a new
kind of humility. Darin A. Croft

Jason Delborne,* Adam Kokotovich, Department of Anatomy, Case Western Reserve
S. Kathleen Barnhill-Dilling University School of Medicine, Cleveland, OH 44106-
4930, USA. Email: [email protected]
North Carolina State University, Raleigh,
NC 27695, USA. REFERENCES
*Corresponding author. Email: [email protected]
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10.1126/science.aav6745

Evolution of teeth in ERRATA
South America
Erratum for the Research Article “Saturn’s
In his Perspective “Marsupial responses magnetic field revealed by the Cassini Grand
to global aridification” (5 October, p. 25) Finale” by M. K. Dougherty et al., Science
on the Report “Rapid Pliocene adaptive 362, eaav6732 (2018). Published online 12
October 2018; 10.1126/science.aav6732

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MIXING AND MATCHING

MATERIALS

By Marc Lavine and Brent Grocholski Downloaded from http://science.sciencemag.org/ on November 5, 2018

PHOTO: JUN JIE LOKE, BIOLOGICAL AND BIOMIMETICS LABORATORY, NANYANG TECHNOLOGICAL UNIVERSITY (NTU), SINGAPORE T he world we interact with is domi- cal sponges transform materials as simple as
nated by intertwined materials silica into components that are both tough
known as composites. Unlike in and exceptionally efcient at manipulating
metal alloys or polymer blends, light. Further, natural materials, many of
where the atoms or molecules are which end up as waste in the process of har-
intimately mixed, components of vesting food, may have properties that can
a composite material retain their compete with those of synthetic materials
individual identities, and their and have the advantage of originating from

careful selection and combination renewable resources.

maximizes certain sets of properties. Here, Carbon-based composites such as those

too, another facet of composite materials fabricated from carbon fiber ofer the unique

emerges—they typically have stronger and combination of high strength and low den-

weaker directions (i.e., asym- sity. Replacing carbon fiber with

metric properties), as they are INSIDE graphene or carbon nanotubes

designed to fulfill the needs of REVIEWS opens a wide range of new prop-
specific applications. erties for optimization. The po-
Composites from renewable tential to develop composites
The benefits of combining ma- and sustainable resources: with exceptional mechanical,
terials are easily learned from na- Challenges and innovations thermal, and electrical proper-
ture. Natural composites such as p. 536 ties provides great incentive to
nacre, wood, and teeth have im-
Biological composites—
complex structures for
functional diversity p. 543

pressive properties arising from Composites with carbon overcome processing hurdles to
their hierarchical structures, nanotubes and graphene: efcient production scale-up.
especially as they are generated An outlook p. 547
from easily obtained starting In all good composites, the
materials that often have limited RELATED ITEM whole is better than the sum of
c PODCAST the parts. The same may be true

capabilities. Though scientists Squid sucker teeth are strong of research on composites, as
have long studied mechanically enough to pierce and anchor looking beyond one’s traditional
tough natural composites, recent prey but are composed solely sources of materials may lead to
research has shown that biologi- of protein building blocks that better composite materials.
can be reshaped upon heating.

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COMPOSITE MATERIALS

REVIEW valorized in the fabrication of a diverse array Downloaded from http://science.sciencemag.org/ on November 1, 2018
of biocomposites.
Composites from renewable
and sustainable resources: Materials scientists can help in advancing
Challenges and innovations sustainable alternatives by quantifying the en-
vironmental burden of a material through its
Amar K. Mohanty1,2*, Singaravelu Vivekanandhan3, product life-cycle analysis (1, 2). The exponen-
Jean-Mathieu Pin1, Manjusri Misra1,2 tial growth of population and modernization
of our society will lead to a threefold increase
Interest in constructing composite materials from biosourced, recycled materials; waste in the demand for global resources if the cur-
resources; and their combinations is growing. Biocomposites have attracted the attention rent resource-intensive path is continued (3).
of automakers for the design of lightweight parts. Hybrid biocomposites made of According to the United Nations, a truckload
petrochemical-based and bioresourced materials have led to technological advances in of plastic waste is poured into the sea every
manufacturing. Greener biocomposites from plant-derived fiber and crop-derived plastics with minute. By 2050, at current rates, the amount
higher biobased content are continuously being developed. Biodegradable composites have of plastic in the ocean will exceed the number of
shown potential for major uses in sustainable packaging. Recycled plastic materials originally fish. The benefit of diverting plastic packaging
destined for landfills can be redirected and repurposed for blending in composite applications, material is estimated at around $80 billion to
thus leading to reduced dependence on virgin petro-based materials. Studies on compatibility $120 billion, which is currently lost to the eco-
of recycled and waste materials with other components in composite structure for improved
interface and better mechanical performance pose major scientific challenges. This research “Wood and other natural
holds the promise of advancing a key global sustainability goal. fibers (e.g., flax, jute, sisal,
and cotton), collectively
T he era of natural fiber composites currently thermoplastics such as polyamide (PA), poly- called ‘biofibers,’ can be used
known as biocomposites dates back to 1908 propylene (PP), and poly(vinyl chloride) (PVC), to reinforce fossil fuel–based
with the introduction of cellulose fiber– as well as thermoset resins such as unsaturated plastic, thus resulting in
reinforced phenolic composites. This inno- polyester (UPE) and epoxy resin. In addition biocomposite materials...
vation was followed by synthetic glass to fiber, mineral fillers such as talc, clay, and Biofiber-PP and biofiber-UPE
fiber–reinforced polyester composites, which calcium carbonate are being used in com- composites have reached
obtained commodity status in the 1940s. The use of posite manufacturing. Such hybrids of fiber and commodity status in many
biobased green polymers to manufacture auto parts mineral fillers play a major role in industrial auto parts, as well as
began in 1941, when Henry Ford made fenders automotive, housing, and even packaging ap- decking, furniture, and
and deck lids from soy protein–based bioplastic. plications. Carbon black plays a vital role as a housing applications.”
The use of composite materials, made with re- reinforcement, especially in rubber-based compos-
newable and sustainable resources, has become ites. The key environmental concern with regard nomy (4). If diverted for composite use, the re-
one of the vital components of the next genera- to composite materials is the difficulty of remov- cycled and waste plastic currently destined for
tion of industrial practice. Their expanding use is ing individual components from their structures landfills and incineration would be used for
driven by a variety of factors, including the need to enable recycling at the end of a material’s ser- sustainable development, thereby reducing de-
for sustainable growth, energy security, lower vice life. At this point, most composite materials pendence on nonrenewable resources such as
carbon footprint, and effective resource man- are either sent to a landfill or incinerated. Wood petroleum. Postindustrial food processing wastes
agement, while functional properties of the and other natural fibers (e.g., flax, jute, sisal, are being explored as biofiller in biodegradable
materials are simultaneously being improved. and cotton), collectively called “biofibers,” can plastics for the development of compostable bio-
Innovative sustainable resources such as bio- be used to reinforce fossil fuel–based plastic, composites. Low-value biomass and waste re-
sourced materials, as well as wastes, coproducts, thus resulting in biocomposite materials. Syn- sources can be pyrolyzed to provide biocabon
and recycled materials, can be used as both the thetic glass fiber–reinforced biobased plastics (biochar) as sustainable filler for biocomposite
matrix and reinforcement in composites to min- such as polylactides (PLAs) are a type of bio- uses. The increased sustainability in composite
imize the use of nonrenewable resources and to composite. Biofiber-PP and biofiber-UPE com- industries requires basic and transformative re-
make better use of waste streams. posites have reached commodity status in many search toward the design of entirely green com-
auto parts, as well as decking, furniture, and posites. Renewable resourced–based sustainable
Composite materials find a wide range of po- housing applications. Hybrid biocomposites of polymers and bioplastics, as well as advanced
tential applications in construction and auto-parts natural and synthetic fibers as well as mixed green fibers such as lignin-based carbon fiber and
structures, electronic components, civil structures, matrix systems also represent a key strategy nanocellulose, have great potential for sustainable
and biomedical implants. Traditionally, indus- in engineering new classes of biobased com- composites. Biobased nonbiodegradable com-
trial sectors that require materials with superior posites. As part of feedstock selection, a wide posites show promising applications in auto parts
mechanical properties use composites made range of renewable products that includes agri- and other manufacturing applications that re-
from glass, aramid, and carbon fibers to reinforce cultural and forestry residues, wheat straw, rice quire durability. Biodegradable composites also
straw, and waste wood, as well as undervalued show promise in sustainable packaging. This com-
1Bioproducts Discovery and Development Centre, industrial coproducts including biofuel coprod- prehensive Review on composites from sustainable
Department of Plant Agriculture, University of Guelph, ucts such as lignin, bagasse, and clean municipal and renewable resources aims to summarize their
Guelph, ON N1G 2W1, Canada. 2School of Engineering, solid wastes, is currently being explored to derive
University of Guelph, Guelph, ON N1G 2W1, Canada. chemicals and materials. Recent advancements
3Sustainable Materials and Nanotechnology Lab, Department in biorefinery concepts create new opportunities
of Physics, V.H.N.S.N. College (Autonomous), Virudhunagar, with side-stream product feedstock that can be
Tamilnadu 626 001, India.
*Corresponding author. Email: [email protected]

Mohanty et al., Science 362, 536–542 (2018) 2 November 2018 1 of 7

PHOTOS: (CLOCKWISE FROM TOP LEFT) ISTOCK/LIOR2, ISTOCK/LUCATO, A. K. MOHANTY, ISTOCK/IVAN4ES, ISTOCK/RDONAR, ISTOCK/NP-E07, A. K. MOHANTY, ISTOCK/OCEANBOUNDDB, ISTOCK/BANKSPHOTOS, A. K. MOHANTY, ISTOCK/JULIO RICCO, A. K. MOHANTY current status, constraints on wider adoption, inforcements. The advantages of biofibers over ly treated as waste in the global poultry industry, Downloaded from http://science.sciencemag.org/ on November 1, 2018
and future opportunities. In keeping with the traditional glass fibers and mineral fillers are their can find application as renewable fiber reinforce-
broad focus of this article, we analyze the current lower density, reduced cost, eco-friendly nature, ment in lightweight biocomposites. Recycled car-
development of such composites and discuss and enhanced performance in certain applica- bon fiber from the aerospace and sporting goods
various fibers and fillers for reinforcements, tions. Among the available natural fillers that industries is another sustainable source that can be
current trends in polymer matrix systems, and can be used for composite applications, wood used to generate hybrid composites with biofibers.
integration of recycled and waste coproducts into is the most commonly used. Cotton fibers are
composite systems to outline future research trends. also widely available. Other agricultural natural Biocarbon, a new sustainable filler and
fibers such as flax, jute, kenaf, industrial hemp, functional material
Fibers and fillers from renewable and and sisal are used as well. Because of their de-
sustainable resources sirable structural properties, the construction field Biocarbon, also known as biochar, has emerged
is the major arena for the use of natural fiber as a new sustainable material for many appli-
In polymer composites, plastic resins remain composites. Unconventional natural fibers such cations. Biochar is not limited to filler and re-
as continuous phase, whereas fibers and fillers as agro-residues (e.g., wheat and rice straws, ground inforcement uses for biocomposites (8); it is also
stay in discontinuous phase to provide reinforce- coconut shells) and grasses (e.g., miscanthus, beneficial for the development of next-generation
ment effects. The composite performance is switch grass, and bamboo) find application in functional carbon materials (9) for potential
governed through the interface between the biocomposites. applications in energy storage and filtration
fibers and the polymer matrix. In composite devices. The thermochemical conversion of
science, the key target is the interface and re- Biofuel coproducts, food processing biomass when oxygen is absent or in limited
lated interfacial bonding as the stress transfer wastes, and other postindustrial wastes supply (also known as pyrolysis) generates liquid
between the fiber and polymer matrix dictates bio-oil, solid biochar, and syngas. Depending on
the overall mechanical performance (5). When Value-added uses of coproducts and by-products temperature, time, and the nature of biomass in
deciding on the appropriate fiber and filler from biorefinery and biomass conversion pro- the pyrolysis process, the amount of oil, char,
system for sustainable composite uses in in- cesses are beneficial for sustainable development. and gas may vary. Biochar or biocarbon (BioC)
dustrial sectors, it is necessary to compare the Distillers’ dried grains with solubles (DDGS) from is an amorphous carbon-rich material that can be
cost and availability, consistency of properties, the corn ethanol industry, lignin coproduct tunable in terms of chemical structure, porosity,
and environmental advantages of sustainable from lignocellulosic ethanol industry as well as size, and intrinsic modulus. Two other amorphous
fibers with those of their traditional synthetic the pulp and paper industry, and bagasse from carbon–based materials are activated carbon (AC)
counterparts. Figure 1 depicts examples of dif- the sugarcane ethanol industry are being used and carbon black (CB). The main distinctions
ferent types of fibers and fillers for biocomposites. in biocomposites (7). Lignin, which is polyphenolic among such carbon-rich materials are based on
in composition, has found value-added uses in their origin, formation process, and structure. The
Lignocellulosic plant fibers sustainable biobased composite materials. Lignin, carbon content of BioC varies from 40 to 90%, as
with its many functional surface –OH groups as compared with 80 to 95% for AC and >95% for
This category, well known as natural fiber or well as with surface modification, has shown CB. Regarding origin of formation, BioC is gen-
biofiber, is broadly classified as wood and non- improved reinforcing effect on resulting bio- erated from biomass; AC from asphalt, coal, and
wood fibers. These include various types such as composite performance. Additionally, fruit and biomass; and CB from petroleum and coal tar.
bast, leaf, seed or fruit, straw, grass, and wood vegetable pomace, coffee chaff, and grain hulls
(6). The mechanical performance of various plant have been explored in composites. Most of these Matrix polymer from renewable and
fibers depends on their cell wall structure, com- biofillers are used for waste valorization, whereas sustainable resources
position, and morphology. Cellulose content, lu- the resulting biocomposites can be used for non-
men size, and microfibrillar angle are other key structural applications. Chicken feathers, current- The majority of plastic resins in biocomposites are
factors governing the stiffness of plant fiber re- predominantly concentrated among petro-based

Flax Sisal Wood pulp Wheat Corn Miscanthus

Kenaf, flax, jute, sisal, ramie, Traditional Sustainable Agro and Straws (wheat, rice, soy, and canola),
cotton, bamboo, henequen, natural reinforcements forestry woody biomass (willow), grasses
wood (soft and hard) fibers residues (Miscanthus), stover (corn)
and fillers
Lignin, DDGS, biocarbon, Industrial Recycled Carpet mats, wooden pellets,
pomace, bagasse, coir, co-products fibers/fillers cardboard sheets, carbon fibers
hull and husks

Grape pomace Bagasse Lignin Carpet Cardboard Carbon

Fig. 1. Fibers and fillers from renewable and sustainable resources.

Mohanty et al., Science 362, 536–542 (2018) 2 November 2018 2 of 7

COMPOSITE MATERIALS

thermoplastics [e.g., PP, polyethylene (PE), and lenges from a combined societal, economic, en- reactive extrusion processing. The most common-
PVC] and thermosets (e.g., UPE and epoxy). vironmental, and human health perspective. ly used coupling agent is maleic anhydride–grafted
Global annual production of plastics was esti- The sustainability measurement is difficult to polypropylene (MAPP) for PP-based biocompos-
mated as 407 million metric tons (MT) in 2015 quantify. Although more energy is required to ites. The optimal content of coupling agents on
(10), and production related to polyolefin with produce biobased low-density polyethylene (bio- specific natural fiber–PP system governs the
PP and PE exceeds this amount by >50%. Tech- LDPE) in comparison with its petroleum-based overall performance. In natural fiber thermo-
nically, the majority of all plastics can be made counterpart, its overall global warming poten- plastic composites, short fibers (<10 mm) are
from renewable resources (11). Figure 2 depicts tial from the life-cycle assessment perspective preferred. In twin screw extruders, the reaction
various types of plastics for use in composites. is relatively lower (16). takes place among fiber, plastic, and coupling
Plastics that are biobased, biodegradable, or agent, with processing and materials combina-
both are known as bioplastics. The current trend Renewable and sustainable tion optimized for development of compatibi-
of biobased polymer development is definitely resource-based biocomposites: lized composite pellets formulated for additional
growing: from a total production capacity of Scientific challenges processing. Further processing may include injec-
~2.05 million MT in 2017 to an expected 2.44 tion molding into the appropriate shape for
million MT in 2022 (12). Bioplastics are generally Fiber-matrix adhesion, matrix and fiber mod- structure-property-processing tests or the final
categorized in three groups: (i) biobased and bio- ification, hybrid strategy, and the desired pro- shape for industrial applications. Besides the
degradable plastics [i.e., polyhydroxyalkanoates cessing approach are key factors in making correct material combination, the final proper-
(PHAs) and PLAs]; (ii) entirely or partly bio- high-performance biocomposites for specific ties of composites also depend on the process-
based and nonbiodegradable plastics [i.e., end-use applications. Across the wide spectrum ing method. Conditions such as screw profile
bio-based PE (bio-PE), biobased polyamide of possible matrix and fiber/filler systems, hybrid and speed are among the vital determinants of
(bio-PA), biobased polyethylene terephthalate synergistic assembly for improved compatibil- final properties in a reactive extrusion process.
(bio-PET), and bio-thermosets such as polyfur- In polymer composites, cost-performance tar-
furyl alcohol (PFA) or bio-polyurethane (bio-PU)]; Petrobased Biobased gets are affected by both the matrix and the Downloaded from http://science.sciencemag.org/ on November 1, 2018
and (iii) petroleum-based biodegradable plastics non-biodegradable biodegradable reinforcement options selected. A hybrid com-
[i.e., polybutylene adipate terephthalate (PBAT), posite system requires a blend of two or more
polycaprolactone (PCL), and polybutylene succi- Epoxy PE Bio-PBS plastics and mixed fibers. Inclusion of recycled
nate (PBS)]. PBS can be fully biobased, and par- PP PVC PHAs or undervalued waste materials further height-
tially biobased PBS is commercially available at UPE PLA ens the scientific challenges. Figure 3 highlights
present. Fully biobased polyethylene furanate, a Polymer the key aspects of sustainable hybrid composite
new nonbiodegradable material, shows immense PCL Matrix design. The successful compatibilization of poly-
promise in industrial applications. Degradable PBS mer matrices that allows a good balance of prop-
plastics are attracting increased attention for PBAT Bio-PTT Bio-PE erties can be achieved by using block copolymers
disposable plastic applications, and nondegradable Bio-PET Bio-PA as additives to act as physical compatibilizers.
bio-PE and bio-PET have also demonstrated PFA The illustrated example related to the PE/iPP
potential for packaging applications. Poly(tri- (polyethylene/isotactic polypropylene) compa-
methylene terephthalate) (PTT) is a semicrystalline Petrobased Biobased tibilized tough blends (18) is particularly relevant
biobased plastic generated from condensation biodegradable non-biodegradable because it allows the direct recycling of those
of biobased propanediol and petrochemical materials from municipal wastes (Fig. 3A, i).
terephthalic acid. Bio-PAs can be used in the Fig. 2. Matrix polymers for biocomposites. The compatibilizer can also react, permitting
automotive and consumer products sectors, al- the grafting into the polymer backbone or ter-
though further large-scale production will be ization is a key scientific challenge. Biofibers minal group, as exemplified in PLA/PP blends
needed to achieve costs comparable to those of are hydrophilic and thus have reduced com- with epoxy reactions (Fig. 3A, ii) (19). The syn-
their petro-based counterparts. Biobased plastics patibility with hydrophobic polymer matrices. ergistic combination of the formulation com-
from biological sources show promise for reduc- A myriad of treatments—including chemical ponents is maximized by increasing their
ing environmental concerns caused by petro- (e.g., silane maleic anhydride), mechanical (e.g., compatibility via ex situ modifications or in situ
chemical plastics. Bioethanol is produced from cutting, carding), physical (thermal, plasma, ir- process engineering (Fig. 3B). Although the filler
starch and sugarcane fermentation and com- radiation), and combinations of chemical, me- aspect ratio can be mechanically tailored, chemical
mercialized for fuel applications. The dehydra- chanical, or biological techniques—have been modifications through silane treatment and ma-
tion of bioethanol can produce ethylene, which, developed to tackle the biofiber drawbacks and leation of the matrix and/or fiber are classical
upon polymerization, makes bio-PE, a material improve compatibility with the matrix. PP and industrial strategies to improve their intrinsic
that has already been commercialized. Besides PLA are two examples of thermoplastic resin reactivity. All of these strategic concepts are
this complete deoxidation strategy, catalytic in plant fiber–based biocomposites uses. The combined in the design of hybrid composites
redox approach of carbohydrates by biological former results in a partial biobased composite (Fig. 3C). A multifunctional compatibilizer is
or chemical processes can lead to high-value and the latter a fully biobased composite. In typically required because it can act physically
monomers (13). Terephtalic acid can be obtained contrast to hydrophobic polymers such as PP, and chemically at the interphase, linking the dif-
from furfural and may lead to elaboration of fully lignocellulosic natural fiber shows good compat- ferent modified matrix-filler and fiber phases.
biobased PET (14). Recently, efforts have been ibility with biodegradable polyester–type bio-
initiated to convert greenhouse gases such as plastics such as PLA and PCL (17). Because the Renewable and sustainable resource-
CO2 into bioplastics like polypropylene carbon- natural fiber adheres poorly to hydrophobic based biocomposites: Progress, recent
ate (PPC). Renewable resource–based polymeric polymers such as PP and PE, it is necessary to treat developments, and future perspectives
materials should be safe in production and can the fiber and/or to use a coupling agent during
be recyclable, and their disposal after use should Structure-property-processing correlation is im-
be harmless to the environment. The success of portant in research and development to find
the polymer industry will depend on the de- specific uses of composites. Biocomposites can be
velopment of such sustainable polymers (15). designed and engineered with various combina-
The development of polymers from sustainable tions of polymer matrix and reinforcing fibers
renewable feedstocks poses key scientific chal- and fillers from renewable and sustainable re-
sources. The reinforcement could be in the form

Mohanty et al., Science 362, 536–542 (2018) 2 November 2018 3 of 7

of short fibers, knitted or woven fabrics or non- manufactured through melt mixing with the use vacuum-assisted resin transfer molding, and sheet
woven fabrics, and braids. Various methods may of extrusion and injection molding processes. molding compound techniques are some of the
be chosen for composite manufacturing, depend- Fabric thermoplastic–type reinforcements undergo key processing methods for fabricating thermoset
ing on materials and the targeted end-use ap- thermoforming and compression molding–type biocomposites. Depending on various combinations
plication. For instance, short-fiber, particulate-type processing. The resin infusion process is com- chosen from the range of fibers and resins systems
filler–reinforced thermoplastic biocomposites are monly adopted for thermoset resins. Hand-layup, available, the biocomposites can be classified

A Matrix compatibilization strategy B Matrix & Fiber modification

i. Physical compatibilization Semi-crystalline Grafting strategy Treatment for
polyolefin Acrylation natural fibers
PE/iPP blends Maleation
Block copolymer design Acetylation Physical
Plasma Milling, sizing
LHf+ no p Interface Oligomers Pattern fabric…
m Polymers...
Tetrablock Chemical
PE-block-iPP-block-PE-block-iPP copolymer O Alkaline
O Silane chemistry…
Adhesion mechanism by O Modified Downloaded from http://science.sciencemag.org/ on November 1, 2018
trapped entanglements matrix

ii. Physical & Chemical compatibilization Fiber with enhanced Fiber
Branching and crosslinking functionality
PLA/PP blends O OR
= Chemical function Si
OO OO OO
xyz RO X
HO OO OH O
On OO
xyz Grafting O PLA
OO OH
O X= NH2
O
polyethylene−glycidyl PLA
methacrylate−methyl O
acrylate terpolymer (PEGMMA)
etc.

C Hybrid synergistic assembly in sustainable composites

Hybrid Morphology Compatibilization Reactions

O OR O OR
Si O Si
O O O O O O O O
O O
Si NH2 O O OO Si ON
OO HO
O
RO Si NH2 + O Si N O
RO H

Treated NH2 Compatibilizer O Multi- NH2
filler OH O
HO O
compatibilization

Polymer A Interphase phenomena

Physical compatibilization between the
polymer phase and the compatibilizer

Polymer A Multifunctional Chemical bond between polymer
(polar) compatibilizer end-group and the compatibilizer
(diblock copolymer)
Compatibilizer Chemical bond between the filler surface
Surface- and the compatibilizer
Polymer B treated
(apolar) fibers Physical bond between the filler surface
and the compatibilizer/polymer phase
Particulate
filler (apolar)

Fig. 3. Compatibilization strategies. The scheme in section i of (A) was redrawn from (18) with permission. The scheme in section ii of (A) was reprinted
and adapted from (19) with permission; copyright (2015) American Chemical Society.

Mohanty et al., Science 362, 536–542 (2018) 2 November 2018 4 of 7

COMPOSITE MATERIALS

IMAGES: (CLOCKWISE FROM TOP LEFT) ISTOCK/RAEVA, ISTOCK/HEINTEH, CLUBCOFFEE LP, ISTOCK/T_KIMURA, ISTOCK/BEN-SCHONEWILLE, A. K. MOHANTY, ISTOCK/THEBIAN, ISTOCK/ANTHIACUMMING into three types: partially biobased, fully bio- (e.g., PLA and Bio-PA) are being studied for au- made from renewable resources. Bio-PU can be Downloaded from http://science.sciencemag.org/ on November 1, 2018
based, and hybrid biocomposites. In accord- tomotive applications. More attention is now prepared from rubber seed oil monoglyceride
ance with the selected polymer resin, the resulting being devoted to the use of recycled content with reacting with diisocyanate (24). Combination of
composites may be thermoplastic or thermoset virgin plastics for the fabrication of composite PLA and PBS, and, in a larger sense, biodegradable
in nature. Figure 4 shows a schematic of bio- materials. However, the broader acceptance of aliphatic polyesters with natural fibers, can lead
composite production from some represent- these biocomposite materials in automotive ap- to biodegradable formulations (25). Because of
ative raw materials and their processing in plications depends on many factors, including their woodlike aesthetic, hybrid biocomposite
manufacturing, packaging, and consumer goods class A finishing, moisture repellence, structural formulations containing natural resins with lignin
areas. Natural fiber composites are more envi- stability, and flame-retardant properties. Sustain- and natural fibers were commercially successful
ronmentally friendly, economic, and lightweight able composites are used in auto parts such as when used in jewelry and musical instruments
than traditional glass or aramid fibers and trim panels, seat backs, packaging trays, spare (26). Coffee chaff, a lignocellulosic waste from
talc-filled composites in both thermoplastic and wheel covers, headliners, dashboards, and air- the coffee roasting industry, has been used to de-
thermoset platforms. They have many industrial baffle components. Apart from automotive com- velop compostable biocomposites for a disposable
uses, including applications in construction, auto- ponents, sustainable composites also receive food packaging application in coffee pods (27).
motive parts, and sporting goods. Biocomposites considerable attention in construction and pack- Kiwifruit skin waste biomass and PLA, as well
also have potential usage in electronics and aging applications. Tables 1 and 2 summarize as grape pomace—biodegradable polyester-based
specialty niche markets. A wide array of agro- a few representative biocomposites with their biocomposites—resulted in compostable knives
forestry biofibers (predominantly wood, as well key properties and industrial uses. Needle-punch and clips, respectively, for industrial applications
as flax, kenaf, and sisal) have been explored as flax/PP mats on compression molding result in (28). DDGS, a corn ethanol coproduct, has been
natural reinforcement or fillers for composite biocomposites with very high impact properties used as filler to increase the thermomechanical
fabrication. For auto manufacturers, one direct that may result from the aligned nature of the properties of PHA bioplastic and the biodegradation
benefit of using sustainable composites is greater fibers, along with high fiber loading (50%) (22). of the resulting composites, showing potential for
assurance of long-term price stability. Thus, The construction and municipal waste plastic- disposable agricultural applications (29). Chicken
many automakers continue to seek low-cost wood fiber–based biocomposites exhibited unde- feather fiber (CFF) waste from the poultry indus-
alternatives using nontraditional fibers and sirable properties compared with virgin plastic try, with glass fiber and epoxy resin, resulted in
fillers and matrix systems including “waste” LDPE-based wood-plastic composites (23). Multi- lightweight hybrid biocomposites (30). As com-
agro-forestry coproducts, waste rubber, cork, component systems using such mixed plastic pared with glass fiber–epoxy composites, the
and recycling waste (20). Another example is wastes (mostly PP and PE) deliver inferior per- CFF or CFF–glass fiber hybrid composites exhib-
the substitution of ground coconut shells (the formance due to incompatibility. Food wastes ited 30 to 40% density reduction because of in-
major by-product of the coconut processing provide another potential sustainable resource ternal void and lower aspect ratio of CFF as
industry) for mineral-based talc. Natural fiber for composite manufacture. The use of biofuel compared with glass fiber. The biocarbon from
composites in auto parts have been thoroughly coproduct and food processing wastes as filler pyrolyzed biomass and waste resources has
explored (21). Both reinforcement and matrices in biocomposites may help improve modulus, created opportunities to advance sustainable com-
are being substituted with sustainable materials. as compared with virgin plastic, while sacrificing posites, ranging from their uses in commodity
Plastics originating from renewable resources toughness. The composite matrix can also be thermoplastic such as PP (31) to high-melting

Materials Processes Composite pellets Injection Products
molding
Virgin plastics Pellets 5 of 7
Recycled plastics Extrusion Profile
(from petroleum or compounding extrusion
renewable resources)
Thermoplastic Composite sheets forming
Polymer
matrix Thermoset

+ Pre-processing Compression molding
Fibres/Fillers steps Thermoforming

Natural fibres Resin Vacuum-assisted resin
Recycled fillers transfer molding
Industrial co-products…
(woven, non-woven, Pultrusion
chopped/long/short
fibers, particulate or
their hybrids)

Fig. 4. Biocomposite product examples: From raw materials to manufacturing.
Mohanty et al., Science 362, 536–542 (2018) 2 November 2018

engineering plastic such as PET (32). Limitations (LCFs) (34). The diversity of lignin sources poses ous fiber–reinforced PLA composites with very Downloaded from http://science.sciencemag.org/ on November 1, 2018
of plant fiber in current biocomposite uses in- challenges in the manufacturing process. The high modulus and strength (39).
clude unwanted odor, hydrophilicity, and low pretreatment process and mechanical perform-
thermal stability. Because biofibers degrade ance, among other aspects, must be further Challenges in adopting sustainable
around 200°C, their widespread use in engineer- developed to bring more cost-competitive LCFs composites widely
ing plastics is restricted. In the automotive in- to commercialization. Nanocelluloses from agri-
dustry, tires and polyurethane-based products cultural and industrial waste have also attracted More eco-friendly composites with enhanced sus-
contain CB filler up to 50 weight %. Again, most attention as sustainable materials (35). Nano- tainability face challenges to their wide-scale ap-
of the interior auto parts are made in black with fibrillated cellulose and cellulose nanocrystals are plication. Measuring the sustainability of plastic and
the help of petro-based CB. Along with these two key types of nanocelluloses. Polymer- and reinforcement/fillers is a complex task affected by
components, the electronic housing products nanocellulose-based composites are under con- factors such as the nature of the feedstock, energy
are also made with CB as a colorant. The py- stant development (36). Melt processing of nano- input during production, durability, health im-
rolysis process also results in bio-oil and syngas, cellulose and thermoplastic has drawn more pacts, and after-life recycling or disposal (40).
which have been explored as raw materials for attention, and the major scientific challenges Biomass supply chains, which address types of
various grades of fuels and chemicals. In com- pertain to process development for improved biomass, harvesting and collecting strategies,
parison with traditional natural fibers, biocarbon dispersion of nanocellulose in the polymer transport and storage mechanisms, as well as
is thermally stable and is particularly suitable to matrix. Surface modification of nanocellulose processing methodologies, are complex in nature
reinforce or fill thermoplastic engineering plastics, is critical for improved fiber-matrix adhesion. and often vary with biomass type. It is necessary
like PET, for biocomposite uses. Traditionally as- Treatment of microfibrillated cellulose (MFC), a to establish a unified protocol for the effective
sociated with high strength and stiffness, the de- nanosized cellulose fiber, with silane changed utilization of bioresources, including waste re-
finition of advanced composites is evolving toward its surface characteristics from hydrophilic to sources. The sustainable method of expanding
expression of multifunctionality that may include hydrophobic without affecting the crystalline purpose-grown biomass, for example, requires
a combination of sophisticated mechanical prop- structure (37), and such modification improved the use of marginal agricultural land. Such an
erties with a high concentration of biobased fiber-matrix adhesion in MFC-epoxy composites. approach is essential for meeting the emerging
content, light weight, and electrical and thermal Green composites have been developed using massive requirement for biomass in the future.
conductivity. Appropriate functionalization of MFC-modified waxy maize starch–based bioresin Durability is a critical test for any biocomposite
bioresin with the intended reinforcement can and modified liquid crystalline cellulose through material proposed for replacing traditional syn-
result in marked performance improvements. hand lay-up and compression molding. Such thetic composite materials. To achieve function-
Highly functionalized resin derived from vege- advanced composites exhibit very high strength ality, biocomposite materials for automotive,
table oil reinforced with fiberglass fabric resulted (~800 MPa), thus creating new possibilities for construction, and other structural applications
in advanced biocomposites (33). Lignin-based structural applications (38). 3D printing, also need to deliver the required service life and long-
carbon fibers and nanocelluloses are considered known as additive manufacturing, can be widely term durability. Inclusion of bioplastic and re-
the next generation of biobased reinforcements used in sustainable composite manufactur- cycled materials in sustainable composite uses
for sustainable composite applications. Carbon ing, especially in biomedical, automotive, and poses major scientific challenges. Designing and
fiber is attracting attention for lightweight construction industries. 3D printing enables the engineering new classes of biocomposite mate-
composite uses. Synthetic carbon fiber is made creation of complex structures that cannot be rials that can exhibit high tolerance against
mostly from acrylonitrile. Lignin, being a renew- created by traditional composite manufacturing various external factors is essential. The classifi-
able resource, has been heavily researched for technologies. A 3D printing technique has been cation of biodegradable and nonbiodegradable
the development of lignin-based carbon fibers developed for processing unidirectional continu- composites is also important from an application
perspective. In addition to durable applications,

Table 1. Properties of representative biocomposites and their hybrids. –, not determined; MAPE, maleic anhydride–grafted polyethylene.

Resin Filler Impact strength Tensile Tensile Comments Reference
strength modulus

Plastic waste (PE and PP) Wood flour 2.9–6.2 kJ/m2 Unnotch 6–13 MPa MAPE compatibilization and (23)
2.3–3.9 GPa
lubricant utilization
............................................................................................................................................................................................................................................................................................................................................

PP Wood, poultry 8.1 kJ/m2 Notch 27 MPa Hybrid biocomposites–MAPP (31)
4.3 GPa
litter biochar compatibilization
............................................................................................................................................................................................................................................................................................................................................

PP Flax fiber 751 J/m Unnotch 40 MPa 6.5 GPa Needle-punch fiber (22)

mat composite
............................................................................................................................................................................................................................................................................................................................................

Neat and modified Starch/cellulose hybrid

Waxy maize starch liquid crystalline cellulose, – 505–790 MPa 22–32 GPa biocomposites (38)

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .m. . . .i.c. . .r. o. . .c. . .r.y. . .s. .t. .a. .l.l. .i.n. .e. . . .c. . .e. .l.l.u. . .l.o. . .s. .e. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Epoxy/acrylate Glass fiber 237 kJ/m2 532 MPa 37 GPa Methacrylated epoxidized (33)

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . N. . . .o. . .t.c. . .h. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .s. . u. . .c. . .r.o. . .s. .e. . . .s. . o. . .y. . a. . .t. .e. . . .r.e. . .s. .i.n. . ./. .g. . .l.a. .s. . .s. . . f. .i.b. . .e. .r. . . . . . . . . . . . . . . . . . . . . . . . .

Bio-polyurethane (Bio-PU) Sisal fiber – 57–119 MPa 1.2–2.2 GPa Rubber seed (24)

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .o. . .i.l. .p. . .o. . .l.y. .u. . .r. .e. .t. .h. . a. . .n. . .e. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

PBS/PLA Flax fiber 9.1-17.8 kJ/m2 Notch 39–55 MPa 3.6–7.4 GPa Fully biodegradable (25)

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .c. .o. . .m. . . .p. . .o. . .s. .i.t. .e. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Carbon fibers, Continuous fiber reinforcement

PLA twisted yarns – 57–185 MPa 5.1–19.5 GPa probed by 3D printing (39)

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .o. . .f. . .j.u. . t. .e. . . .f. .i.b. .e. . .r. .s. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Mohanty et al., Science 362, 536–542 (2018) 2 November 2018 6 of 7

COMPOSITE MATERIALS

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natural fibers furniture, headphones ACKNOWLEDGMENTS
.....................................................................................................................................................................................................................
Funding: This work is financially supported by the Natural
certain biocomposites are targeted for short life composites exhibit limited success because of Sciences and Engineering Research Council of Canada
cycles. These materials must adhere to international their cost and durability restrictions in automo- (NSERC)–Discovery Grants; the Ontario Ministry of Agriculture,
standards for biodegradability and compostabil- tive and/or housing structures. All-green com- Food and Rural Affairs (OMAFRA), Canada/University of
ity. One challenge is having the required compost- posites and biodegradable plastics are gaining Guelph Bioeconomy for Industrial Uses Research Program; the
ing facility at the disposal site of such materials. momentum in sustainable packaging. The use of Agriculture and Agri-Food Canada and Competitive Green
sustainable biocarbon fillers derived from waste Technologies through AgriInnovation Program; and the
Outlook biomass, industrial waste, and food waste dem- Ontario Research Fund, Research Excellence Program,
onstrates enormous potential for lightweight Round-7 (ORF-RE07) from the Ontario Ministry of Research,
Fossil fuel–based traditional composite structures sustainable composites in auto parts and other Innovation and Science (MRIS), Canada. Competing interests:
persist in the environment. Because they are growing demands from the manufacturing sec- The authors have no competing interests.
minimally recycled, these materials often end up tor. Achieving increased utilization of wastes and
being incinerated or placed in a landfill. In ad- undervalued industrial coproducts depends on 10.1126/science.aat9072
dition to fiber-reinforced composites, minerals creating a strong value proposition across the
such as talc and calcium carbonate–filled polymer entire value chain. The economic and functional
composites and/or their hybrids with fibers are merits of composites made from renewable and
being used widely in composite industries. Hybrid sustainable resources must be coupled with
biocomposites with petro- and biobased combi- leadership from industry executives and senior
nations, which are neither 100% fossil fuel–based government officials to drive global growth in
nor 100% biobased, have achieved some commer- this innovative class of materials for positive
cial success. Wood and other agricultural natural societal, environmental, and economic impacts.
fibers (flax, jute, etc.) used with petro-based plas-
tics (PP, PE, epoxy, etc.) are more eco-friendly REFERENCES AND NOTES
than 100% fossil fuel–based composites and have
found use in housing structures, decking indus- 1. Nat. Mater. 16, 691 (2017).
tries with wood plastic composites, other natural 2. Nat. Mater. 15, 113 (2016).
fiber–based hybrid biocomposites in automotive 3. United Nations Environment Programme, International
parts, and consumer products. Biocomposites
from recycled fibers and natural fibers have Resource Panel, www.unep.org/resourcepanel (2018).
also entered into consumer product applica- 4. “The new plastics economy: Rethinking the future
tions. Currently, all-green (i.e., 100% bio-based)
of plastics & catalysing action” (Ellen McArthur Foundation,
2017).
5. K. L. Pickering, M. A. Efendy, T. M. Le, Compos. A 83, 98–112
(2016).

Mohanty et al., Science 362, 536–542 (2018) 2 November 2018 7 of 7

COMPOSITE MATERIALS

REVIEW science and various branches of biology, including
functional morphology, evolutionary and devel-

Biological composites—complex opmental biology, and sensory physiology.
Multifunctionality of biological materials

structures for functional diversity Biological materials may need to simultaneous-
ly fulfill different functions to serve not only

the needs of the (living) organism but also the

Michaela Eder, Shahrouz Amini, Peter Fratzl* needs of populations, such as growth, locomo-

tion (7), signaling (8), repair, mechanical sta-

The bulk of Earth’s biological materials consist of few base substances—essentially bility (9), resistance against light irradiation (10)

proteins, polysaccharides, and minerals—that assemble into large varieties of structures. or against low temperatures (11), and the pos-

Multifunctionality arises naturally from this structural complexity: An example is the sibility for functional adaptation (12). Because

combination of rigidity and flexibility in protein-based teeth of the squid sucker ring. Other of this, Torquato et al. stated in 2003 that “the

examples are time-delayed actuation in plant seed pods triggered by environmental ultimate multifunctional materials are provided

signals, such as fire and water, and surface nanostructures that combine light manipulation by nature” (13).

with mechanical protection or water repellency. Bioinspired engineering transfers some of The potential for multifunctionality is inher-

these structural principles into technically more relevant base materials to obtain new, often ently contained in the fact that properties are

unexpected combinations of material properties. Less appreciated is the huge potential of tuned through the internal structure. In partic-

using bioinspired structural complexity to avoid unnecessary chemical diversity, enabling ular, hierarchical structuring that is omnipres-

easier recycling and, thus, a more sustainable materials economy. ent in biological materials opens the possibility Downloaded from http://science.sciencemag.org/ on November 1, 2018

of adopting different physical properties in dif-

T he challenges of life—from feeding to loco- and adaptive? How does nature combine several ferent size ranges (14). A typical example would
motion, communication, and protection— functions in one material? be structural colors that require features at the
require materials and systems to fulfill a submicron range corresponding to the wave-
large variety of functions. This has been Answers to such questions require considering lengths of visible light, whereas mechanical prop-
the driving force for the evolution of teeth, the function of biological materials in the natural erties may be controlled at different scales.
environment to which they adapt. An evolution-

skeletons, claws, and sensory systems. Although ary perspective can be particularly useful because Most biological materials are based on fibers as

natural materials have long been a prime source it may reveal how evolutionary pressures led to primary motif. Bone is an excellent example in

of inspiration for engineered ones, with our mod- the adaptation of material structure. As a con- which collagen fibers and mineral are assembled

ern tools from nanoscience that allow inspec- sequence, bioinspired materials research is a rela- into a great variety of structures that have dif-

tion and construction at the scale of molecules, tively new field at the interface between materials ferent mechanical performances (15). Bone is

research in this direction is rapidly expanding

(1–5). This may seem surprising at first glance,

given human development of steel construction,

copper wiring, and silicon chips. By contrast, the

major parts of biological materials are based on

just a few substances, polysaccharides (such

as cellulose and chitin), proteins, and a few min- Silica glass Calcium
erals (Fig. 1), which have considerably poorer phosphate
properties than engineering materials. But the

renewed interest in biological materials is pre-

cisely due to this fact: Natural organisms cannot

rely on materials selection (6) to design a system; Calcium Mineral Collagen
they have to generate it from the available basket carbonate

of base materials. Hence, the diversity of proper-

ties and functions of biological materials is less

due to a diversity of compositions than to a di- Protein
versity of structures (Fig. 1). For example, the pro-

tein keratin is used in gripping and snapping Sugar

tools (such as nails or beaks) and also for thermal Chitin Silk

insulation in wool; composites of protein and

mineral build skeletons and teeth; and chitin in

insects and arthropods is used to build carapaces

and sensory systems and to give structural color. Cellulose Keratin

A study of these materials leads to a number of

questions: How does one get valuable function-

ality based on cheap base materials? How does

one build a complex system based on little var-

iation in constituents so as to facilitate recycling?

Can we use structure to make materials active

Max Planck Institute of Colloids and Interfaces, Department Fig. 1. Biological materials are built with a limited number of building blocks, based on
of Biomaterials, Research Campus Golm, 14424 Potsdam, polysaccharides, proteins, and minerals. A diversity of structures leads to a diversity of functions in
Germany. tooth, bone, artery wall, tendon, spider web, beak, feather, wool, fingernail, tree, cotton, beetle carapace,
*Corresponding author. Email: [email protected] lobster shell, snail shell, mussel shell, and the skeleton of the glass sponge (clockwise from top).

Eder et al., Science 362, 543–547 (2018) 2 November 2018 1 of 5

not only the mechanical support for our body but ality through one type of protein building block Downloaded from http://science.sciencemag.org/ on November 1, 2018tinctive characteristic offers the possibility to
also the reservoir for some of the most important called “suckerins” and through their interactions Bioadhesivesprovide self-healing, adhesive properties and
ions for the functioning of cells: calcium and into complex structural arrangements and archi- high solubility and solution stability in weak
phosphate. More generally, hard-soft hybrid mate- tectures (19). The macroscopic geometrical ar- acidic solvents (e.g., acetic acid), as well as ther-
rials in the form of multilayers or tessellations rangement of the sucker ring provides excellent moplastic properties (19, 20), and nominates SRT
allow the tuning of a wide range of properties stability during the lateral bending of these for- as a model structure for a wide range of bio-
without a change in composition (16). midable teeth to facilitate an effective punctur- medical applications.
ing action actuated by their surrounding tentacle
The combination of toughness and strength musculature (21). As shown in Fig. 2, sucker ring Because of this reversible network, the SRT
is one aspect of mechanical functionality that teeth (SRT) consist of an oriented tubular struc- protein structure can be thermally processed,
has been studied extensively in biomaterials such ture with graded pore size and pore volume frac- molded, and reshaped with no or minimal changes
as nacre and bone (2, 17, 18). However, biodiversity tion. Given the homogeneous molecular structure in the intrinsic properties (26). This reversible
is huge, and many more examples of multifunc- and in the absence of cross-linking or metal ions protein network distinguishes SRT from related
tional biological materials have been and will be coordination (22), it is this graded distribution materials in the squid beak (27) or in insect exo-
studied. Here we focus on three examples. The of porosity that provides the graded mechani- skeletons (28). In such biological materials, the
first is a thermoplastic protein that is manufac- cal properties of SRT, which is a hallmark of many presence of a chitin-protein composite and inter-
tured into a graded porous material in the squid biological materials such as crustacean exo- chain covalent cross-links prevent the protein-
sucker ring. The second describes an example of skeleton (5). In peripheral regions, a smaller aceous matrix from any structural recovery, whereas
serotiny in plants, in which a seed capsule stays diameter and lower pore fraction promote higher the simplicity of the structural organizations at
closed for many years only to open and shed elastic modulus and hardness (23), which is re- the molecular scale promote self-assembly and
seeds during the first rain after a bush fire—all quired for gripping. A higher flexibility is ob- recovery in SRT. Such properties are attractive
this by a cellulose-based composite without the tained in the core zones by wider nanotubes for many applications (Fig. 2), including biomed-
help of living cells once the material is synthe- and a higher pore fraction. ical applications such as drug delivery and bio-
sized. The third discusses a range of organisms adhesives (19, 20).
for which light manipulation is performed by the The SRT proteins self-assemble to form a block
same material needed for mechanical protection copolymer structure, whereby nanoconfined Durable and multiresponsive
or for water repellency. b sheets (Fig. 2) promote rigidity, and an amor- encapsulation—Banksia seed pods
phous matrix provides flexibility (24). Moreover,
Thermoplastic material with graded the isotropic orientation of the b sheets, which Many plants do not release their seeds straight
properties and strong grip—squid differentiate them from the aligned b sheets in after maturation but rather wait for conditions
sucker ring teeth spider silk, tune their load-bearing characteristic that will provide better chances for distribu-
for compression and shear purposes. By contrast, tion and germination. The Australian plant genus
Despite a fully proteinaceous structure, the toothed the aligned b sheets of spider silk provide a su- Banksia stores seeds for up to 15 years in meta-
sucker rings of squid tentacles present remark- perior elasticity for uniaxial tension (25). In the bolically inactive closed pods (follicles; Fig. 3, A and
able physicochemical and thermomechanical absence of covalent bonds, the suckerins self- B) (29) before increased temperatures, as caused
characteristics, which, by far, transcend the prop- assemble through hydrogen-bond interactions by bush-fires, trigger seed release. The required
erties of their building blocks (19, 20). These to form a robust but sufficiently dynamic supra- opening temperatures are not only species de-
gripping tools, which are used for piercing and molecular network (24). Consequently, this dis- pendent (30) but can also vary within species
anchoring of prey, attain their multifunction- and adapt to geographic location and climatic

Simplicity in building blocks Graded pore size Diversity in properties, functions, and applications
and pore fraction
Oriented tubular structure 3D printing

Toothed sucker ring

Mechanical Thermoplasticity
strength

Optical transparency Self-healing

Solubility Biodegradability Drug delivery

Amorphous domains Biocompatibility
Crystalline β sheets

Isotropic β sheets
network

Semicrystalline structure

Fig. 2. Squid sucker ring teeth possesses a semicrystalline supramolecular network with variant physicochemical and thermomechanical
characteristics. Although SRT are entirely made of a protein family called “suckerins,” the different length scales in their tuned networks and
structural arrangement result in a diversity of properties and applications. [Image credit: The schematic image of the squid is reproduced from (21)
with permission from Mary Ann Liebert, Inc.]

Eder et al., Science 362, 543–547 (2018) 2 November 2018 2 of 5

COMPOSITE MATERIALS

conditions (31). Opening is initiated by increased increase our knowledge of biological material The iridescent green is achieved by continuous Downloaded from http://science.sciencemag.org/ on November 1, 2018
temperatures, but the seeds are not released im- functionalities and possibly evolutionary pro- multilayered concavities that reflect a yellow light
mediately (Fig. 3, C and G). Instead, they are held cesses. For example, a recent study of structural by a normal incident and a polarized blue light
back until a species-dependent number of rain- color in marine algae found similar optical struc- through a double reflection (43). By contrast, the
falls triggers seed release (Fig. 3, D and H) in an tures for light harvesting and radiation protec- iridescent blue in Morpho butterflies is formed
environment conducive for germination (32). tion in distantly related species (10). This example by discrete multilayers of the cuticle (Fig. 4) (47).
The seed pods, therefore, consist of a biological shows how biological materials science can help In addition to the coloration purposes, biological
composite that allows for decade-long durability reveal new examples of convergent evolution, in photonic structures have also been used for anti-
followed by a predefined deformation triggered which structures with similar form and function reflective properties and optical transparency.
and powered by two consecutive signals—heat develop independently from each other. On the The optical transparency of cicada wings and
and humidity—making it a small robotic device other hand, known examples of convergent evo- moth eyes attained by hexagon arrays of cone-
that can perform a simple task without an exter- lution might help in understanding and revealing shaped nanoprotuberances that provide a graded
nal energy source, triggered by a rare event. Thus, functionalities of biological materials. reflex index (44) aid in reducing reflection and
these seed pods may provide additional inspi- camouflage and in efficient light harvesting.
ration in the current quest for actuating soft Light-manipulating, superhydrophobic,
robotic devices (33–36). antimicrobial, damage-tolerant Optical properties generated by structures
mechanical devices—from insect wings offer the potential for combination with other
Durability for long-term seed storage and multi- to seashells functionalities. Numerous examples of this are
responsiveness for opening and seed release are found in nature (Fig. 4). The geometrical fea-
achieved by a structured functional composite Numerous organisms manipulate light for har- tures and arrangement of the nanopillars in
made of cellulose, hemicelluloses, lignin, wax, vesting and protection, communication, sensing, butterfly and cicada wings increase the surface
and tannins. Each follicle consists of two peri- camouflage, or mate attraction in sunny uplands, roughness and enhance antiwetting properties.
carp valves in the centimeter range. The valves dark forests, or marine ecosystems (41, 42). To Consequently, the reduced wettability promotes
are multilayers with endo-, meso-, and exocarp, achieve and tune optical functionalities, nature superhydrophobic characteristics (48), resulting
which have different cellulose orientations (37) has devised photonic structures which are tai- in self-cleaning and antibiofouling properties
that shrink by different amounts upon ripen- lored to manipulate light through optical phe- (44) such as those based on nanoprotuberance
ing and, thus, store internal stresses. They are nomena such as specular reflection, diffraction, arrays of the cicada wing (Fig. 4). Furthermore,
connected by the junction zone (Fig. 3, B, C, and transmission, collection, or a combination of the presence of these nanopillar features on the
E)—a tissue with a high surface area of inter- these effects (41, 42). Photonic structures can wing surface prevents bacterial fouling, because
digitating cells—that is sealed with wax that interact with light to acquire structural colors the physical shape of the pillars helps rupture the
melts at about 45 to 50°C (31, 38), temperatures by reflection (43), antireflectivity by diffraction cell membrane of adhering bacteria (44). Appli-
that can be reached on summer days in the field. (44), or optical transparency and light sensation cations of the multifunctional photonic structures
These waxes are not related to seed pod opening mechanisms by collection and transmission have not been limited to surface characteristics.
but instead contribute to follicle integrity in (45, 46). Probably the best-known examples of Beyond the reflection-diffraction effects, the bulk
creating a barrier against water loss and an an- structural colors are insect cuticles and wings photonic structures have been tuned to serve
tiadhesive film against wetting, insects, and mi- (44). The two-dimensional (2D) arrangements collection and transmission applications while
croorganisms. The low melting temperatures may of multilayered cuticle in Papilio palinurus (43) integrating optical characteristics with mechanical
furthermore seal microcracks, which probably and Morpho butterflies (47) are responsible for properties. Such structures can be found in the
arise during long-term exposure to environmen- their iridescent green and blue colors, respectively. integrated visualization system of chiton (46) or
tal challenges such as microbes, strong bird beaks,
or weathering. In addition to the self-sealing Durability Responsiveness
waxes, condensed tannins in the mechanically
weak parenchymatic tissue contribute to integrity Closed, long-term Temperature-triggered Water-triggered
by a high antioxidative capacity and increased
water retention ability (39, 40). seed storage first opening second opening

In Banksia attenuata, the initial opening tem- AB C JZ opening D crack on
peratures and the dimensional stability depend
on internal follicle geometry, in particular, on the JZ JZ opening one side
radii of the biaxially curved follicle interiors (31), JZ
indicated by the white line in Fig. 3F. Opening cJrZack on
at increased temperatures occurs by the soften-
ing of the endocarp (green layer in Fig. 3, F and one side
G), which changes the internal force balance and
allows the stored prestresses to be released (31) inner curvature JZ
by the formation of a crack and an initial open-
ing of the junction zone (Fig. 3C). Further open- E F seeds G H
ing for seed release (Fig. 3D) requires wetting
and drying cycles, which activate bending of the JZ JZ
endo-mesocarp bilayer (32) (Fig. 3H).
Fig. 3. Opening of B. attenuata infructescences (cones) collected in Western Australia.
The B. attenuata example illustrates how (A to D) Cones from the North [(A), left side] contain mainly closed follicles (B). Half-open
adaptation strategies and (multi)functionalities (C) and open follicles (D) are frequently found on cones in the South, where opening
in biological materials can be better understood temperatures are lower [right infructescence in (A)]. (E) Light micrograph of the junction
by including ecological aspects in biomaterials zone (JZ) sealed with wax (scale bar 100 mm). (F to H) Virtual cuts through micro-tomographic
research. Furthermore, it highlights the impor- reconstructions of closed (F), half-open (G), and open follicles (H) showing the seeds with the
tance of sampling biological tissues in their nat- separator in between [(F) and (G)] and the endocarp-mesocarp bilayer (colored in green and
ural environments and of relating their properties yellow in one of the two pericarp valves). The white line in (F) indicates the internal valve
to the environmental challenges in those habi- curvature, which changes with geographic location and climate.
tats. Comparative studies between species also

Eder et al., Science 362, 543–547 (2018) 2 November 2018 3 of 5

Sensation Multifunctional photonic structures Antireflection

Coloration

1 µm 30 µm 1 µm 1 µm 1 µm
Mechanical protection
Antibacterial, camouflage Downloaded from http://science.sciencemag.org/ on November 1, 2018
Superhydrophobicity, antibiofouling, self-cleaning

Fig. 4. Biological photonic structures with additional integrated func- biofouling, self-cleaning, and antibacterial properties. [Image credits: From
tionalities. These photonic structures are honed to manipulate light for left to right, chiton, adapted from (46) and reprinted with permission
photosensation, coloration, or optical transparency purposes while from the American Association for the Advancement of Science; brittlestar,
achieving additional characteristics through the architectural arrangement adapted with permission from Springer Nature (45); blue-rayed limpet,
of the same structural materials. The mechanical robustness of the chiton adapted from (50); morpho butterfly wing, adapted and reformatted
and brittlestar lenses (left) have been attained along with light transparency from a micrograph by Shinya Yoshioka (Osaka University) and (47) by
for photosensation mechanisms. The surficial architectures of the permission from Springer Nature; and cicada wing, adapted and
butterfly and cicada wings (middle and right) provide superhydrophobic reformatted from (44) and (52) by permissions from Annual Review, Inc.,
surfaces and consequently promote other characteristics such as anti- and IOP Publishing, respectively.

the light sensory system of the brittlestar (Fig. 4) characteristics through manipulation of the archi- a material that can be used in building construc-
(45, 49). The chiton dorsal shell, which is used as tecture using available materials. tion, but it is also a device that fulfills several
a biomineralized armor for protection, contains functions for the plant, from mechanical sup-
translucent lenses dispersed across the shell plate. Outlook port to water and nutrient transport. In similar
Similar to the shell structure, these microlenses ways, most of our organs, such as muscle or bone
are made of aragonite; however, the highly aligned These examples of biological materials systems and even liver, might be considered functional
crystalline structure of the lenses, as well as a lower mostly function without direct action of living devices or materials. When translating this into
amount of intercrystalline organic domains, min- cells. Hence, they are composite materials in the engineering, the same comment applies: Multi-
imizes light scattering (46). Similarly, the dorsal engineering sense, synthesized for specific func- functional materials need to incorporate knowl-
arm plates of brittlestars are covered with a 3D tions that are important for the organism. These edge about the desired function to be useful.
network of microlenses (Fig. 4), which are com- materials based on proteins and polysaccharides Whereas nature grows materials, organs, and
posed of single calcite crystals (45, 49). These are not meant to last forever but rather to be re- whole organisms from the base substances it
photosensory organs can collect and transfer the used, degraded, or even digested. For this to be can synthesize, today’s engineering processes
light to the dermal receptors while providing possible, it is a great advantage that all materials are based on a separation of tasks and knowl-
mechanical protection for the animal. of a given organism are of the same general type edge fields, from chemistry, materials science,
with additional functionality being introduced production engineering, and device develop-
A prominent example of composite photonic by structure rather than by the addition of mate- ment all the way to product design, with var-
architectures is the mineralized blue-rayed limpet rials with different chemical composition. Instead ious selection and assembly processes along
shell (Fig. 4), which is tuned to attain mechanical of durability, which is a hallmark of many engi- this chain. The advantages of a more integrated
robustness while achieving three differentiated neering materials, the strategy pursued by na- approach have been recognized in many areas,
optical properties: transparency, selective reflec- ture is a material lifetime adapted to the function, for example, in biomaterials development in
tion, and absorption (50). In this shell, which is followed by degradation and reuse (by the same which the compatibility and the communica-
decorated with bright blue strips, the translu- or by different organisms). This is greatly facili- tion of materials with cells and organs is an
cency is achieved through an irregular lamellar tated by the fact that there is not too much di- essential part of the materials research itself. Re-
structure at the outer layer. By contrast, the se- versity in the combination of materials (51), so search on materials and on functional devices
lective reflection of blue-green light is created by that enzymes for degradation are readily avail- are traditionally close in the textile industry or
means of a co-oriented calcite lamellae structure. able, for example. Hence, nature’s paucity of base architecture. In general, an increased interaction
Beneath this multilayer zigzag structure (Fig. 4), materials could actually be an advantage when of materials scientists with product designers
a disordered layer composed of amorphous col- we use this to inspire a new materials economy could reduce the distinction between material
loidal particles absorbs the light to provide better with fewer materials that are structured specif- and functional device in all areas of engineer-
contrast (50). These examples illustrate how na- ically for the function we need. ing and, thus, provide a growing need for the
ture develops site-specific design strategies to development of multifunctional materials.
achieve the required functionalities and variant Multifunctionality blurs the distinction be-
tween material and device. A tree stem is clearly

Eder et al., Science 362, 543–547 (2018) 2 November 2018 4 of 5

COMPOSITE MATERIALS

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Eder et al., Science 362, 543–547 (2018) 2 November 2018 5 of 5

COMPOSITE MATERIALS

REVIEW CNT or graphene dispersions. Second, the surfaces
of both graphene and nanotube are atomically
Composites with carbon nanotubes smooth, devoid of any dangling bonds or defects
and graphene: An outlook (except at the edges in graphene or tips in
nanotubes), which means that strong matrix-
Ian A. Kinloch1, Jonghwan Suhr2, Jun Lou3, Robert J. Young1, Pulickel M. Ajayan3* filler bonds are hard to accomplish, leading to
poor interfacial load transfer during mechanical
Composite materials with carbon nanotube and graphene additives have long been deformation (1) and high electron and phonon Downloaded from http://science.sciencemag.org/ on November 1, 2018
considered as exciting prospects among nanotechnology applications. However, after scatter, compromising electrical and thermal
nearly two decades of work in the area, questions remain about the practical impact of properties. This interfacial problem was a major
nanotube and graphene composites. This uncertainty stems from factors that include poor roadblock in carbon fiber composites before
load transfer, interfacial engineering, dispersion, and viscosity-related issues that lead to industry figured out the sizing of fibers via
processing challenges in such nanocomposites. Moreover, there has been little effort chemical modification, but for nanotubes and
to identify selection rules for the use of nanotubes or graphene in composite matrices for graphene, this problem is severe, and attempts to
specific applications. This review is a critical look at the status of composites for chemically functionalize CNT or graphene surfaces
developing high-strength, low-density, high-conductivity materials with nanotubes or may substantially compromise their intrinsic prop-
graphene. An outlook of the different approaches that can lead to practically useful erties (4). This compromise also relates to a third
nanotube and graphene composites is presented, pointing out the challenges and issue, which is the inhomogeneous dispersion of
opportunities that exist in the field. nanotubes and graphene in the matrix. Without
proper surface treatments, CNTs or graphene tend
C arbon nanomaterials have had an unprec- We will consider three important questions to aggregate easily, owing to strong van der Waals
edented impact over the past three dec- that may broadly define the fate of this field. interactions between them, to form poorly dis-
ades in defining the reach and applications Why should these unique structures be of any persed bundles or agglomerates in the matrix,
of nanotechnology. Starting with the dis- interest in composites, why have they not pro- which often leads to poor interfacial connectiv-
covery of fullerenes and moving through duced substantial progress after much effort, and ity and formation of mechanical stress concen-
the carbon nanotube (CNT) era to graphene and what can be done to make them work as good tration or other functionally singular sites,
other two-dimensional (2D) materials, the aca- reinforcements in composites? The discussion resulting in severely affected composite perform-
demic world has been flush with new ideas, in- will go beyond just that of mechanical proper- ances. Noncovalent functionalization methods
ventions, and innumerable attempts to find the ties and also consider their excellent electrical (5) could be used to partially overcome the dis-
killer applications for these remarkable nano- and thermal properties. persion challenge, but this approach is ineffective
structures. Here we will discuss one such ap- in solving the interface problem. Therefore, a
plication, which when first introduced seemed Graphene represents the thinnest possible systematic and careful engineering approach is
close to embracing these materials but for var- atomically flat layer, made of a planar hexagonal needed to design CNT or graphene composites with
ious reasons has not met expectations: that of honeycomb lattice of strong C-C bonds that build optimal performances (Fig. 1). We can show the
composite materials. In particular, the question up graphite when stacked via weak van der Waals potential for using CNT or graphene composites for
of whether structures such as carbon nanotubes interlayer forces. Graphene has a Young’s modulus applications by plotting the hypothetical position
and graphene, touted as ideal reinforcements in near 1 TPa in the plane, reflecting the intrinsic of different CNT or graphene composites in a mod-
composite matrices because of their mechanical carbon bond stiffness, but being very thin, it can ified Ashby plot (Fig. 1B) and the position of fu-
properties, really are the right choices for me- be flexible in bending, twist, and other deforma- ture continuous CNT or graphene fiber composites.
chanical reinforcement still remains largely un- tion modes (2). The in-plane electrical and ther- Finally, the ideal dispersion of material through-
answered. Moreover, the realm of functionalities mal conductivities are the highest among known out the composite is very application dependent;
that can be accessed by introducing nanotubes materials, but the through-thickness properties of typically for mechanical properties, one wants
versus graphene in a matrix needs careful eval- stacked graphene are very poor. CNTs are rolled- as high a loading of the filler as possible that is
uation and thought. Although both are sp2 up graphenes with the in-plane properties trans- aligned in the direction of the load, whereas for
allotropes, the structure, morphology, and di- lated to axial properties, making them among electrical percolation, one aims for a random
mensionality of these two profoundly interesting the stiffest axial fibers ever created. Similar to percolated network with as low a concentration
carbon nanostructures are indeed quite different, graphene, they can also be easily bent, twisted, as possible. For multifunctional applications, the
and so is the nature of their interactions with and buckled (3). As graphene stacks up to make required microstructures may therefore even be
the adjacent matrix (1). Hence, the overall com- multilayer structures, CNTs can also have a nested contradictory.
posite mechanical behavior provided by these structure of tubes inside tubes [single-walled
two reinforcement units could be distinct. It (SWNTs) to multiwalled nanotubes (MWNTs)], Carbon nanotube and graphene fillers,
would indeed be useful to have selection rules which has a notable effect in determining their interfaces, and load transfer
that choose one over the other in composite mechanical properties. In general, although the
applications, but no such rational approaches local stiffness that can be measured is extremely A great deal of effort has been made to de-
have emerged in the design of nanocomposites high, owing to a near defect-free structure of velop lightweight, strong composite materials
with CNT or graphene phases. graphene and nanotubes, a couple of major with CNTs and graphene as reinforcement, and
issues make reinforcement of these structures although these are considered to be discon-
1National Graphene Institute and School of Materials, in matrices challenging. First, both graphene tinuous short fillers, they possess outstanding
University of Manchester, Manchester M13 9PL, UK. 2School and nanotubes are particulate fillers, with their mechanical properties. The extremely high Young’s
of Mechanical Engineering and Department of Energy larger dimensions (lateral size of graphene or modulus of CNTs and graphene, their nanoscale
Science, Sungkyunkwan University, Suwon, 16419, South lengths of nanotubes) reaching several hundred dimensions, along with particular geometries
Korea. 3Department of Materials Science and NanoEngineering, micrometers at the most or, in exemplary cases, that offer high specific surface area, present un-
Rice University, Houston, TX 77005, USA. millimeters. Short fibers are generally poor load precedented opportunities to efficiently tailor
*Corresponding author: Email: [email protected] carriers in fiber composites, and this effect is the interface properties between the reinforce-
clearly seen when composites are made with ments and composite matrices. CNT or graphene
nanocomposites may not be as strong or stiff as
a continuously reinforced composite such as
typical carbon fiber laminates that are currently

Kinloch et al., Science 362, 547–553 (2018) 2 November 2018 1 of 7