SIMON LEVIN wins National Medal of Science for unraveling ecological complexity

Simon Levin

Simon Levin (Photo by Brian Wilson)

Simon Levin, the James S. McDonnell Distinguished University Professor in Ecology and Evolutionary Biology, received a National Medal of Science, the nation’s highest scientific honor. Levin was honored at a White House ceremony in early 2016 along with eight fellow Medal of Science recipients, and eight recipients of the National Medal of Technology and Innovation.

Levin focuses his research on complexity, particularly how large-scale patterns — such as at the ecosystem level — are maintained by small-scale behavioral and evolutionary factors at the level of individual organisms. His work uses observational data and mathematical models to explore topics such as biological diversity, the evolution of structure and organization, and the management of public goods and shared resources. While primarily related to ecology, Levin’s work also has analyzed conservation, financial and economic systems, and the dynamics of infectious diseases and antibiotic resistance.

Big answers from small creatures

A graduate student tracks the spread of viruses from bats to humans in Madagascar

By Cara Brook

IT IS SPRINGTIME in the Makira-Masoala peninsula of northeastern Madagascar, and the lychee trees are in full fruit. I sit crouched with my research team in camping chairs as dusk settles, our eyes intent on Rousettus madagascariensis, one of three species of endemic Malagasy fruit bat. The fox-faced bats flit deftly amongst the leafy branches, dodging our nets as they search out juicy pink fruits for their evening meal.

Our quiet vigil is interrupted by the arrival of a whistling gray-haired man from the nearby village who carries a net strung on a pole in one hand and a garish yellow plastic fuel can in the other. With a nod to us, he strides up to a neighboring tree and expertly scoops five of the feasting bats, pins the net to the ground with a bare hand, and coaxes the bats one-by-one into his yellow can. Mission accomplished, he straightens up with a wink and turns back home, rattling his can of bats in time to his whistle as he walks.

Handeha hihinina andrehy izy?” I ask my Malagasy colleagues in astonishment. Is he going to eat the bats? Laughing at my horror, they nod in affirmation.

Bats as reservoirs

I study zoonotic diseases, infections that transmit from wildlife to humans, as a graduate student in Princeton’s Department of Ecology and Evolutionary Biology. Bats are native reservoir hosts — meaning they host viruses without getting sick — for a number of the world’s most dangerous human diseases, including rabies, Ebola and SARS. I want to understand how bats host these viruses without getting sick and what factors contribute to the viruses’ spillover to human populations.

Field lab

Graduate student Cara Brook (rear) and colleague Christian Ranaivoson, a graduate student at the University of Antananarivo and an intern with the Pasteur Institute of Madagascar, process fresh bat fluids in their field lab in Maromizaha, Madagascar, in September 2014. (Photo by Deborah Bower.)

A lot of my work involves building mathematical models to understand disease. When I started graduate school, I barely understood what a “model” was. Four years later, I recognize that a model is simply a representation of reality — it can be physical, like a model of the solar system; experimental, like a mouse that a scientist infects to monitor disease progression; or mathematical, like the equations we use to describe disease transmission in my field of disease ecology.

The goal is to build simple models that still adequately represent reality. One of my professors, Bryan Grenfell, once told me, “If you apply a complex model to a complex system, then you have two things that you don’t understand.” If we can understand our models, then we can learn by observing the differences between these models and the more complex reality.

In disease ecology, our simple models are mathematical equations that class all potential disease hosts — bats, in my research — into three categories: (1) susceptible to infection; (2) currently infected; or (3) recovered from infection and now immune. We use our equations to predict how the proportion of hosts within each category changes over time, and then we collect data to determine whether our predictions match reality.

Remote corners

One of the ideas we are testing is whether bats are fundamentally different from other mammals in their capacity for resisting or tolerating viral infections. I build models depicting the spread of infected cells within individual bats and explore the physiological processes that might allow a bat cell to host a replicating virus without experiencing the cellular damage that causes the host to feel sick.

In the lab, I grow layers of bat cells, infect them with virus, and monitor cell-to-cell viral spread. Then I compare these data with what is predicted in my models. If the data match the model, then maybe the mechanism for disease mitigation that I chose for my model also is the one used in real life.

At a population level, bat-virus transmission, including spillover, peaks in the winter, and we want to know why. I build population-level transmission models that incorporate different seasonal pathways to cause winter infections, then I try to match those models to data. Collecting field data is hard — I spend years trekking to remote corners of Madagascar, mastering obscure Malagasy dialects, and rigging complex pulley systems out of nets, fishing lines and carabiners.

At the end of it all, like the man in Makira- Masoala, I catch a few bats. Instead of cooking them for dinner, however, I use fine-gauge needles, cryogenic vials and sterile swabs to collect their blood and other bodily fluids before I let them go. I haul the fluids in vats of liquid nitrogen to the laboratories of the Pasteur Institute of Madagascar in the capital city of Antananarivo. From there, samples are shipped to collaborators in London, Berlin, New York and Washington, D.C., while others remain in-country. My collaborators and I perform a variety of tests on these transported fluids to ascertain whether the bats were susceptible, infected or recovered from infection at the time of sampling.

When all is said and done, the results are sometimes difficult to interpret. Science is a gradual process, and the goal is to always narrow the window of possible hypotheses at least a little bit.

For me, science is a recognition of, as John Steinbeck put it, “how man is related to the whole thing.” I’m still trying to understand how humans fit into the zoonotic cycle of disease. I’m nearing the end of my Ph.D., but I have enough questions to keep me going for a lifetime.

Cara Brook is a fifth-year doctoral student. Her advisers are Andrew Dobson, professor of ecology and evolutionary biology; Bryan Grenfell, the Kathryn Briger and Sarah Fenton Professor of Ecology and Evolutionary Biology and Public Affairs; Andrea Graham, associate professor of ecology and evolutionary biology; and C. Jessica Metcalf, assistant professor of ecology and evolutionary biology and public affairs. Brook’s research is funded by the National Science Foundation, the National Geographic Society and PIVOT, a Madagascar-based health care nongovernmental society.

Wild birds: A trip to the market reveals species imperiled

Wild Birds

“Wild birds are being vacuumed out of the forests, gardens and fields of Indonesia, and we have to quickly figure out which species are in danger of extinction.” –David Wilcove, professor of ecology and evolutionary biology and public affairs in the Woodrow Wilson School

THE SIGHT OF A SOUTHEAST ASIAN BIRD market rivals the din of one for being overwhelming. Thousands of wild-caught birds are packed into cages that hang from eaves and fill market stalls to the ceiling, lining the paths trod by prospective buyers like a living wall. Taken from fields and forests, these birds are prized for their song, their colors, their spiritual significance or their long-time association with status and wealth. For the people who come to these markets, the birds — young and old, endangered and common — have meaning and value.

But to scientists, conservationists and governments, the wild-pet trade is a destructive yet unmonitored and elusive force on wildlife populations.

Princeton University researchers went deep into the wild-bird markets and trapping operations on the Indonesian island of Sumatra to document the draining of species by the pet trade. They found there a new and interesting weapon in the struggle to gauge — and halt — the devastation of the wildlife trade on animal populations: the very markets where the animals are bought and sold.

Species that are disappearing as a result of the pet trade can be identified by changes in their market prices and trade volumes, a study led by the Princeton researchers found. The researchers studied open-air pet markets on Sumatra from 1987 to 2013 and found that bird species that increased in price but decreased in availability exhibited plummeting populations in the wild.

The researchers concluded in the journal Biological Conservation in July 2015 that a prolonged rise in price coupled with a slide in availability could indicate that a species is being wiped out by its popularity in the pet trade. Through regular pet-market monitoring, conservationists and governments could use this information as an early indicator that a particular species is in trouble, the researchers reported.

Lead author Bert Harris, who was a postdoctoral fellow in the Program in Science, Technology and Environmental Policy in Princeton’s Woodrow Wilson School of Public and International Affairs when the work was conducted, said that market monitoring can be done far more quickly and cheaply than field-based monitoring of wild populations.

birds

Birds such as the Oriental white-eye (top photo ) are packed into tight cages where they are at risk of disease. Many Asian and African countries host a startling number of species yet have lax-to-nonexistent monitoring and conservation programs. The Princeton researchers’ market-monitoring method can be done far more quickly and cheaply than field-based monitoring of wild populations. PHOTO COURTESY OF DAVID WILCOVE

One important function of the study is to highlight the pet trade as an emerging threat facing many birds and other wildlife, one that can act independently from other drivers of extinction such as habitat loss, said senior author David Wilcove, a professor of ecology and evolutionary biology and public affairs in the Wilson School.

He and Harris worked with co-authors Jonathan Green, who was a Princeton postdoctoral researcher in the Wilson School and is now at the University of Cambridge; Xingli Giam, who earned his Ph.D. at Princeton in 2014 and is now at the University of Washington; and researchers from the Wildlife Conservation Society and the Indonesian Institute of Sciences.

“Wild birds are being vacuumed out of the forests, gardens and fields of Indonesia and we have to quickly figure out which species are in danger of extinction,” Wilcove said. “We’ve got to change how we tackle this problem.”

Carter Roberts, president and CEO of the World Wildlife Fund, said that the researchers’ use of wildlife-trade market data to identify endangered species is a “potentially breakthrough idea.”

“What I think makes this paper so exciting is that it suggests a two-pronged approach to addressing the threat to biodiversity posed by the wildlife trade: using market data to identify the species that are likely being severely overexploited, and then targeted research and conservation efforts at those species,” Roberts said.

The researchers found that 14 birds popular in Sumatran pet markets were identified by local experts as declining or severely declining — yet, only two are officially recognized as imperiled. In addition, only two species are restricted to old growth forests, meaning that deforestation alone could not explain the declines. The pet trade was clearly a culprit, too. Furthermore, the researchers found that six species that are not popular as pets exhibited population increases. The researchers confirmed their method by studying the cases of two birds that are critically endangered by the pet trade — the yellow-crested cockatoo and the Bali myna.

Existing studies have explored wildlife markets, but only documented a species’ market volume, or availability, Harris said. The Princeton-led study, which was supported by the High Meadows Foundation, is the first to consider price and market volume. Market availability alone can fluctuate for reasons unrelated to a species’ wild population, such as a decrease in popularity, he said.

During the course of the research, Harris visited bird markets to gather price and availability data. They are chaotic places where Westerners asking about prices are viewed with suspicion.

“The markets are the dirty part of conservation,” Harris said. “They’re noisy and smelly. And after someone who looks like me asks about prices two or three weeks in a row, sellers just stop responding.”

Wilcove was inspired to conduct the current research after a trip to Sumatra when he noticed a prevalence of wild-caught pet birds. Research has found that 22 percent of Indonesian households own birds.

One bird the researchers identified as declining in the wild, the white-rumped shama, which is prized for its song, can be raised in captivity. Yet people seem to prefer the wild individuals, Wilcove said. He and Harris want to explore how governments and conservation groups can convince people to keep captive-raised birds.

“It’s time for some new approaches,” Wilcove said.

–By Morgan Kelly

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Student identifies difference between the dinosaur sexes

Evan Saitta

PHOTO BY DENISE APPLEWHITE

THE DISCOVERY OF A SINGLE ANATOMICAL DIFFERENCE between males and females of a species of Stegosaurus provides some of the most conclusive evidence that some dinosaurs looked different based on sex, according to research published in PLoS One and conducted by Evan Saitta while he was an undergraduate at Princeton.

The study found that the back plates of the species Stegosaurus mjosi came in two varieties that indicated the animal’s sex — short and wide, and tall and narrow. Females had one type of plate and males the other. The lack of a particular female-specific bone tissue found in birds and some dinosaurs, however, made it difficult to determine which sex had which plate type.

Saitta, who graduated from Princeton in 2014 and conducted the research for his senior thesis project, drew from existing animals, particularly horned animals, to suggest that the distinct shape of male and female S. mjosi plates indicated two different functions. He supposes that the tall, narrow plates belonged to females, who would have needed the pointier plates to defend themselves against predators. The wide plates, which were 45 percent larger in surface area, likely served as “billboard” displays males used to attract females, similar to the plumes of the male peacock.

Beyond the implications for Stegosaurus, the research establishes that sexual dimorphism — in which males and females of a species have distinct physical forms — could exist in non-avian dinosaurs, a group that includes iconic reptiles such as Tyrannosaurus and Brontosaurus, Saitta said. Existing work on sexual dimorphism in non-avian dinosaurs had been inconclusive. Saitta is now a graduate student at the University of Bristol in the United Kingdom.

Andrew Farke, the Augustyn Family Curator of Paleontology at the Raymond M. Alf Museum of Paleontology in Claremont, California, said that the work provides a potential foothold for other researchers wanting to explore sexual dimorphism in Stegosaurus and possibly other non-avian dinosaurs.

“This is very species specific, so there’s a lot of work that needs to be done to extend this to other animals,” said Farke, who is familiar with the study but had no role in it. “It’s not the end of the road, but I think it will stimulate people to look at this issue in Stegosaurus.”

–By Morgan Kelly

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Measles may weaken immune system up to three years

Measles vaccination

Measles may weaken immune system up to three years. PHOTO BY SHUTTERSTOCK

THE MEASLES VIRUS can lead to serious disease in children by suppressing their immune systems for up to three years, according to a study published in the journal Science on May 8, 2015. The study provides evidence that measles may throw the body into a much longer-term state of “immune amnesia,” where essential memory cells that protect the body against infectious diseases are partially wiped out. This vulnerability was previously thought to last a month or two.

“We already knew that measles attacks immune memory, and that it was immunosuppressive for a short amount of time. But this paper suggests that immune suppression lasts much longer than previously suspected,” said C. Jessica Metcalf, co-author and assistant professor of ecology and evolutionary biology and public affairs, who is affiliated with Princeton’s Woodrow Wilson School of Public and International Affairs.

The research findings suggest that — apart from the major direct benefits — measles vaccination may also provide indirect immunological protection against other infectious diseases.

The work was funded by the Bill & Melinda Gates Foundation, the Science and Technology Directorate of the Department of Homeland Security, and the Research and Policy for Infectious Disease Dynamics (RAPIDD) Program of the National Institutes of Health’s Fogarty International Center.

–By B. Rose Huber

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SIMON LEVIN Receives Tyler Prize for Environmental Achievement

Simon Levin

Simon Levin (Photo by Brian Wilson)

Simon Levin, the George M. Moffett Professor of Biology, was awarded the 2014 Tyler Prize for Environmental Achievement for bridging ecological research and environmental policy, economics and social science.

Levin received an award of $200,000 with the prize, which was established in 1973 and is awarded by the international Tyler Prize Executive Committee with the administrative support of the University of Southern California. Levin received the prize at a ceremony on April 25, 2014, in Los Angeles.

Levin, whose research has revealed the multifaceted relationships between species and ecosystems, has played a foundational role in shaping environmental policy and advancing the study of complex ecosystems, according to the Tyler Prize Executive Committee.

“What is so impressive about Simon Levin and his work is that he is a connector,” said Owen Lind, chair of the committee and a biology professor at Baylor University. “His work has bridged the theoretical with the work of ecologists in the field, and connected complex ecological systems to social science and environmental and public policy. It is rare to see one expert have such a dramatic impact on so many fields.”

–By Holly Welles

Striking resemblance: A physical law may govern very different biological activities

Starlings

FLOCKS OF BIRDS FLY ACROSS THE SKY in shifting configurations. In the retina of an eye, millions of neurons ignite in ever-changing combinations, translating light into meaningful images. Yet both of these seemingly random behaviors have an underlying order that can be described by mathematics.

Like these cells and birds, when atoms and molecules come together they can display coordinated behaviors that are more than the sum of their parts. At a critical point, such as the boundary between liquid and gas, local interactions between molecules propagate through an entire material, changing its essential properties.

Princeton biophysicist William Bialek thinks criticality may also underlie collective behaviors in living organisms, and he’s using real-world data to test this hypothesis. Recently, Bialek and his colleagues have analyzed the flocking behaviors of birds, the genetic networks of fruit fly embryos and the activation patterns of salamander neurons.

“In physics, we use the same mathematical language to describe many seemingly different behaviors,” said Bialek, the John Archibald Wheeler/Battelle Professor in Physics and the Lewis-Sigler Institute for Integrative Genomics. “So we understand that the emergence of collective behavior from all the individual interactions has a kind of universality.”

To explore the possibility that this universality might extend to living systems, Bialek made use of a large dataset on the changing positions and velocities of thousands of individual birds in a flock of starlings. A group of Italian physicists used multiple cameras to record the birds and calculate their exact locations over time in three dimensions — “a technical triumph,” according to Bialek.

The researchers, including former Princeton postdoctoral fellows Thierry Mora and Aleksandra Walczak, analyzed the deviations of each bird from the flock’s average speed and direction of movement. They found not only that these variations were correlated between nearby birds, but also that the fluctuations from the average propagated through the group over long distances. This pattern of rapid, remote signal transmission echoes the changes that occur among molecules during a phase change from solid to liquid or liquid to gas. At a critical point, this could allow information to spread swiftly through the group, enabling the whole flock to nimbly change direction.

“The model you build just by keeping track of what each bird does relative to its neighbors predicts what happens throughout the entire flock,” Bialek said. “And it does so with an accuracy that is beyond what we had any reason to expect. It’s really a very precise prediction.”

Other biological examples of criticality play out on a microscopic scale. Bialek has an ongoing collaboration with Princeton’s Squibb Professor in Molecular Biology Eric Wieschaus, a Howard Hughes Medical Institute researcher and Nobel Prize winner, who has uncovered many of the genes involved in the embryonic development of the fruit fly — a model biological system.

Bialek has found signatures of criticality in gene activation patterns during the first few hours of fly embryo development. The synchronized actions of “gap genes” establish the fly’s 14-segment body plan. Mutations in these genes lead to gaps between segments, whose effects are reflected in the names of the genes: two examples are “hunchback” and “giant.”

Recently, Thomas Gregor, an assistant professor of physics and also a member of the Lewis-Sigler Institute, has developed experimental tools to precisely measure the activity of many gap genes at once, all along the halfmillimeter length of the fly embryo. These measurements allowed Bialek and physics graduate student Dmitry Krotov to test whether the patterns of gene activity across the embryo fit a model of criticality. Indeed, using data from 24 embryos, they found that fluctuations from the average level of gene activity at each point along the embryo were correlated between certain pairs of gap genes, which regulate one another’s activity like on/off switches. They mapped the locations of these switch points, which appear to act like signals that spread over long distances, just as changes in velocity are correlated in a flock of birds.

Bialek has also looked for signatures of criticality among the activation patterns in a patch of 160 nerve cells from a salamander retina, a model system for studying this light-sensing layer of the eye. In collaboration with Michael Berry, an associate professor of molecular biology and the Princeton Neuroscience Institute, Bialek and his colleagues showed how the coordinated activity of the neurons could be tuned to a critical state.

Bialek thinks critical systems may be common features of life that have repeatedly evolved in different organisms and at different levels — both molecular and behavioral. This could explain why, though systems of cells or groups of organisms could be organized in any number of possible ways, networks with similar properties continue to emerge.

“Is there anything special about the way nature has organized things in living systems?” Bialek wondered. He said much more work is necessary to claim criticality as a general biological principle. “But I do think we’re seeing in the data, somehow, signs of that specialness — things that it seems you can only get if the system has been set up in particular ways and not in others,” he said. “That I find very appealing.”

This work was supported in part by the National Science Foundation, the National Institutes of Health, the Howard Hughes Medical Institute, the W.M. Keck Foundation and the Swartz Foundation.

–By Molly Sharlach

Africa’s poison ‘apple’ provides common ground for elephants and livestock

Impala

The tall and bushy plant known as the Sodom apple has overrun vast swaths of East African savanna and pastureland, including parts of Kenya’s Amboseli National Park. New research suggests that certain animals, including elephants and impalas, could keep this invasive plant in check. (Photo courtesy of Rob Pringle)

AFRICAN WILDLIFE OFTEN RUN AFOUL of ranchers securing food and water resources for their animals, but the interests of fauna and farmer might finally be unified by the “Sodom apple,” a toxic invasive plant that has overrun vast swaths of East African savanna and pastureland.

Not a true apple, Solanum campylacanthum is a relative of the eggplant that smothers native grasses with its thorny stalks, while its striking yellow fruit provides a deadly temptation to sheep and cattle.

New research suggests, however, that certain wild animals, particularly elephants, could be a boon to human-raised livestock because of their voracious appetite for the Sodom apple. A fiveyear study led by Princeton University researchers found that elephants and impalas, among other wild animals, can not only safely gorge themselves on the plant, but also can efficiently regulate its otherwise explosive growth.

Just as the governments of nations such as Kenya prepare to pour millions into eradicating the plant, the findings present a method for controlling the Sodom apple that is cost-effective for humans and beneficial for the survival of African elephants, explained first author Robert Pringle, a Princeton assistant professor of ecology and evolutionary biology.

Elephants

An elephant prepares to uproot a Solanum campylacanthum plant in the upland savanna of central Kenya. Although this woody shrub is toxic to many mammal species, large browsers such as elephants can eat it, and in so doing help to reduce its abundance.

“The Holy Grail in ecology is these win-win situations where we can preserve wildlife in a way that is beneficial to human livelihoods,” Pringle said “Elephants have a reputation as destructive, but they may be playing a role in keeping pastures grassy.”

The findings are important given the threats to elephants from poaching, Pringle said. “We need to understand to what extent these threatened animals have unique ecological functions.”

Elephants and impalas can withstand S. campylacanthum’s poison because they belong to a class of herbivores known as “browsers” that subsist on woody plants and shrubs, many species of which pack a toxic punch, Pringle said. On the other hand, “grazers” such as cows, sheep and zebras primarily eat grass, which is rarely poisonous. These animals easily succumb to the Sodom apple, which causes emphysema, pneumonia, bleeding ulcers, brain swelling and death.

An unexpected feast Pringle was roughly three years into a study about the effects of elephants on plant diversity when he noticed that the Sodom apple was conspicuously absent from some experiment sites. He and other researchers had set up 36 exclosures — which are designed to keep animals out rather than in — totaling nearly 89 acres (36 hectares) at the Mpala Research Centre in Kenya, a multi-institutional research preserve with which Princeton has been long involved.

There were four types of exclosure: one type open to all animals; another where only elephants were excluded; one in which elephants and impalas were excluded; and another off limits to all animals.

It was in the sites that excluded elephants and impala that the Sodom apple particularly flourished, Pringle said, which defied everything he knew about the plant.

“I had always thought that these fruits were horrible and toxic, but when I saw them in the experiment, I knew some animal was otherwise eating them. I just didn’t know which one,” Pringle said. “The question became, ‘Who’s eating the apple?”

Using the exclosures, Pringle and his coauthors documented the zest with which wild African browsers will eat S. campylacanthum. Pringle worked with Corina Tarnita, a Princeton mathematical biologist and assistant professor of ecology and evolutionary biology, as well as with collaborators from the University of Wyoming, University of Florida, University of California-Davis, Mpala Center and University of British Columbia.

The researchers specifically observed the foraging activity of elephants, impalas, smalldog- sized antelopes known as dik-diks, and rodents. Using cameras, they captured about 30,000 hours of foraging, and discovered that elephants and impalas were the primary eaters of the plants.

There is a catch to the elephants’ and impalas’ appetite for the Sodom apple: When fruit goes in one end, seeds come out the other. Though some seeds are destroyed during digestion, most reemerge and are potentially able to germinate.

Pringle and Tarnita developed a mathematical model to conduct a sort of cost-benefit analysis of how the Sodom apple’s ability to proliferate is affected by being eaten. The model weighed the “cost” to the plant of being partially consumed against the potential benefit of having healthy seeds scattered across the countryside in an animal’s droppings.

While elephants ate an enormous amount of Solanum seeds, they also often destroyed the entire plant, ripping it out of the ground and stuffing the whole bush into their mouths. The model showed that to offset the damage an elephant wreaks on a plant, 80 percent of the seeds the animal eats would have to emerge from it unscathed. On top of that, each seed would have to be 10-times more likely to take root than one that simply fell to the ground from its parent.

Impalas, on the other hand, can have a positive overall effect on the plants, the researchers found. Impalas ate the majority of the fruit consumed — one impala ate 18 fruit in just a few minutes. But they do not severely damage the parent plant while feeding and also spread a lot of seeds in their dung. Of the seeds eaten by an impala, only 60 percent would need to survive, and those seeds would have to be a mere three-times more likely to sprout than a seed that simply fell from its parent.

“A model allows you to explore a space you’re not fully able to reach experimentally,” said Tarnita, who uses math to understand the outcome of interactions between organisms. “This model helped us conclude that although it is theoretically possible for elephants to benefit the plant, that outcome is extremely unlikely.”

The study was published in the June 22, 2014, edition of the Proceedings of the Royal Society B. The work was supported by the National Science Foundation, the National Sciences and Engineering Research Council of Canada, the Sherwood Family Foundation, and the National Geographic Committee for Research and Exploration.

–By Morgan Kelly

Collective behavior could help animals survive a changing environment

Princeton researchers found that collective intelligence is vital to certain animals’ ability to evaluate and respond to their environment. Conducted on golden shiners, the research demonstrated that social animals such as schooling fish rely heavily on grouping to effectively navigate their environment. (Image by Sean Fogarty)

Princeton researchers found that collective intelligence is vital to certain animals’ ability to evaluate and respond to their environment. Conducted on golden shiners, the research demonstrated that social animals such as schooling fish rely heavily on grouping to effectively navigate their environment. (Image by Sean Fogarty)

For social animals such as schooling fish, the loss of their numbers to human activity could eventually threaten entire populations, according to a finding that such animals rely heavily on grouping to effectively navigate their environment.

Princeton researchers have found that collective intelligence is vital to certain animals’ ability to evaluate and respond to their environment. Conducted on fish, the research demonstrated that small groups and individuals become disoriented in complex, changing environments. However, as group size is increased, the fish suddenly became highly responsive to their surroundings.

These results should prompt a close examination of how endangered group or herd animals are preserved and managed, said Iain Couzin, a professor of ecology and evolutionary biology. If wild animals depend on collective intelligence for migration, breeding and locating essential resources, they could be imperiled by any activity that diminishes or divides the group, such as overhunting and habitat loss, he explained.

“Processes that increase group fragmentation or reduce population density may initially appear to have little influence, yet a further reduction in group size may suddenly and dramatically impact the capacity of a species to respond effectively to their environment,” Couzin said. “If the mechanism we observed is found to be widespread, then we need to be aware of tipping points that could result in the sudden collapse of migratory species.”

The work is among the first to experimentally explain the extent to which collective intelligence improves awareness of complex environments, the researchers write. As it’s understood, a group of individuals gain an advantage by pooling imperfect estimates with those around them, which more or less “averages” single experiences into surprisingly accurate common knowledge.

With their work, Couzin and his co-authors uncovered an additional layer to understanding collective intelligence. The conventional view assumes that individual group members have some level of knowledge albeit incomplete. Yet the Princeton researchers found that in some cases individuals have no ability to estimate how a problem needs to be solved, while the group as a whole can find a solution through their social interactions. Moreover, they found that the more numerous the neighbors, the richer the individual — and thus group — knowledge is.

These findings correlate with recent research showing that collective intelligence — even in humans — can rely less on the intelligence of each group member than on the effectiveness of their communal interaction, Couzin said. In humans, research suggests that such cooperation would take the form of open and equal communication among individuals regardless of their respective smarts, he said.

The researchers placed fish known as golden shiners in experimental tanks in groups as low as one and as high as 256. The tanks featured a moving light field that was bright on the outer edges and tapered into a dark center. To reflect the changing nature of natural environments, they also incorporated small patches of darkness that moved around randomly. Prolific schoolers and enthusiasts of darkness, the golden shiners would pursue the shaded areas as the researchers recorded their movement using computer vision software. Although the fish sought the shade regardless of group size, their capability to do so increased dramatically once groups spanned a large enough area.

The researchers then tracked the motion of individual fish to gauge the role of social influence on their movement. They found that individuals adjusted their speed according to local light level by moving faster in more brightly lit areas, but without social influence the fish did not necessarily turn toward the darker regions. Groups, however, readily swam to dark areas and were able to track those preferred regions as they moved.

This collective sensing emerged due to the coherent nature of social interactions, the authors report. As one side of the group slowed and turned toward the shaded area, the other members did as well. Also, slowing down increased density and resulted in darker regions becoming more attractive to these social animals.

Couzin worked with lead authors Andrew Berdahl, a Princeton graduate student, and postdoctoral fellow Colin Torney, both in Couzin’s lab, as well as with former lab members Christos Ioannou and Jolyon Faria, who are now at the University of Bristol and the University of Oxford, respectively. The work was published in the Jan. 31, 2013, issue of Science, and was supported in part by grants from the National Science Foundation, the U.S. Office of Naval Research, the U.S. Army Research Office and the Natural Sciences and Engineering Research Council of Canada.

–By Morgan Kelly

Far from random, evolution follows a predictable pattern

Large milkweed bugs

Large milkweed bugs (above) feed on plants that produce a class of steroid-like cardiotoxins called cardenolides as a natural defense. The ability to eat these plants has evolved separately but in a predictable manner in several different orders of insects, including butterflies and moths (Lepidoptera); beetles and weevils (Coleoptera); and aphids, bed bugs, milkweed bugs and other sucking insects (Hemiptera). (Photo courtesy of Peter Andolfatto)

Evolution, often perceived as a series of random changes, might in fact be driven by a simple and repeated genetic solution to an environmental pressure, according to new research.

“Is evolution predictable? To a surprising extent the answer is yes,” according to Peter Andolfatto, an assistant professor in Princeton’s Department of Ecology and Evolutionary Biology and the Lewis-Sigler Institute for Integrative Genomics.

Andolfatto’s team has found that knowing how external conditions affect the proteins encoded by a species’ genes could allow researchers to determine a predictable evolutionary pattern driven by outside factors. Scientists could then pinpoint how the diversity of adaptations seen in the natural world developed even in distantly related animals.

The researchers carried out a survey of DNA sequences from 29 distantly related insect species, the largest sample of organisms yet examined for a single evolutionary trait. Fourteen of these species have evolved a nearly identical characteristic due to one external influence — they feed on plants that produce cardenolides, a class of steroid-like cardiotoxins that are a natural defense for plants such as milkweed and dogbane.

Though separated by 300 million years of evolution, these diverse insects — which include beetles, butterflies and aphids — experienced changes to a key protein called sodium-potassium adenosine triphosphatase, or the sodium-potassium pump, which regulates a cell’s crucial sodium-to-potassium ratio.

The protein in these insects eventually evolved a resistance to cardenolides, which usually cripple the protein’s ability to “pump” potassium into cells and excess sodium out.

To make this discovery, Andolfatto and his co-authors first sequenced and assembled all the expressed genes in the studied species. They used these sequences to predict how the sodium-potassium pump would be encoded in each of the species’ genes based on cardenolide exposure.

The researchers found that the genes of cardenolide-resistant insects incorporated various mutations that allowed them to resist the toxin. During the evolutionary timeframe examined, the sodium-potassium pump of insects feeding on dogbane and milkweed underwent 33 mutations at sites known to affect sensitivity to cardenolides. These mutations often involved similar or identical amino-acid changes that reduced susceptibility to the toxin. On the other hand, the sodium-potassium pump mutated just once in insects that do not feed on these plants.

Jianzhi Zhang, a University of Michigan professor of ecology and evolutionary biology, said that the Princeton-based study shows that certain traits have a limited number of molecular mechanisms, and that numerous, distinct species can share the few mechanisms there are. “The finding of parallel evolution in not two, but numerous herbivorous insects increases the significance of the study because such frequent parallelism is extremely unlikely to have happened simply by chance,” said Zhang, who is familiar with the study but had no role in it.

Andolfatto worked with lead author and Postdoctoral Research Associate Ying Zhen, and graduate students Matthew Aardema and Molly Schumer, all from Princeton’s ecology and evolutionary biology department, as well as Edgar Medina, a biological sciences graduate student at the University of the Andes in Colombia. The research was supported by grants from the Centre for Genetic Engineering and Biotechnology, the National Science Foundation and the National Institutes of Health and was published in the Sept. 28, 2012, issue of Science.
–By Morgan Kelly