The effective collective: Grouping could ensure animals find their way in a changing environment (Science)

Image of golden shiner fish
Golden shiners were used to study collective behavior (Image courtesy of Sean Fogarty)

By Morgan Kelly, Office of Communications

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 University researchers report in the journal Science 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 senior researcher Iain Couzin, a Princeton 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. Collective intelligence is an established advantage of groups, including humans. 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. For instance, the paper in Science cites a 1907 study that predicted with near precision the weight of an ox based on the estimates of 787 people.

With their work, Couzin and his coauthors 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 currently 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.

Read the abstract.

Citation: Berdahl, Andrew, Colin J. Torney, Christos C. Ioannou, Jolyon J. Faria, and Iain D. Couzin. 2013. Emergent sensing of complex environments by mobile animal groups. Science. Article first published online: Jan. 31, 2013. DOI: 10.1126/science.1225883

This work 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.

Researchers harness nature to produce the fuel of the future (PNAS)

By Catherine Zandonella, Office of the Dean for Research

Hydrogen has tremendous potential as an eco-friendly fuel, but it is expensive to produce. Now researchers at Princeton University and Rutgers University have moved a step closer to harnessing nature to produce hydrogen for us.

The team, led by Princeton chemistry professor Annabella Selloni, takes inspiration from bacteria that make hydrogen from water using enzymes called di-iron hydrogenases. Selloni’s team uses computer models to figure out how to incorporate the magic of these enzymes into the design of practical synthetic catalysts that humans can use to produce hydrogen from water.

In this latest paper, Selloni and co-authors present a solution to an issue that has dogged the field: the catalysts designed so far are susceptible to poisoning by the oxygen present during the reaction. By making changes to the catalyst to improve the stability of the structure in water, the researchers found that they had also created a catalyst that is tolerant to oxygen without sacrificing efficiency. What is more, their artificial catalyst could be made from abundant and cheap components, such as iron, indicating that the catalyst could be a cost-effective way of producing hydrogen.

Selloni and her team conducted their research in silico — that is, using computer modeling. The goal is to learn enough about how these catalysts work to someday create working catalysts that can make vast quantities of inexpensive hydrogen for use in vehicles and electricity production.

The team included Patrick Hoi-Land Sit, an associate research scholar in chemistry at Princeton; Roberto Car, Princeton’s Ralph W. *31 Dornte Professor in Chemistry, and Morrel H. Cohen, a Senior Chemist at Princeton and Member of the Graduate Faculty of Rutgers University. Selloni is Princeton’s David B. Jones Professor of Chemistry.

Read the abstract.

Citation: Sit, Patrick H.-L., Roberto Car, Morrel H. Cohen, and Annabella Selloni. Oxygen tolerance of an in silico-designed bioinspired hydrogen-evolving catalyst in water. PNAS 2013; published ahead of print January 22, 2013, doi:10.1073/pnas.1215149110

This work was supported by the Department of Energy, Office of Basic Energy Sciences, Division of Materials Sciences and Engineering under Award DE-FG02-06ER-46344. We also used resources of the National Energy Research Scientific Computing Center, which is supported by the Office of Science of the US Department of Energy under Contract DE-AC02-05CH11231. The team also used computational resources from the Princeton Institute for Computational Science and Engineering (PICSciE) and the Office of Information Technology (OIT) High Performance Computing Center and Visualization Laboratory at Princeton University.

Spring may come earlier to North American forests (Geophysical Research Letters)

By Catherine Zandonella, Office of the Dean for Research

Trees in the continental U.S. could send out new spring leaves up to 17 days earlier in the coming century than they did before global temperatures started to rise, according to a new study by Princeton University researchers. These climate-driven changes could lead to changes in the composition of northeastern forests and give a boost to their ability to take up carbon dioxide.

Trees play an important role in taking up carbon dioxide from the atmosphere, so researchers led by David Medvigy, assistant professor in Princeton’s department of geosciences, wanted to evaluate predictions of spring budburst — when deciduous trees push out new growth after months of winter dormancy — from models that predict how carbon emissions will impact global temperatures.

The date of budburst affects how much carbon dioxide is taken up each year, yet most climate models have used overly simplistic schemes for representing spring budburst, modeling for example a single species of tree to represent all the trees in a geographic region.

In 2012, the Princeton team published a new model that relied on warming temperatures and the waning number of cold days to predict spring budburst. The model, which was published in the Journal of Geophysical Research, proved accurate when compared to data on actual budburst in the northeastern United States.

In the current paper published online in Geophysical Research Letters, Medvigy and his colleagues tested the model against a broader set of observations collected by the USA National Phenology Network, a nation-wide tree ecology monitoring network consisting of federal agencies, educational institutions and citizen scientists. The team incorporated the 2012 model into predictions of future budburst based on four possible climate scenarios used in planning exercises by the Intergovernmental Panel on Climate Change.

The researchers included Su-Jong Jeong, a postdoctoral research associate in Geosciences, along with Elena Shevliakova, a senior climate modeler, and Sergey Malyshev, a professional specialist, both in the Department of Ecology and Evolutionary Biology and associated with the U.S. National Oceanic and Atmospheric Administration’s Geophysical Fluid Dynamics Laboratory.

The team estimated that, compared to the late 20th century, red maple budburst will occur 8 to 40 days earlier, depending on the part of the country, by the year 2100. They found that the northern parts of the United States will have more pronounced changes than the southern parts, with the largest changes occurring in Maine, New York, Michigan, and Wisconsin.

The researchers also evaluated how warming temperatures could affect the budburst date of different species of tree. They found that budburst shifted to earlier in the year in both early-budding trees such as common aspen (Populus tremuloides) and late-budding trees such as red maple (Acer rubrum), but that the effect was greater in the late-budding trees and that over time the differences in budding dates narrowed.

The researchers noted that early budburst may give deciduous trees, such as oaks and maples, a competitive advantage over evergreen trees such as pines and hemlocks. With deciduous trees growing for longer periods of the year, they may begin to outstrip growth of evergreens, leading to lasting changes in forest make-up.

The researchers further predicted that warming will trigger a speed-up of the spring “greenwave,” or budburst that moves from south to north across the continent during the spring.

The finding is also interesting from the standpoint of future changes in springtime weather, said Medvigy, because budburst causes an abrupt change in how quickly energy, water and pollutants are exchanged between the land and the atmosphere. Once the leaves come out, energy from the sun is increasingly used to evaporate water from the leaves rather than to heat up the surface. This can lead to changes in daily temperature ranges, surface humidity, streamflow, and even nutrient loss from ecosystems, according to Medvigy.

Read the abstract.


Jeong, Su-Jong, David Medvigy, Elena Shevliakova, and Sergey Malyshev. 2013. Predicting changes in temperate forest budburst using continental-scale observations and models. Geophysical Research Letters. Article first published online: Jan. 25, 2013. DOI: 10.1029/2012GL054431

This research was supported by award NA08OAR4320752 from the National Oceanic and Atmospheric Administration, U.S. Department of Commerce.

Herpes viruses commandeer protein production to storm neurons (Cell Host and Microbe)

By Morgan Kelly, Office of Communications

Viruses in the herpes family most commonly found in humans infect nervous system cells by “turning on” and then seizing control of the internal system these cells rely on to sense injury, among other signaling functions.

Princeton University researchers report in the journal Cell Host and Microbe that the pseudorabies virus (PRV) — a model herpes virus that infects animals — initiates and commandeers protein production in axons, the long offshoots of the cell body that connect neurons to other neurons and to tissue. After entering the neuron at the axon, the virus particles — which deliver the viral DNA that infects host cells — use the newly made proteins to travel to and infect the cell nucleus. Once there, the infection can spread to other neurons.

The research is the latest from the laboratory of senior researcher Lynn Enquist, the Henry L. Hillman Professor in Molecular Biology, to unravel the puzzling efficiency with which PRV and related herpes viruses invade the nervous system. PRV is an alpha-herpes virus, a prolific herpes subfamily that includes herpes simplex virus 1 (HSV-1), an extremely common human virus that causes cold sores and other lesions.

In the current paper, the researchers write that PRV “cleverly exploited” a natural cell process to speed up infection, a theme that resonates in past work from the Enquist lab on alpha-herpes viruses. In 2012, another researcher in the lab reported in Cell Host and Microbe that PRV and HSV-1 infections affect movement of neuronal mitochondria, the mobile organelles that regulate a cell’s energy supply, communication, and self-destruction response to infection.

For this newest research, Enquist worked with lead author Orkide Koyuncu, a postdoctoral research associate in molecular biology, and David Perlman, head of the molecular biology department’s mass spectrometry facility. They suggest that PRV particles first replicate in non-neuronal (such as skin and other tissue) cells at the site of body entry. The particles then enter axon terminals as the axon carries out its regular status-reports with those cells. The process of viral-particle entry is sensed by the neuron as a damage signal, which begins the protein production that will carry the virus particles to the nucleus.

Interestingly, the researchers discovered that the movement of incoming virus particles was disrupted by a genuine damage signal initiated before PRV infection. They hypothesized that the immediate response spurred by injury, infection or inflammation slows down other processes within the axon, which the researchers call “competitive inhibition.” When the molecular details of this crosstalk are fully understood, these signals could be used clinically to prevent the spread of alpha-herpes viruses.

Read the paper.

Citation: Koyuncu, Orkide O., David H. Perlman, Lynn W. Enquist. 2013. Efficient Retrograde Transport of Pseudorabies Virus within Neurons Requires Local Protein Synthesis in Axons. Cell Host & Microbe Vol. 13, no. 1, pp. 54-66.

This work was supported by U.S. National Institutes of Health grant R01NS033506-18.

From dark hearts comes the kindness of mankind (Evolution)

By Morgan Kelly, Office of Communications

The kindness of mankind most likely developed from our more sinister and self-serving tendencies, according to Princeton University and University of Arizona research that suggests society’s rules against selfishness are rooted in the very exploitation they condemn.

The report in the journal Evolution proposes that altruism — society’s protection of resources and the collective good by punishing “cheaters” — did not develop as a reaction to avarice. Instead, communal disavowal of greed originated when competing selfish individuals sought to control and cancel out one another. Over time, the direct efforts of the dominant fat cats to contain a few competitors evolved into a community-wide desire to guard its own well-being.

The study authors propose that a system of greed dominating greed was simply easier for our human ancestors to manage. In this way, the work challenges dominant theories that selfish and altruistic social arrangements formed independently — instead the two structures stand as evolutionary phases of group interaction, the researchers write.

Second author Andrew Gallup, a former Princeton postdoctoral researcher in ecology and evolutionary biology now a visiting assistant professor of psychology at Bard College, worked with first author Omar Eldakar, a former Arizona postdoctoral fellow now a visiting assistant professor of biology at Oberlin College, and William Driscoll, an ecology and evolutionary biology doctoral student at Arizona.

To test their hypothesis, the researchers constructed a simulation model that gauged how a community withstands a system built on altruistic punishment, or selfish-on-selfish punishment. The authors found that altruism demands a lot of initial expenditure for the group — in terms of communal time, resources and risk of reprisal from the punished — as well as advanced levels of cognition and cooperation.

On the other hand, a construct in which a few profligate players keep like-minded individuals in check involves only those members of the community — everyone else can passively enjoy the benefits of fewer people taking more than their share. At the same time, the reigning individuals enjoy uncontested spoils and, in some cases, reverence.

Social orders maintained by those who bend the rules play out in nature and human history, the authors note: Tree wasps that police hives to make sure that no member other than the queen lays eggs will often lay illicit eggs themselves. Cancer cells will prevent other tumors from forming. Medieval knights would pillage the same civilians they readily defended from invaders, while neighborhoods ruled by the Italian Mafia traditionally had the lowest levels of crime.

What comes from these arrangements, the researchers conclude, is a sense of order and equality that the group eventually takes upon itself to enforce, thus giving rise to altruism.

Read the abstract.

Eldakar, O. T., Gallup, A. C. and Driscoll, W. W. (2013), When Hawks Give Rise To Doves: The Evolution and Transition of Enforcement Strategies. Evolution. doi: 10.1111/evo.12031

This work was supported by the National Institutes of Health.

Cancer cells exchange leaders during invasion (PNAS)

By Catherine Zandonella, Office of the Dean for Research

A new study has found that cancer cells appear to exchange leading roles as they migrate out of a tumor in the early stages of invasion, or metastasis, of other sites in the body. Metastatic cancer accounts for more than 90% of cancer-related deaths.

A team led by Robert Austin, professor of physics at Princeton University, found that individual cancer cells take turns as trailblazers when they carve their way through the dense wall — known as the extracellular matrix — that stands between a tumor and the blood vessels which can carry the cells to other parts of the body.

The researchers also found that the cells leave the tumor in search of food, since cells that had plenty of available nutrients did not migrate. The finding reinforces the hypothesis that metastasis occurs when tumors become so densely packed that blood vessels cannot penetrate the interior and cancer cells must migrate to survive.

The researchers included first author Liyu Liu of the Chinese Academy of Sciences; Guillaume Duclos of the National Center for Scientific Research in Paris; Bo Sun, Jeongseog Lee, Amy Wu, Howard Stone and James Sturm of Princeton University; Yoonseok Kam and Robert Gatenby of H. Lee Moffitt Cancer Center in Tampa; and Eduardo Sontag of Rutgers University. The article appeared in the Proceedings of the National Academy of Sciences.

To study cancer cell behavior, the researchers constructed a small chamber with three compartments arranged like floors in an apartment building. On the bottom floor was a well of glucose, the preferred food for metastatic cells. The middle floor contained a dense layer of collagen, a protein that makes up the extracellular matrix that surrounds tumors. On the top floor they placed metastatic cancer cells, which were labeled with fluorescent dye for visibility. They trained a microscope and camera on the chamber.

Through the microscope, the researchers filmed the cancer cells as they moved down through the chamber toward the glucose. The researchers found that a single cell would become the leader for some time, then drop back as another cell took the lead in what the authors term a “collective invasion strategy.” They also found that the collagen was pushed aside, leaving a wake in which cells behind the leader could travel.

Because the collagen is very dense, the cells must expend a lot of energy to reach the glucose, and indeed the researchers found that cells without a need for glucose did not bother to burrow down into the collagen. The researchers used collagen with a density similar to that of human breast tissue.

The study adds to the growing understanding of metastasis and could serve to assist researchers in developing strategies for its prevention.

Liyu Liu, Guillaume Duclos, Bo Sun, Jeongseog Lee, Amy Wu, Yoonseok Kam, Eduardo D. Sontag, Howard A. Stone, James C. Sturm, Robert A. Gatenby, and Robert H. Austin. Minimization of thermodynamic costs in cancer cell invasion. PNAS January 14, 2013 201221147.

Read the paper (open access).

This work was supported by the National Science Foundation and the National Cancer Institute.

Racial diversity and judicial influence (American Journal of Political Science)

By Michael Hotchkiss, Office of Communications

Adding a black judge to an appellate panel with two nonblack judges nearly ensures the panel will vote in favor of an affirmative action program, according to research by Jonathan Kastellec, an assistant professor of politics at Princeton, who has evaluated the consequences of judicial diversity on the U.S. Court of Appeals.

While Kastellec’s research also shows that black judges are significantly more likely to support affirmative action programs, the small percentage of racial minorities on the federal bench means the key question is whether their presence on appellate courts influences their colleagues and affects case outcomes.

The results have important implications for assessing the relationship between diversity and representation on federal courts.

Kastellec, J. P. (2013), Racial Diversity and Judicial Influence on Appellate Courts. American Journal of Political Science, 57: 167–183. doi: 10.1111/j.1540-5907.2012.00618.x

Read the article

Downplaying positive impressions: Warmth versus competence (Journal of Experimental Social Psychology)

By Michael Hotchkiss, Office of Communications

When people want to appear warm, they tend to agree, compliment, perform favors and encourage others to talk. When they want to appear competent, they emphasize their accomplishments, exude confidence and control the conversation. But people trying to manage how others see them also take advantage of a negative relationship between warmth and competence, according to Princeton University researchers Deborah Son Holoien, a graduate student in psychology, and Susan Fiske, the Eugene Higgins Professor of Psychology. Four studies detailed in this article found that people will act less competent to appear warm and act less warm to appear competent.

Holoien, Deborah Son and Susan Fiske. 2013 Downplaying positive impressions: Compensation between warmth and competence in impression management. Journal of Experimental Social Psychology 49: 33–41.

Read the abstract

This work was supported by a National Science Foundation Graduate Research Fellowship.

Nursing gerbils unravel benefit of multiple mothers in collective mammals (Mammalian Biology)

By Morgan Kelly, Office of Communications

In mammals such as rodents that raise their young as a group, infants will nurse from their mother as well as other females, a dynamic known as allosuckling. Ecologists have long hypothesized that allosuckling lets newborns stockpile antibodies to various diseases, but the experimental proof has been lacking until now.

An in-press report in the journal Mammalian Biology found that infant Mongolian gerbils that suckled from females given separate vaccines for two different diseases wound up with antibodies for both illnesses.

The findings not only demonstrate the potential purpose of allosuckling, but also provide the first framework for further studying it in the wild by using traceable antibodies, said first author Romain Garnier, a postdoctoral researcher in Princeton University’s Department of Ecology and Evolutionary Biology. Garnier conducted the research with Sylvain Gandon and Thierry Boulinier of the Center for Functional and Evolutionary Ecology in France, and with Yannick Chaval and Nathalie Charbonnel at the Center for Biology and Management of Populations in France.

Garnier and his coauthors administered an influenza vaccine to one group of female gerbils, and a vaccine for Borrelia burgdorferi — the bacterial agent of Lyme disease — to another group. Once impregnated, female gerbils from each vaccine group were paired and, as the gerbils do in nature, kept separate from the male gerbils to birth and rear their young. In the wild, females can choose which young to nurse and infant gerbils can likewise choose which female to suckle. In the typical lab, however, one male, one female and their young are housed together, the researchers wrote.

When screened upon birth, all the infant gerbils had no detectable antibodies against influenza while one had antibodies against B. burgdorferi, according to the paper. But after eight days of nursing, all the infants contained high levels of antibodies for both influenza and B. burgdorferi, suggesting that the females nursed the young — their own and those of the other female — evenly. These results suggest that allosuckling is indeed intended to expose newborn animals to a host of antibodies.

This benefit sheds light on a peculiar arrangement in cooperative mammals that ecologists have puzzled over, the authors wrote. In social species, females usually fall into dominant or subordinate groups with the subordinate females typically involved in tending to the young produced by dominant females. Yet, in many cases, subordinate females are “allowed” to breed. Garnier and his colleagues suggest that the potentially larger antibody pool available through nursing might be one of the reasons why.

Cita­tion: Garnier, R., et al., Evidence of cross-transfer of maternal antibodies through allosuckling in a mammal: Potential importance for behavioral ecology. Mammal. Biol. (2012).

Read the abstract.

Gypsy moth caterpillar takes bite out of forest carbon storage (Environmental Research Letters)

Forests are important carbon dioxide storage mechanisms, but a voracious leaf-eating caterpillar is cutting into the trees’ capacity to remove the greenhouse gas from the atmosphere, according to new research by scientists at Princeton University, Rutgers University and the United States Forest Service.

The gypsy moth caterpillar, widespread in the northeastern United States, can wreak devastation on forests as it devours the leaves of oak, pine, and other tree species. The new research found that this defoliation has a significant detrimental effect on the ecosystem’s capacity to act as a carbon sink.

The study found that an oak-pine forest in the New Jersey pinelands hit by the gypsy moth every five years would store about one-third less of the above-ground carbon as an unharmed similar forest, according to David Medvigy, assistant professor of geosciences at Princeton University.

The research was conducted by Medvigy and Karina Schäfer, assistant professor of ecosystem ecology at Rutgers University as well as researchers from the US Forest Service: Kenneth Clark of the Silas Little Experimental Forest in New Jersey and Nicholas Skowronski of the Northern Research Station in West Virginia.

The research was published in the journal Environmental Research Letters. (Read the open access article.) A news article about the study can be found here.

Citation: Medvigy, D., K. L. Clark, N. S. Skowronskiand and K. V. R. Schäfer. 2012. Simulated impacts of insect defoliation on forest carbon dynamics. Environ. Res. Lett. 7 045703