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

Math and music spark student’s research interests

Alexander Iriza

Alexander Iriza. Photo by Denise Applewhite

WHILE PRINCETON SENIOR Alexander Iriza, of Astoria, New York, credits his parents for sparking his interest in math — his mother gave him math workbooks when he was a toddler — that was merely “a nudge” in the right direction.

For his senior thesis, required of all Princeton undergraduates, Iriza worked with Yannis Kevrekidis, the Pomeroy and Betty Perry Smith Professor in Engineering, to examine specific data analysis techniques.

“The idea is to start with a dynamical system of many particles that interact with each other on the microscopic level,” Iriza explained. “It’s believed that many animal species in the wild operate in this way, with each organism having its own personal preferences but also reacting to the individuals in its vicinity. Then we seek to understand the often beautiful and complex behavior that emerges at the macroscopic level of the entire flock.”

Iriza was also a violinist in the University orchestra. His exceptional scholarship led to his being named salutatorian for the Class of 2014, delivering a speech in Latin at Commencement. Comparing the maturity and depth of Iriza’s work to that of a strong graduate student, or even a postdoc or colleague, Kevrekidis said: “His intellectual strength, his work ethic, his joy in discovery and thinking, [and] his own vision about research directions single him out among the wonderful students I have had the good fortune to work with in my 28 years in Princeton. I truly look forward to finding out what he will accomplish in his research life.”

–By Jamie Saxon

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