PNAS: Leadership, collective behavior, and the evolution of migration

Posted by on Nov 1 2010 in Headlines3 comments

Migration is a remarkable and widespread form of collective motion that is observed over a broad range of spatial and temporal scales. Often migratory individuals face the challenge of tracking long range, noisy environmental cues in order to reach suitable habitats. Detecting directional information, however, may come at a cost. This raises a number of questions: How do individuals balance the cost and benefits of migration? What is the role of social interaction? How robust is an evolved migratory strategy to anthropogenic pressures occurring on ecological timescales? And more generally, what are the principles that underlie the evolution of collective migration? To address these issues, we have developed a computational and analytic framework that integrates individual-based models of collective motion with a mathematical description of evolution based on game theory and adaptive dynamics.

In our approach, we assume two evolvable traits; a `leadership’ or `gradient detection ability’ which enables individuals to sense their environment, and a `sociality trait` which represents a tendency to follow the direction of nearby individuals. Depending on the combination of these traits, populations may exhibit random walks, solitary migration or collective migration, either with or without fission fusion among groups. If these traits come at no cost, the population evolves to a homogeneous state in which all individuals have high leadership and moderate sociality that leads to collective migration with compact groups. However, including costs for environmental sensing dramatically changes the evolutionary outcome.

For a broad range of costs and population densities, we predict that individuals who invest in acquiring information from environmental cues (leaders) are readily exploited by others who adopt a socially facilitated movement behavior (social individuals). Both types of individuals acquire equivalent fitness, thus leading to a bimodal evolutionary stable state. Evolved populations organize into groups of different sizes that merge and split as they migrate. Leaders typically occupy the front of the group through a self-sorting process while social individuals follow nearby individuals without any signaling from, or ability to recognize, leaders. The principle of leadership demonstrated by Couzin et al. (2005), i.e. that the proportion of leaders needed to guide migratory groups with a desired accuracy reduces with group size, emerges spontaneously in the evolved population.

In a further work this individual-based approach was reduced to an analytically tractable abstract model by using a mean-field approximation of social interactions based on the theory of nonlinear coupled oscillators. By making this approximation the infinite dimensional system of interacting individuals was reduced to two key parameters, meaning the evolutionary dynamics could then be studied using the adaptive dynamics framework. Through this work exact conditions for the evolution of specialized subpopulations of leaders and followers were obtained.

Using our framework we have also studied the potential response of evolutionary strategies to environmental changes on short ecological timescales. Our work predicts a gradual decline of migration due to increasing habitat destruction and we argue that much greater restoration is required to recover lost behaviors (i.e., a strong hysteresis effect).

Photo credits: Prof. Ryan K. Brook, University of Saskatchewan.

Videos demonstrating the phenomenon:

http://icouzin.princeton.edu/wp-content/uploads/2010/09/simul.mov

http://icouzin.princeton.edu/wp-content/uploads/2010/09/simulZoom.mov

Coverage press for this work: 

Relevant references:

Shaw, A.K. & Couzin, I.D. (2012) Migration or residency? The evolution of movement behavior and information usage in seasonal environments. Submitted.

Guttal, V., Romanczuk, P., Simpson, S.J. & Couzin, I.D. (2012) Cannibalism as a driver of the evolution of behavioral phase polyphenism in locusts. Submitted.

Couzin, I.D., Ioannou, C.C., Demirel, G., Gross, T., Torney, C.J., Hartnett, A., Conradt, L., Levin, S.A. & Leonard, N.E. (2011) Uninformed individuals promote democratic consensus in animal groupsScience 332(6062), 1578-1580.

Frewen, T. A., Couzin, I. D., Kolpas, A., Moehlis, J., Coifman, R. & Kevrekidis, I. O. (2011) Coarse collective dynamics of animal groupsLecture Notes in Computational Science and Engineering 75, 299-309.

Torney, C., Berdahl, A. and Couzin, I.D. (2011) Signaling and the evolution of cooperative foraging in dynamic environmentsPLoS Computational Biology 7(9), e1002194.

Guttal, V., & Couzin, I. D. (2011) Leadership, collective motion and the evolution of migratory strategiesCommunicative and Integrative Biology, 4, 294-298. Open Access.

Guttal, V. & Couzin, I. D. (2010) Social interactions, information use and the evolution of collective migrationPNAS 107(37), 16172-16177.

     > ‘From the Cover’, ‘This Week in PNAS’ and PNAS Commentary by Simpson and Sword “Evolving Migration” 107(39), 16753-16754.

Torney, C., Levin, S. A. & Couzin, I. D. (2010) Specialization and evolutionary branching within migratory populationsPNAS 107(47), 20394-20399.

     >  Recommended by ‘Faculty of 1000’

Torney, C., Neufeld, Z. & Couzin, I.D. (2009) Context-dependent interaction leads to emergent search behavior in social aggregatesPNAS 106(52), 22055-22060.

Conradt, L., Roper, T.J., Couzin, I.D. & Krause, J. (2009) “Leading according to need” in self-organizing groups. The American Naturalist 173(3), 304-312.
Deisboeck, T. & Couzin, I.D. (2009) Collective behavior in cancer cell populationsBioEssays 31(2), 190-197. 
Couzin, I.D. (2007) Collective mindsNature 455, 715.

Nabet, B., Leonard, N.E., Couzin, I.D. & Levin, S.A.(2006) Leadership in animal group motion: a bifurcation analysisProceedings of the 17th Symposium on Mathematical Theory of Networks and Systems, 1-14

Couzin, I.D., Krause, J., Franks, N.R. & Levin, S.A. (2005) Effective leadership and decision making in animal groups on the moveNature 433, 513-516.



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  1. This is a wonderful field of group dynamics and interaction. My fascination has been in extrapolating the model to biological entities like Immunoglobulin molecules and their environment (read antigen) sensitivity while in circulation and ex-vivo. the therapeutic differences between Intravenous Immunoglobulin and purified monoclonal antibodies has more than a dose response difference . the self sensitivity (social group) and antigenic specificity (environmental cost) of the different Ig groups is an unexplored and fascinating avenue of medical (group) investigative thought 

  2. […] professor Ian Couzin, do Departamento de Ecologia e Biologia Evolutiva, Princeton University EUA, perguntou para si […]

  3.  
    So-called environmentally induced migration is multi-level problem. According to Essam El-Hinnawi definition form 1985 environmental refugees as those people who have been forced to leave their traditional habitat, temporarily or permanently, because of a marked environmental disruption (natural or triggered by people) that jeopardised their existence and/or seriously affected the quality of their life. The fundamental distinction between `environmental migrants` and `environmental refugees` is a standpoint of contemporsry studies in EDPs.
    According to Bogumil Terminski it seems reasonable to distinguish the general category of environmental migrants from the more specific (subordinate to it) category of environmental refugees.
    Environmental migrants, therefore, are persons making a short-lived, cyclical, or longerterm change of residence, of a voluntary or forced character, due to specific environmental factors. Environmental refugees form a specific type of environmental migrant.
    Environmental refugees, therefore, are persons compelled to spontaneous, short-lived, cyclical, or longer-term changes of residence due to sudden or gradually worsening changes in environmental factors important to their living, which may be of either a short-term or an irreversible character.

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