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Evolving Migration COMMENTARY Evolving migration Stephen J. Simpson1 and Gregory A. Sword School of Biological Sciences, University of Sydney, Sydney, New South Wales 2006, Australia ass migrations of wildebeest, model by Guttal and Couzin (5), such caribou, song birds, sting a situation evolved spontaneously. M rays, and monarch butterflies Distinct groups of leaders and sociable are among the wonders of individuals arose under a wide range of the natural world (Fig. 1). At a very dif- scenarios in which population density and ferent scale, the coordinated migration of cost functions were varied. However, other cells within the body is central to embry- outcomes were possible under certain ological development, immune responses, conditions. At very low densities with low and wound healing. Although the scale, gradient-following costs, most individuals functions, and mechanisms may differ, were leaders, resulting in individuals mi- these examples share one key feature: grating independently rather than collec- they are the product of local interactions tively. Conversely, at extremely high among individual agents (wildebeest, but- population densities when gradient fol- terflies, or cells). The proximate mecha- Fig. 1. Caribou migration: a spectacular annual lowing costs were high, stationary aggre- nisms where collective behavior arises event in the Arctic. (Photograph courtesy of Ryan gations resulted. Nevertheless, collective K. Brook.) from local interactions between indi- migration in which a majority of sociable viduals have become a fertile area of re- followers exploited the gradient-following search, founded on models from statis- the gradient (high gradient detection and abilities of a minority of leaders was ob- tical physics in which interacting agents intermediate sociability). served over the vast majority of the pa- are modeled as self-propelled particles As grist for evolution in the model, cost rameter space explored. (1–4). Guttal and Couzin (5) take such functions were specified for each of these The process by which the two stable analyses to the next level and ask how and variable traits: the greater the gradient strategies arise and coexist reveals the under what ecological circumstances might detection ability and level of sociability, central role of information structure and collective migration have evolved. the higher the cost to the individual. Costs collective dynamics in affecting the fitness Collective migration is a group level of detecting and following a gradient payoffs to individual group members. phenomenon, but its underlying mecha- might include reduced vigilance to preda- Under most conditions, all individuals in nisms are at the level of individuals. What, tors and the energetic costs of maintaining a population that initially lacks both gra- then, are the individual level traits that gradient detection mechanisms, whereas dient detection and sociability rapidly might be subject to selection, and how the costs of sociability could include in- evolve the ability to detect a gradient be- might the collective level phenomena creased competition for food, disease cause of the associated fitness benefits of arising from these traits feed back to affect transmission, or greater visibility to pred- migration. At the same time, individuals fi the tness of the individuals involved? ators (6). On the positive side of the evo- who also acquire a mutation to become fi Guttal and Couzin (5) model a situation lutionary ledger, fitness benefits were sociable gain an additional tness advan- where two traits are subject to selection. tage because of the increased migratory fi gained according to how far and precisely The rst is the capacity of an organism to organisms migrated in the direction of accuracy accrued through the many respond to a gradient or some other ex- the gradient. wrongs principle of group navigation (8). ternal cue, indicating the correct direction Having set their agents free to evolve, Thus, individuals with both strong gradient of migration. Real examples of cues used Guttal and Couzin (5) find that popu- detection and sociability parameters ini- by migrating organisms include magnetic lations typically evolved two coexisting tially come to dominate the population. It fields, sunlight, wind direction, tempera- and equally fit individual strategies: a mi- is at this point that the information pro- ture, and chemical gradients. The second nority of individuals evolved to become vided within the group facilitates some evolvable trait in the model is the socia- leaders, and the rest were highly sociable surprising evolutionary dynamics. Indi- bility of an organism: specifically, its ten- viduals can achieve higher relative fitness followers. Leaders assiduously followed the dency to be attracted to and align with by relaxing their gradient detection ability environmental gradient and largely ignored moving neighbors. Examples include the while obtaining the benefits of migration other individuals, whereas sociable in- visually guided responses of starlings through increased social attraction to dividuals were attracted by one another but and locusts or physical adhesion and gradient-detecting group members or their chemical signaling among bacteria. Vari- had little or no ability to detect the gradi- followers. As a result, an overall decrease ous combinations of traits values in the ent. As a consequence, the entire group in gradient detection ability is observed, model could result in a spectrum of pop- tracked the gradient together, with leaders whereas the strength of sociability in- ulation level outcomes, including indi- showing the way and sociable individuals creases. The stage is now set for a split in viduals moving randomly (low gradient tagging along and freeloaded on the gra- strategies. Some individuals achieve higher detection and low sociability), migrat- dient-following ability of the leaders. relative fitness by further reducing the ing independently of one another (high Couzin et al. (1) had previously shown costs of gradient detection and increasing gradient detection and low sociability), in an agent-based simulation how a small forming aggregations but not migrating number of informed individuals can direct (low gradient detection and high sociabil- a large group of naive individuals to a re- Author contributions: S.J.S. and G.A.S. wrote the paper. ity), migrating together along the gradient source site, as seen, for example, in the The authors declare no conflict of interest. (high gradient detection and high socia- way that a small number of informed scout See companion article 10.1073/pnas.1006874107. fi bility), or forming lamentous groups that honey bees directs a large swarm of igno- 1To whom correspondence should be addressed. E-mail: split and fuse again as they move along rant insects to a new nest site (7). In the [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1011693107 PNAS Early Edition | 1of2 Downloaded by guest on September 26, 2021 their sociability, thereby exclusively be- hibit collective migration? One intriguing movement decisions, the scale at which coming followers. In other individuals, possibility is that individuals that fail to such stimuli can be detected, and the fre- mutations that increase gradient detec- migrate in an otherwise collectively mi- quency at which conspecifics encounter tion ability but reduce sociability become grating population are simply sociable each other during migration. favored; they evolve as leaders that gain individuals who failed to get the message It is well known that populations may a fitness advantage through increased in- and did not experience sufficient stimuli- lose or gain migratory behavior (9). dividual migratory benefits and relaxed from leaders whom they otherwise would A clever aspect of the model by Guttal costs of sociality. The net result is a have followed. Alternatively, there are, of and Couzin (5) is that they used the shape frequency-dependent balance of the two of migration benefit function as a surro- alternative strategies with equal fitness in gate for increasing habitat fragmentation the population. The population exhibits Collective migration can to examine the potential impact of collective migration but is actually com- arise even in very anthropogenic changes on migratory pat- prised of two sets of individuals following terns. Using a simple nonlinear function, very different rules. sparse populations, they could adjust how far individuals Many behavioral strategies are condi- needed to migrate before enjoying in- tional: the animal exhibits one strategy when individuals rarely creased benefits. As habitat fragmentation under some circumstances and another along the migratory route increases, for strategy in a different set of conditions. interact. example, through loss of stop-over sites, Variation among individuals in migratory migration is gradually lost because of the strategies is well known in nature (9). To higher costs of reaching more distant model a scenario in which individuals with course, many other ways in which an destinations. However, restoring the habi- a high gradient detection ability might ei- organism’s state, developmental stage, and tat does not simply restore migration. ther avoid exploitation by sociable indi- environment could mediate its expression This is because minor mutations that only viduals or exploit the gradient detection of migratory behavior. Extensions of in- slightly improve gradient detection do not ability of others, they were allowed to turn dividually
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