American Society of Naturalists

A membership society whose goal is to advance and to diffuse knowledge of organic evolution and other broad biological principles so as to enhance the conceptual unification of the biological sciences.

“Ant collective behavior is heritable and shaped by selection”

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Justin T. Walsh, Simon Garnier, and Timothy A. Linksvayer (Nov 2020)

Researchers estimate the degree to which variation in collective behavior is heritable and has fitness consequences in ants

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Variation in ant collective behavior is heritable and affects the success of colonies

Collective behavior is ubiquitous in nature. Examples include flocks of birds, schools of fish, and nest building in social insects. A growing body of research finds that groups vary in their collective behavior; however, much less is known about how collective behavior evolves, including whether it is heritable or if it affects the success of groups. In a new paper published in the The American Naturalist, researchers at the University of Pennsylvania (Justin Walsh and Timothy Linksvayer) and the New Jersey Institute of Technology (Simon Garnier), demonstrate that behavioral variation between pharaoh ant colonies is heritable—that offspring colonies exhibit similar behavioral levels to their parental colonies—and that colony behavioral variation is linked to variation in colony success.

Walsh and coauthors design behavioral assays to measure foraging, aggression, and exploration of pharaoh ant colonies from a pedigreed laboratory population. In addition to collective behaviors, the authors also quantify the body size of colony members and numerous measures of colony productivity such as the production of new workers and queens. They use these colony productivity measures to show that variation in collective behavior is linked to the success of colonies, as colonies with higher foraging levels produce both more new workers and more new reproductives (queens and males). Overall, these results shed light on the genetic basis and evolution of collective behavior.


Abstract

Collective behaviors are widespread in nature and usually assumed to be strongly shaped by natural selection. However, the degree to which variation in collective behavior is heritable and has fitness consequences—the two prerequisites for evolution by natural selection—is largely unknown. We used a new pharaoh ant (Monomorium pharaonis) mapping population to estimate the heritability, genetic correlations, and fitness consequences of three collective behaviors (foraging, aggression, and exploration) as well as body size, sex ratio, and caste ratio. Heritability estimates for the collective behaviors were moderate, ranging from 0.17 to 0.32, but lower than our estimates for the heritability of caste ratio, sex ratio, and the body size of new workers, queens, and males. Moreover, variation among colonies in collective behaviors was phenotypically correlated, suggesting that selection may shape multiple colony collective behaviors simultaneously. Finally, we found evidence for directional selection that was similar in strength to estimates of selection in natural populations. Altogether, our study begins to elucidate the genetic architecture of collective behavior and is one of the first studies to demonstrate that it is shaped by selection.