NSF-BSF: Natural selection on the social interactions that mediate collective behavior: ecological pressures and genomic architecture

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The project investigates how evolution shapes resilience to changing conditions. Ant colonies operate without central control. Ants use brief local interactions that in the aggregate, allow colonies to adjust to changing conditions. The project will continue a unique long-term study tracking a population of harvester ant colonies in the desert of the southwest US over 30 years, including periods of heavy rainfall and a long drought that now appears to be ending. Colonies regulate foraging activity in response to changes in food availability and water stress. Colonies differ in how they regulate foraging; some are more likely than others to restrict foraging activity in dry weather so as to conserve water. The project will use genetic methods to find genetic differences among colonies that differ in behavior, to learn whether the regulation of foraging behavior is inherited from parent to offspring colonies, and to examine how colony behavior is associated with its reproductive success in numbers of offspring colonies. This work will show how natural selection is shaping the collective behavior of colonies, and how selection can shift in response to changing drought conditions.Collective behavior occurs at every level of biological organization, from cells to animals. It operates without central control, using local interactions that in the aggregate produce a collective outcome. Natural selection on collective behavior, as on any trait, acts in relation to ecological pressures. The project investigates the evolution of collective behavior in a natural population, linking the individual and collective levels, how selection pressure on collective behavior shifts in changing ecological conditions. The project draws on and continues a 30-year study of the demography, behavior, ecology and evolution of a population of colonies of the red harvester ant (Pogonomyrmex barbatus) in the desert of southwestern US, and develops a database that makes these data available for analysis. Previous work shows that desert harvester ant colonies regulate foraging activity to manage water stress, using brief olfactory interactions between outgoing and returning foragers inside the nest. Colonies vary in how they regulate foraging activity, and previous work conducted in drought conditions, shows this is associated with colony reproductive success in offspring colonies. The project examines how changing ecological conditions, especially rainfall, lead to shifts in the selection pressures that link foraging activity and reproductive success. Reduced representation genomic sequencing will be used to identify parent-offspring pairs of colonies, and thus measure reproductive success in number of offspring colonies. The heritability from parent to offspring colonies of the regulation of foraging will be investigated. A genome-wide association study will be conducted to investigate the genetic architecture underlying this variation in collective behavior.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.