CAREER: Genetic Architecture and Proximate Mechanisms Underlying Indirect Genetic Effects on Cooperative Antipredator Behavior

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A central problem in modern biology is understanding how an individual's traits, whether physical features, disease or behavior, result from the combined action of genes, the physical environment and the social environment in which an individual interacts. Describing genetic influences on behavior is particularly challenging if genes in social partners interact to generate behavior. Little is known about the extent of such genetic influences, whether their effects vary across populations or the physiological mechanisms that allow the genes in one individual to influence another individual's behavior. Trinidadian guppies are an excellent model system to study these effects on behavior because guppies perform a suite of cooperative antipredator behavior that is strongly influenced by social partners and which varies greatly across populations depending on predation risk. This project uses statistical genetics to describe the relative importance of an individual's own genes and those of its social partners for generating cooperation among guppies. This project will also link variation in physiology, gene expression, and sensory anatomy to variation in cooperation across populations. Undergraduates from under-represented groups will be provided long-term comprehensive research and mentorship experiences. An active learning curriculum for evolution classes will be developed. This work will advance our scientific understanding of the genetics of complex traits, including social behavior, while preparing diverse students to be scientists, educators, and mentors.How interacting phenotypes, such as cooperation, evolve depends on both the genetic architecture of the behavior and the structure of the social environment. This project will describe the complete genetic architecture of indirect genetic effects (IGEs) on guppy antipredator behavior, especially as it might vary with changes in social selection imposed by cooperation under differential predation risk. A quantitative genetic breeding design paired with behavioral experiments will measure the influence imposed by and responsiveness to social partners and genetic covariances between those traits for high and low predation populations. Variation in these traits will be correlated with differences in gene expression for hormone receptors and cognate hormone secretion, pheromone excretion, and somatosensory anatomy. Differences in social environments will be characterized by measuring the proportions of individuals in each population that are influential on and/or responsive to social their partners. Lastly, the combination of influential and responsive partners will be varied to measure how well different combinations cooperate, quantifying differences in social selection across populations. This work will provide some of the first experimental links between proximate mechanisms, variation in IGEs, and social selection. Data will be archived and made publically available through Dryad Digital Repository and GenBank, as appropriate.