The foraging gene as a modifier of behavior: gene regulation, pleiotropy and plasticity

The Drosophila melanogaster foraging (for) gene, with its rover and sitter larval foraging variants, is an established behavior genetics model. Orthologues of the foraging gene also modulate the individual and social behavior of a wide range of species including the regulation of behavior in eusocial insects. In Drosophila, foraging modifies the expression of multiple traits, including feeding and foraging, stress tolerance, sleep, metabolism, aggression, escape responses, social behavior, and learning and memory. From a social context perspective, Drosophila foraging affects larval clustering during foraging under high larval densities, adult social behavior and social networks, and social learning. We wondered how foraging accomplishes its behavioral pleiotropy at the molecular level. We found that D. melanogaster foraging has a complex modular genomic structure with four promoters, 21 transcripts, and eight protein isoforms. The four promoter modules are differentially regulated during development and in a timescale, tissue, and cell-type dependent manner. Two examples illustrate these findings: the epigenetic regulation of the adult rover-sitter foraging-related phenotypes by G9a, a histone methyltransferase, and the regulation of differences the latency of rover compared to sitter larval escape responses to noxious stimuli such as parasitoid wasps. Our work provides a nuanced picture of the molecular basis of foraging’s pleiotropy and its contributions to behavioral plasticity. Together this data sets the scene for future studies of foraging’s co-option in social behavior evolution.

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