The loci of behavioral evolution: Fas2 and tilB underlie differences in pupation site choice behavior between Drosophila melanogaster and D. simulans

Abstract

The recent boom in genotype-phenotype studies has led to a greater understanding of the genetic architecture of a variety of traits. Among these traits, however, behaviors are still lacking, perhaps because they are complex and environmentally sensitive phenotypes, making them difficult to measure reliably for association studies. Here, we aim to fill this gap in knowledge with the results of a genetic screen for a complex behavioral difference, pupation site choice, between Drosophila melanogaster and D. simulans. In this study, we demonstrate a significant contribution of the X chromosome to the difference in pupation site choice behavior between these species. Using a panel of X-chromosome deletions, we screened the majority of the X chromosome for causal loci, and identified two regions that explain a large proportion of the X-effect. We then used gene disruptions and RNAi to demonstrate the substantial effects of a single gene within each region: Fas2 and tilB. Finally, we show that differences in tilB expression underlie species differences in pupation site choice behavior, and that generally, pupation site choice behavior appears to be correlated with relative expression of this gene. Our results suggest that even complex, environmentally sensitive behaviors may evolve through changes to loci with large phenotypic effects.\n\nAuthor summaryBehaviors are complex traits that involve sensory detection, higher level processing, and a coordinated output by the nervous system. This level of processing is highly susceptible to environmentally induced variation. Because of their complexity and sensitivity, behaviors are difficult to study; as a result, we have very little understanding of the genes involved in behavioral variation. In this study, we use common laboratory fruit fly model, Drosophila, to address this gap and dissect the genetic underpinnings of an environmentally sensitive behavior that differs between species. We find that a significant amount of the phenotypic difference between species is explained by a single chromosome. We further show that just two genes on this chromosome account for a large majority of its effect, suggesting that the genetic basis of complex behavioral evolution may be simpler than anticipated. For one of these genes, we show that a species-level difference in gene expression is associated with the difference in behavior. Our results contribute to a growing number of studies identifying the genetic components of behavior. Ultimately, we hope to use these data to better predict the number, types, and effects of genetic mutations necessary for complex behaviors to evolve.