Quantitative genetics of natural variation of behavior in Drosophila melanogaster: the possible role of the social environment on creating persistent patterns of group activity

Using a set of nine effectively isogenic lines collected from nature in 1998, we observed unperturbed behaviors of mixed-sex groups of Drosophila melanogaster. We repeatedly scanned replicated groups of genetically identical individuals, five females and five males, and recorded the behavior of each individual (i.e., walking, feeding, grooming, flying, courting, mating, fighting, or resting). From these behaviors, we made a composite variable of activity for our quantitative genetic analysis. Genotypes differed in activity, explaining 14.41% of the variation in activity; 8.60% of the variation was explained by a significant genotype x sex interaction, which signifies genetic variation for sexual dimorphism in behavior. Phenotypic plasticity explained 11.13% of the variation in activity. Different genotypes and sexes within genotypes had different rank orders of the component behaviors that contribute to activity. We found no effect of common rearing environment. Instead, differences between replicate groups within genotype accounted for 19.47% variation in activity, and activity was significantly repeatable across scans. This emergent group behavior is likely caused by differences between groups of interacting individuals, even though individuals were genetically identical across groups. Thus, emergent group behavior explained almost as much variation in activity as the combined sources of genetic variation (23.01%), and this is an additional level on which selection could operate: individuals and groups. We discuss how differences among groups could change patterns of additive genetic variation available for evolution. Furthermore, because the behavior of an individual is influenced by conspecifics, genotype interactions between individuals could contribute to indirect selection. Finally, if we consider activity as a syndrome governing all component behaviors with strong genetic correlations among behaviors within an individual, then these component behaviors cannot evolve independently. These results suggest that reductionist approaches of molecular behavior genetics may be incomplete and/or misleading when considering similar phenotypes at the population level or when trying to understand how behaviors evolve.