Individual, but not population asymmetries, are modulated by social environment and genotype in Drosophila melanogaster

Abstract

theory predicts that social interactions can induce an alignment of behavioral asymmetries between individuals (i.e., population-level lateralization), but evidence for this effect is mixed. To understand how interaction with other individuals affects behavioral asymmetries, we systematically manipulated the social environment of Drosophila melanogaster, testing individual flies and dyads (female-male, female-female and male-male pairs). In these social contexts we measured individual and population asymmetries in individual behaviors (circling asymmetry, wing use) and dyadic behaviors (relative position and orientation between two flies) in five different genotypes. We reasoned that if coordination between individuals drives alignment of behavioral asymmetries, greater alignment at the populationlevel should be observed in social contexts compared to solitary individuals. We observed that the presence of other individuals influenced the behavior and position of flies but had unexpected effects on individual and population asymmetries: individual-level asymmetries were strong and modulated by the social context but population-level asymmetries were mild or absent. Moreover, the strength of individual-level asymmetries differed between strains, but this was not the case for populationlevel asymmetries. These findings suggest that the degree of social interaction found in Drosophila is insufficient to drive population-level behavioral asymmetries.Consistent left-right asymmetries in brain and behavior are widespread among animal species 1-4 . For instance, the vast majority of people is right handed (a behavior controlled by the left hemisphere), and an advantage of using the left eye (right hemisphere) has been observed in agonistic interactions in chicks 5 , lizards 6 , toads 7 and baboons 8 , while in bees the use of left antennae enhances aggressive behavior 9 and the use of the right antenna is involved in social behavior 10 . In these cases, when asymmetries are aligned on the same side in the majority of the population, we consider this population-level lateralization or directional asymmetry. In other cases, individuals exhibit strong and consistent preferences for one side, but these are not aligned at the population level and we define these cases individual-level lateralization or antisymmetry.How the presence of other individuals influences these asymmetries at the individual and group level remains largely unknown. Mathematical models suggest that selective pressures associated with living in social contexts enhance the alignment of behavioral asymmetries (population-level lateralization), due to the advantages of coordinating between individuals 11,12 . This hypothesis predicts population-level asymmetries in social contexts more than in individual contexts, for the contexts that occurred repeatedly in the course of evolution (for a recent review see 13 ). The growing evidence on the effect of the social context on asymmetric behavior, though, is mixed 9,14 . Contexts that are expected to elicit coord...

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