Evolutionary Mechanisms Behind Social Structures in Drosophila

Cultural norms, collective decisions, reproductive behaviour, and pathogen transmission all emerge from interaction patterns within animal social groups. These patterns of organization are captured by social network analysis, and social interaction networks (SINs) have been described for a wide variety of animals including fish, insects, birds, and mammals. The analysis of SINs in the fruit fly, Drosophila melanogaster, revealed complex group dynamics and that the structure of group life is inherited. The aim of this thesis is to apply social network analysis to various Drosophila species and model the evolution of social behaviour. Using a comparative ecological, phylogenetic, and behavioural approach, I compare the different properties of SINs formed by 20 drosophilids. I investigate whether drosophilid network structures arise from common ancestry, a response to the species’ past climate, other social behaviours, or a combination of these factors and demonstrate that the social distance at which flies interact correlates with the drosophilid phylogeny. This indicates that rudimentary aspects of social communication have remained largely unchanged in the evolutionary history of these insects. I also report that differences in past geographic climate data predict species’ differences in current SIN properties, whilephylogenetic signal tests revealed that drosophilid phylogeny offered no value in predicting species’ SINs. This suggests that group-level social behaviour in drosophilids is shaped by divergent climates. Other mechanisms that promotecharacter displacement between closely related species could also account for species’ differences in SINs, such as reinforcement. To test whether social structures are associated with sexual isolation between species, I conduct an experimental evolution study using the sister species Drosophila pseudoobscura (Dpse) and Drosophila persimilis (Dper). Like previously published work, I maintained independent populations of Dpse and Dper flies in mixed cultures (experimental sympatry) and independent populations of Dpse and Dper flies in separate cultures (experimental allopatry). I find evidence that sexual isolation, measured through frequency of hybrid offspring, decreased after 6 generations of selection in experimental sympatry. I also establish that the cuticular hydrocarbon (CHC) compound 5, 9-pentacosadiene (5, 9-PD) diverged between male Dpse/Dper and converged between female Dpse/Dper, suggesting increased sexual dimorphism reinforced the species barriers. When investigating social structures of mixed-sex and mixed-species fly groups,I find no evidence that SINs influence sexual isolation. To determine if this resulted fromanalyzing complex social groups, I divided the fly groups into smaller subgroups and compared SINs generated from heterospecific interactions versus conspecific interactions. Through this analysis, I detected divergence in the SINs between allopatric and sympatric Dpse flies. Together the results suggest divergence between CHCs, and SINs are associated with increased sexual isolation between species maintained in experimental sympatry for six generations. This thesis enhances the scope of social network analysis in Drosophila by testing broad evolutionary hypotheses and the findings bring us closer to understanding how social behaviour evolved within the fly.

Keywords: Drosophila
Evolution
Social Networks
Advisor: Levine, Joel D