Female behavioral cues control male courtship plasticity independent of female pheromones in African Drosophila melanogaster

Abstract

Sexual interactions involve the exchange of information-including olfactory, auditory, and visual cues-that has been shaped by sexual selection to maximize fitness. While these courtship signals and behaviors are often characterized as stereotypical and species-specific, male courtship is plastic and can depend on the population identity of the courted female. The ability of a male to adjust his courtship behavior based on female identity has significant implications for how selection operates on courtship, potentially driving behavioral divergence between populations and the eventual emergence of new species. A major challenge is identifying the cues that males use to adjust their courtship strategy. We used Drosophila melanogaster to investigate the mechanisms facilitating courtship plasticity, focusing on male song production. Male song is often considered the paramount behavior performed by males and is stimulated by female pheromones. Previous observations have focused on cosmopolitan (non-African) genotypes, whereas the singing rate and singing plasticity is highly variable in African populations. In genotypes from Zimbabwe, females have a different major pheromone compound (5,9-HD) compared to non-African females and show strong behavioral preference for Zimbabwe males. We created a Zimbabwe genotype lacking 5,9-HD by disrupting the gene desat2 in the Zimbabwe Z53 strain. We tested the hypothesis that Zimbabwe male courtship plasticity depends on female pheromones by allowing males to court non-African, wild type Z53, and Z53 desat2 null mutant females. We found that males treated Z53 desat2 null females like wild type Z53 females, not using pheromone cues to determine singing and courtship plasticity. This suggests that other female behavioral feedback influences singing plasticity. This courtship plasticity could contribute to the asymmetrical reproductive isolation between these populations and could provide insight to the broad pattern of asymmetrical reproductive isolation across broad taxonomic groups.