The genetic basis of male mating success in the Yellow Fever mosquito, Aedes aegypti

Abstract

Aedes aegypti is responsible for the transmission of many emerging and re-emerging pathogens. Understanding Ae. aegypti mating behaviour and its genetic basis is important for the improvement and development of mosquito control strategies. While male mating success is intrinsically important in spreading desirable genes, sterility, or endosymbionts in reproductive control, we know relatively little about variation in the male mating success phenotype and its genetic basis. Through this thesis I investigated the variation in male mating success, using a novel assay designed to incorporate relevant sexual selection pressures, and estimated its heritability. I found evidence for a skew in male mating success, with very few males mating multiple times, despite the capacity to do so. Male mating success likely has a genetic basis, though the proportion of additive genetic variation contributing to the phenotype is low. I went on to use an experimental evolution and whole genome sequencing approach to demonstrate the role of sexual selection in shaping the Ae. aegypti genome. Manipulating the strength of sexual selection resulted in rapid genome-wide changes across all three chromosomes, with populations evolved in the presence of sexual selection retaining genomic similarity to their field-derived ancestors, which are predicted to have experienced strong sexual selection. I used gene ontology and functional effect analyses to show that many of the genes that responded consistently in all experimental replicates were associated with odour perception. I also identified a small number of potentially sexually selected genes that, after expression manipulation with RNAi, were tested for effects on male mating phenotypes. Males with reduced expression of one of these genes, pickpocket315, showed an altered mating phenotype, with males less likely to inseminate females, and making fewer attempts to mate overall. These results highlight that sexual selection is an important evolutionary force in Ae. aegypti mating systems, creating variation in phenotypes, and exerting a powerful effect on the genome. The results also have important consequences for those strategies that depend upon rearing mosquitoes en-masse for field release, and for the design of new mosquito control strategies that target mating behaviours.