Evolution of chemical signals in Heliconius butterflies

Speciation requires a reduction in gene flow between species. This can be achieved even in sympatry if reproductive barrier traits are under divergent ecological or sexual selection. Chemical signals are the oldest form of communication in the living world, and have promoted speciation in many taxa through the process of “sensory drive”. Heliconius butterflies are model organisms in speciation, but few studies so far have been carried out on the evolution, genetics, physiology and regulation of their pheromones. In this study, I focus on two types of Heliconius pheromones: male sex pheromones (MSPs) involved in courtship, and antiaphrodisiacs used to enforce female monogamy. I investigated the macroevolution of MSPs across the Heliconiini tribe and found a burst of diversification at the base of the most speciose clade, and also that MSP divergence between sister species is strongly affected by the extent of sympatry. Both patterns are consistent with MSPs role as reproductive barriers in these butterflies. Using genetic crosses between two sympatric sister species, H. elevatus and H. pardalinus, I then mapped QTLs controlling differences in seven putative MSPs, and found that most QTLs were clustered and found in areas of genomic divergence between the species. For comparison with MSPs, I investigated the macroevolution of antiaphrodisiacs. I did not observe any evidence for a role of antiaphrodisiacs in reproductive isolation, but I identified some candidate compounds that may be behaviourally active, and observed an effect of host plant on antiaphrodisiac composition. Lastly, I found that the MSP and antiaphrodisiac blend compositions in H. charithonia and H. atthis, species with different mating strategies, to be strongly age-dependent. Despite these advances, the complexity of chemical signalling in these butterflies remains largely unknown. The candidate compounds and genes that I have uncovered are targets of future research through detailed behavioural assays, and genetic manipulation.