Insights into the Evolution of Moth Pheromone Communication: Lessons from the European Corn Borer

Abstract: Chemical communication by means of sex pheromones is central to the mating systems of a wide range of organisms. Because reproductive isolation is often based on pheromone differences, understanding how pheromones diverge is necessary for a complete comprehension of the speciation process. Moths (Insecta: Lepidoptera) contributes highly relevant examples to the theory of speciation because subtle chemical changes in their sex pheromones may often be the initial triggers for population divergence, and lead to reproductive isolation. Over the years, the European corn borer Ostrinia nubilalis and its congeners have become a model system for investigating the genetics of pheromone communication systems and the role of sexual signals in speciation. The Ostrinia system has received a lot of attention because of the naturally-occurring pheromone polymorphism, and the relatively simple nature of the pheromone components which seemed amenable to a reductionistic approach. The system has turned out to be surprisingly complex, because the genetic bases for pheromone production by females, chemosensory responses by males, and behavioural responses by males have been shown to be different. In this thesis, I report on advances made on several fronts of the Ostrinia communication system. To summarize, I describe the identification of the enzyme-encoding gene pgFAR which is responsible for phenotypic variation in female pheromone production among O. nubilalis and allied species. The pgFAR gene encodes a Lepidoptera-specific fatty acyl-CoA reductase that catalyzes the NADPH-dependent reduction of fatty acyl substrates during the pheromone biosynthesis. I could show that (i) structural variation in the coding region of the protein is tightly associated with variation in the substrate preference of the enzyme, (ii) the ratio of pheromone components used by O. nubilalis and its congeners is modulated by the pgFAR activity, (iii) the pgFAR gene experience positive Darwinian selection, and (iv) mutational changes at sites under selection cause both gradual or saltational shift in the enzyme activity. I also explored whether pheromone-specific olfactory receptors expressed on male antenna are candidate barrier genes involved in the differentiation between the pheromone races of O. nubilalis. I found evidence that three sex-linked loci are under selection and well associated with genetic differentiation between the races, suggesting that these genes are good candidate barriergenes worth considering for measuring natural selection in the wild. Finally, I document the role played by a male courtship pheromone in mate choice, and its implication on the evolution of female pheromone as a consequence of gene sharing.