Mosaic evolution of molecular pathways for sex pheromone communication in a butterfly

Unraveling theorigin of molecular pathways underlying the evolution of adaptive traits is essential forunderstandinghow new lineagesemerge, including the relative contribution ofconserved, ancestral traits, and newly evolved, derived traits. Here, we investigated the evolutionary divergence of sex pheromone communication from moths (mostly nocturnal) to butterflies (mostly diurnal)that occurred~98million years ago. In moths, females typically emit pheromones to attract male mates, but in butterflies pheromonesand used by females for mate choice. The molecular bases of sex pheromone communication arewellunderstood in moths, but haveremained virtually unexplored in butterflies. We useda combination of transcriptomics, real time qPCR, and phylogenetics, to identify genes involved in different steps of sex pheromone communication in the butterflyBicyclus anynana. Our results show that the biosynthesis and reception of sex pheromonesrelies both on moth-specific gene families (reductases) and onmore ancestral insect gene families (desaturases, olfactory receptors, odorant binding proteins). Interestingly, B. anynana further appears to use what was believed to be the moth-specific neuropeptide Pheromone Biosynthesis Activating Neuropeptide (PBAN) for regulationof sex pheromone production. Altogether, our results suggest that a mosaic pattern best explains how sex pheromone communication evolved in butterflies, with some molecular components derived from moths, and others conserved from more ancient insect ancestors. This is the first large-scale analysis of the genetic pathways underlying sex pheromone communication in a butterfly.