Genomic architecture of species-specific sex pheromone variation and mate choice

Abstract

Speciation often begins with subtle changes in sexual communication and mate choice, yet the genetic basis of these early reproductive barriers remains largely unresolved. Here, we dissect the chemical and genomic architecture underlying species-specific female cuticular sex pheromones and their role in mate choice in two closely related parasitoid wasp species. Using high-resolution quantitative trait locus (QTL) mapping, fine-scale chemical profiling, and behavioral assays on hybrid populations, we identify three methyl-branched alkanes as key pheromonal compounds that strongly predict male mating preferences. QTL explaining their species-specific variation partially co-localize with genomic regions enriched for candidate genes involved in cuticular hydrocarbon biosynthesis, including cytochrome P450 enzymes and fatty acid synthases. These findings suggest a potential mechanistic link between the variation in these gene clusters and species-specific chemical signaling. Further comparative analyses reveal hitherto unrecognized sex-specific regulatory effects, cytoplasmic influences, and complex genomic interactions shaping the variation in these pheromonal profiles. This study is among the first to connect individual pheromone compounds with mate choice and their underlying genomic basis in a haplodiploid system, offering a rare glimpse into how chemical divergence can reinforce behavioral isolation and potentially drive early speciation.