Our understanding of animal ornaments and the mating preferences driving their exaggeration is limited by knowledge of their genetics. Post-copulatory sexual selection is credited with the rapid evolution of female sperm-storage organ morphology and corresponding sperm quality traits across diverse taxa. In Drosophila, the mechanisms by which longer flagella convey an advantage in the competition among sperm for limited storage space in the female, and by which female sperm-storage organ morphology biases fertilization in favour of longer sperm have been resolved. However, the evolutionary genetics underlying this model post-copulatory ornament and preference system have remained elusive. Here we combined comparative analyses of 149 Drosophila species, a genome-wide association study in Drosophila melanogaster and molecular evolutionary analysis of ~9,400 genes to elucidate how sperm and female sperm-storage organ length co-evolved into one of nature's most extreme ornaments and preferences. Our results reveal a diverse repertoire of pleiotropic genes linking sperm length and seminal receptacle length expression to central nervous system development and sensory biology. Sperm length development appears condition-dependent and is governed by conserved hormonal (insulin/insulin-like growth factor) and developmental (including Notch and Fruitless) pathways. Central developmental pathway genes, including Notch, also comprised the majority of a restricted set of genes contributing to both intraspecific and interspecific variation in sperm length. Our findings support 'good genes' models of female preference evolution.
© 2024. The Author(s), under exclusive licence to Springer Nature Limited.