Molecular evolution of luciferase diversified bioluminescent signals in sea fireflies

Understanding the genetic causes of evolutionary diversification is challenging because differences across species are complex, often involving many genes. However, cases where single or few genetic loci affect a feature that varies dramatically across a radiation of species, would provide tractable opportunities to understand the genetics of diversification. Here, we show the diversification of bioluminescent signals in cypridinid ostracods (sea fireflies) to be strongly influenced by a single gene, cypridinid-luciferase. We find different evolutionary processes, including selection, drift, and constraint, each acted on c-luciferase at different times during evolutionary history and impacted different phenotypes, diversifying behavioral signals across species. In particular, some amino acid sites in c-luciferase evolved under episodic diversifying selection, and are associated significantly with phenotypic changes in both enzyme kinetics and color, which impact signals directly. We also find that multiple other amino acid positions in c-luciferase evolved neutrally or under purifying selection and may have impacted the variation of color of bioluminescent signals across genera. This work provides a rare glimpse into the genetic basis of diversification across many species, showing how multiple evolutionary processes may act at different times during a radiation of species to diversify phenotypes. These results indicate not only selection but also drift and constraint may be important evolutionary drivers of species diversification.