Ancient secretory pathways contributed to the evolutionary origin of an ecologically impactful bioluminescence system

Abstract

Evolutionary innovations in chemical secretion - such as the production of secondary metabolites, pheromones, and toxins - profoundly impact ecological interactions across a broad diversity of life. These secretory innovations may involve a "legacy-plus-innovation" mode of evolution, whereby new biochemical pathways are integrated with conserved secretory processes to create novel products. Among secretory innovations, bioluminescence is important because it evolved convergently many times to influence predator-prey interactions, while often producing courtship signals linked to increased rates of speciation. However, whether or not deeply conserved secretory genes are used in secretory bioluminescence remains unexplored. Here, we show that in the ostracod Vargula tsujii, the evolutionary novel c-luciferase gene is co-expressed with many conserved genes, including those related to toxin production and high-output protein secretion. Our results demonstrate that the legacy-plus-innovation mode of secretory evolution, previously applied to sensory modalities of olfaction, gustation, and nociception, also encompasses light-producing signals generated by bioluminescent secretions. This extension broadens the paradigm of secretory diversification to include not only chemical signals but also bioluminescent light as an important medium of ecological interaction and evolutionary innovation. Significance StatementAnimals produce an enormous diversity of secreted chemical products, like toxins and pheromones, with wide-ranging impacts on ecological interactions. Although a deeply conserved toolkit of secretory genes may often underlie chemical interactions mediated through smell, taste, and sensing pain, whether or not this evolutionary mode generalizes to sensing light is unknown. Here we show that a bioluminescence secretion system, which creates light for anti-predator and courtship interactions, also uses genes of a deeply conserved secretory toolkit. Therefore, secretory innovations may act through all sensory modalities by integrating conserved genes with novel biosynthesis pathways, to serve as crucibles of evolutionary and ecological diversity.