Gene age shapes functional and evolutionary properties of the Drosophila seminal fluid proteome

Abstract

Seminal fluid proteins (Sfps) are crucial for animal reproductive success, with most Sfps-encoding genes believed to be evolutionarily young and rapidly evolving. By employing estimates of the phylogenetic origin of each Drosophila melanogaster Sfp gene based on genomic resources that include outgroup species to the Drosophila genus, we examined the functional attributes and evolutionary characteristics of Sfp genes relative to their evolutionary age. Contrary to common belief, 62% of Sfp genes existed in the genome of the ancestor to such genus. These ancient genes have broadened their expression profiles, expanded their biological roles, and formed a denser network of interactions with non-Sfp genes. This increased pleiotropy has imposed constraints on the rate of sequence evolution in ancient Sfp genes compared to younger ones. Within the Sfp interactome, we identified a fast-evolving core sub-network of younger genes with more restricted tissue expression and functions. Our findings uncover a large, previously unrecognized set of ancient Sfp genes with distinct genomic, functional, and evolutionary characteristics compared to the younger, more commonly studied Sfp genes.