Gene Duplication and Adaptive Evolution of Digestive Proteases in Drosophila arizonae Female Reproductive Tracts

Open Access
Publisher Website
Google Scholar
Abstract
It frequently has been postulated that intersexual coevolution between the male ejaculate and the female reproductive tract is a driving force in the rapid evolution of reproductive proteins. The dearth of research on female tracts, however, presents a major obstacle to empirical tests of this hypothesis. Here, we employ a comparative EST approach to identify 241 candidate female reproductive proteins in Drosophila arizonae, a repleta group species in which physiological ejaculate–female coevolution has been documented. Thirty-one of these proteins exhibit elevated amino acid substitution rates, making them candidates for molecular coevolution with the male ejaculate. Strikingly, we also discovered 12 unique digestive proteases whose expression is specific to the D. arizonae lower female reproductive tract. These enzymes belong to classes most commonly found in the gastrointestinal tracts of a diverse array of organisms. We show that these proteases are associated with recent, lineage-specific gene duplications in the Drosophila repleta species group, and exhibit strong signatures of positive selection. Observation of adaptive evolution in several female reproductive tract proteins indicates they are active players in the evolution of reproductive tract interactions. Additionally, pervasive gene duplication, adaptive evolution, and rapid acquisition of a novel digestive function by the female reproductive tract points to a novel coevolutionary mechanism of ejaculate–female interaction. In a broad range of organisms, including humans, molecular interactions between the male ejaculate and the female reproductive tract play integral roles in sexual reproduction. Although these interactions are essential, the biochemical composition of the male ejaculate can change rapidly over short evolutionary time periods. It is often hypothesized that this rapid evolution reflects a coevolutionary relationship with the female reproductive tract. The paucity of research on females, however, presents a formidable challenge to empirical tests of this hypothesis. In this study, we sought to identify proteins in the female reproductive tracts of D. arizonae that may be interacting or coevolving with the male ejaculate. Unexpectedly, we discovered that D. arizonae females produce an array of “digestive” enzymes in their reproductive tracts. These classes of enzymes are normally found in the gut, where they degrade ingested food for nutritional uptake. In D. arizonae, these enzymes have resulted from recent gene duplications, and natural selection has caused rapid and radical changes in their amino acid sequences. We propose that this pattern of duplication and diversification reflects the “female side” of a coevolutionary relationship with the male ejaculate. Exploring the “male side” of this relationship is an important avenue for future research.