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.
Highlights
Extensive research across a broad range of taxa has revealed that the proteins involved in sexual reproduction often evolve rapidly due to positive selection
It is often hypothesized that this rapid evolution reflects a coevolutionary relationship with the female reproductive tract
We discovered that D. arizonae females produce an array of ‘‘digestive’’ enzymes in their reproductive tracts
Summary
Extensive research across a broad range of taxa has revealed that the proteins involved in sexual reproduction often evolve rapidly due to positive selection (reviewed in [1,2,3]). The selective forces that underlie this pattern remain unclear, it frequently has been postulated that adaptive evolution of reproductive proteins may result from intersexual coevolution [1,2,3]. Several female reproductive tract proteins [28,29,30] and egg membrane proteins [31] show evidence of positive selection, these analyses largely have been confined to the melanogaster species group. It is unclear, how diversity in female reproductive physiology and mating system across the genus [reviewed in 12,32] is reflected in their reproductive proteins.
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