Adaptive Evolution of Recently Duplicated Accessory Gland Protein Genes in Desert Drosophila

Abstract

The relationship between animal mating system variation and patterns of protein polymorphism and divergence is poorly understood. Drosophila provides an excellent system for addressing this issue, as there is abundant interspecific mating system variation. For example, compared to D. melanogaster subgroup species, repleta group species have higher remating rates, delayed sexual maturity, and several other interesting differences. We previously showed that accessory gland protein genes (Acp's) of Drosophila mojavensis and D. arizonae evolve more rapidly than Acp's in the D. melanogaster subgroup and that adaptive Acp protein evolution is likely more common in D. mojavensis/D. arizonae than in D. melanogaster/D. simulans. These findings are consistent with the idea that greater postcopulatory selection results in more adaptive evolution of seminal fluid proteins in the repleta group flies. Here we report another interesting evolutionary difference between the repleta group and the D. melanogaster subgroup Acp's. Acp gene duplications are present in D. melanogaster, but their high sequence divergence indicates that the fixation rate of duplicated Acp's has been low in this lineage. Here we report that D. mojavensis and D. arizonae genomes contain several very young duplicated Acp's and that these Acp's have experienced very rapid, adaptive protein divergence. We propose that rapid remating of female desert Drosophila generates selection for continuous diversification of the male Acp complement to improve male fertilization potential. Thus, mating system variation may be associated with adaptive protein divergence as well as with duplication of Acp's in Drosophila.

Postmating transcriptional changes in reproductive tracts of con- and heterospecifically mated Drosophila mojavensis females

“…The mating systems of these two species are characterized by frequent female remating relative to D. melanogaster (20), along with extensive intersexual coevolution of postcopulatory traits (21)(22)(23), including rapid evolution of both male and female reproductive proteins (24)(25)(26)(27)(28). Consistent with expectations, interspecific crosses also exhibit strong PMPZ isolation, particularly those involving D. mojavensis females.…”

Duplication, Selection and Gene Conversion in aDrosophila mojavensisFemale Reproductive Protein Family

“…Lineage-specific duplicates are common among Drosophila reproductive proteins (Cirera and Aguadé 1998;Loppin et al 2005;Dorus et al 2008;Findlay et al 2008), particularly within the repleta species group Wagstaff and Begun 2007;Almeida andDesalle 2008, 2009). Genomewide patterns of gene gain and loss across twelve Drosophila genomes, furthermore, indicates proteins involved in sexual reproduction turn over more rapidly than other functional classes (Hahn et al 2007).…”

“…Seminal proteins and sperm proteins have been observed to evolve rapidly in a broad range of taxa (reviewed in Swanson and Vacquier 2002;Clark et al 2006;. Similarly, lineage-specific gene duplications have been documented in Drosophila seminal fluid proteins (Cirera and Aguadé 1998;Wagstaff and Begun 2007;Almeida andDesalle 2008, 2009;Findlay et al 2008), as well as fertilization proteins in both Drosophila and abalone (Loppin et al 2005;Clark et al 2007). Finally, Drosophila male ejaculates are known to undergo a high frequency of lineage-specific changes in seminal fluid content, by functionally coopting existing genes and acquiring novel genes from noncoding sequence (Begun and Lindfors 2005;Mueller et al 2005;Begun et al 2006;Findlay et al 2008).…”

Sperm wars and the evolution of male fertility

“…Evidence for a role of sperm competition in protein evolution also comes from studies of Drosophila. Here too accessory gland genes show evidence of strong positive selection (Haerty et al 2007), and accessory gland protein divergence is greater in lineages of Drosophila with greater postmating sexual selection (Wagstaff & Begun 2007).…”