Academic journal article Genetics

Duplication, Selection and Gene Conversion in a Drosophila Mojavensis Female Reproductive Protein Family

Academic journal article Genetics

Duplication, Selection and Gene Conversion in a Drosophila Mojavensis Female Reproductive Protein Family

Article excerpt


Protein components of the Drosophila male ejaculate, several of which evolve rapidly, are critical modulators of reproductive success. Recent studies of female reproductive tract proteins indicate they also are extremely divergent between species, suggesting that reproductive molecules may coevolve between the sexes. Our current understanding of intersexual coevolution, however, is severely limited by the paucity of genetic and evolutionary studies on the female molecules involved. Physiological evidence of ejaculate-female coadaptation, paired with a promiscuous mating system, makes Drosophila mojavensis an exciting model system in which to study the evolution of reproductive proteins. Here we explore the evolutionary dynamics of a five-paralog gene family of female reproductive proteases within populations of D. mojavensis and throughout the repleta species group. We show that the proteins have experienced ongoing gene duplication and adaptive evolution and further exhibit dynamic patterns of pseudogenation, copy number variation, gene conversion, and selection within geographically isolated populations of D. mojavensis. The integration of these patterns in a single gene family has never before been documented in a reproductive protein.

IN internally fertilizing organisms, female reproductive tracts are the arena for a dynamic molecular interface between the sexes. Ejaculate-female interactions are essential to sperm fate and fertilization, guiding sperm through the female reproductive tract, preserving them in this environment, and ultimately mediating gamete fusion (reviewed in Neubaum and Wolfner 1999). Reproductive tract interactions also modulate critical postmating changes in female behavior and physiology, such as upregulating immune response, reformatting the female reproductive tract, and delaying female remating (reviewed in Robertson 2007; Wolfner 2007).

Despite the significance of ejaculate-female interactions for overall fitness, the male molecules involved in these processes exhibit dynamic evolutionary histories. 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; Panhuis et al. 2006). Similarly, lineage-specific gene duplications have been documented in Drosophila seminal fluid proteins (Cirera and Aguade 1998; Wagstaff and Begun 2007; Almeida and Desalle 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).

The rapid evolution of male ejaculates frequently is postulated to arise from molecular coevolution with interacting proteins in the female reproductive tract (Parker 1979; Eberhard 1996; Swanson and Vacquier 2002). If this is the case, female reproductive molecules are also expected to evolve rapidly. Recent evidence of adaptive evolution in Drosophila female reproductive tract proteins is consistent with this prediction (Swanson et al. 2004; Panhuis and Swanson 2006; Kelleher et al. 2007; Lawniczak and Begun 2007; Prokupek et al. 2008). Compared to the preponderance of studies of male ejaculates, however, the dynamics of female proteins remain largely unexplored.

Two, nonmutually exclusive mechanisms are hypothesized to result in reciprocal evolutionary change between male and female reproductive molecules. First, cryptic female choice could empower females to bias fertilization success toward certain males based on postcopulatory biochemical cues (Eberhard 1996). Cryptic female choice may lead to cyclical evolution of male trait and female preference, consistent with traditional models of runaway sexual selection (Fisher 1915; 1930). …

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