Molecular Population Genetics of Accessory Gland Protein Genes and Testis-Expressed Genes in Drosophila Mojavensis and D. Arizonae

Article excerpt


Molecular population genetic investigation of Drosophila male reproductive genes has focused primarily on melanogaster subgroup accessory gland protein genes (Acp's). Consistent with observations from male reproductive genes of numerous taxa, Acp's evolve more rapidly than nonreproductive genes. However, within the Drosophila genus, large data sets from additional types of male reproductive genes and from different species groups are lacking. Here we report findings from a molecular population genetics analysis of male reproductive genes of the repleta group species, Drosophila arizonae and D. mojavensis. We find that Acp's have dramatically higher average pairwise K^sub a^/K^sub s^ (0.93) than testis-enriched genes (0.19) and previously reported melanogaster subgroup Acp's (0.42). Overall, 10 of 19 Acp's have K^sub a^/ K^sub s^ > 1 either in nonpolarized analyses or in at least one lineage of polarized analyses. Of the nine Acp's for which outgroup data were available, average K^sub a^/ K^sub s^ was considerably higher in D. mojavensis (2.08) than in D. arizonae (0.87). Contrasts of polymorphism and divergence suggest that adaptive protein evolution at Acp's is more common in D. mojavensis than in D. arizonae.

MOLECULAR studies in a diverse array of animal taxa suggest that genes involved in reproduction evolve at an accelerated rate relative to other genes (reviewed in SWANSON and VACQUIER 2002). Positive selection has been inferred for some proteins (SwANSON and VACQUIER 1995; METZ and PALUMBI 1996; SUTTON and WILKINSON 1997; WYCKOFF et al. 2000; TORGERSON et al. 2002), although population genetic data are sufficiently sparse to leave unresolved the question of the relative importance of directional selection vs. genetic drift in reproduction-related proteins compared to other protein classes. In any case, rapid phenotypic/ molecular evolution of reproductive characters/genes is consistent with the notion that male-male and malefemale interactions may contribute to the rapid divergence between populations and the evolution of reproductive isolation (EBERHARD 1996; RICE 1998).

Molecular evolutionary investigation of Drosophila reproduction has focused on male accessory gland protein genes (Acp's) of melanogaster subgroup species. The number of putative Acp's in these species is on the order of 83 (SwANSON et al. 2001), although <20 have extensive experimental support (SCHAFER 1986; DiBENEDETTO et al. 1987; CHEN et al. 1988; MONSMA and WOLFNER 1988; WOLFNER et al. 1997). Genetic analysis has shown that Acp's contribute to proper sperm storage (NEUBAUM and WOLFNER 1999; TRAM and WOLFNER 1999; CHAPMAN et al. 2000), normal ovulation and oviposition (HERNDON and WOLFNER 1995; HEIFETZ et al. 2000), increased egg-laying rates, and reduced female receptivity (CHEN et al. 1988; AIGAKI et al. 1991; KALB et al. 1993; CHAPMAN et al. 2003; LIU and KUBLI 2003). Acp's show higher rates of protein divergence (AouADÉ 1997, 1998,1999; TsAURand Wu 1997; TSAURétal. 1998; BEGUN et al. 2000; SWANSON et al. 2001) and protein polymorphism (COULTHART and SINGH 1988; BEGUN et al. 2000) compared to "average" proteins in Drosophila melanogaster and D. simulans (e.g., BEGUN et al. 2000). Less energy has been devoted to population genetic investigation of male reproductive genes primarily expressed in testes (but see DUVERNELL and EANES 2000; PARSCH et al. 200Ia). However, a few analyses suggest that Drosophila testis-expressed genes evolve quickly (PARSCH et al. 2001b; MEIKLEJOHN et al. 2004; RICHARDS et al 2005) and may sometimes be associated with evolution of novel function (LONG and LANGLEY 1993; NURMINSKY et al. 1998; BETRAN and LONG 2003).

Because our current population genetic understanding of Drosophila is dominated by data from melanogaster subgroup species, we have no way of knowing whether the patterns of polymorphism and divergence or the functional biology of reproduction-related proteins will be similar in other Drosophila species (WAGSTAFF and BEGUN 2005). …