Academic journal article Genetics

Associations between Sperm Competition and Natural Variation in Male Reproductive Genes on the Third Chromosome of Drosophila Melanogaster

Academic journal article Genetics

Associations between Sperm Competition and Natural Variation in Male Reproductive Genes on the Third Chromosome of Drosophila Melanogaster

Article excerpt

ABSTRACT

We applied association analysis to elucidate the genetic basis for variation in phenotypes affecting postcopulatory sexual selection in a natural population of Drosophila melanogaster. We scored 96 third chromosome substitution lines for nine phenotypes affecting sperm competitive ability and genotyped them at 72 polymorphisms in 13 male reproductive genes. Significant heterogeneity among lines (P < 0.01) was detected for all phenotypes except male-induced refractoriness (P = 0.053). We identified 24 associations (8 single-marker associations, 12 three-marker haplotype associations, and 4 cases of epistasis revealed by single-marker interactions). Fewer than 9 of these associations are likely to be false positives. Several associations were consistent with previous findings [Acp70A with the male's influence on the female's refractoriness to remating (refractory), Esterase-6 with a male's remating probability (remating) and a measure of female offspring production ( fecundity)], but many are novel associations with uncharacterized seminal fluid proteins. Four genes showed evidence for pleiotropic effects [CG6168 with a measure of sperm competition (P2') and refractory, CG14560 with a defensive measure of sperm competition (P1') and a measure of female fecundity, Acp62F with P2' and a measure of female fecundity, and Esterase-6 with remating and a measure of female fecundity]. Our findings provide evidence that pleiotropy and epistasis are important factors in the genetic architecture of male reproductive success and show that haplotype analyses can identify associations missed in the single-marker approach.

IN species with polygamous mating systems, male success at gaining copulations may not be a reliable predictor of reproductive fitness, especially when sperm from multiple males are concurrently present in the reproductive tract of a single female (Parker 1970). Multiple mating by females establishes the opportunity for postcopulatory sexual selection through either cryptic female choice or sperm competition (Eberhard and Cordero 2003; Wigby and Chapman 2004). Postcopulatory sexual selection can be an important determinant of male reproductive fitness and studies from a variety of taxa consistently reveal marked differences among males in their ability to outcompete rival sperm for access to fertilizations (e.g., Preston et al. 2003; Konior et al. 2005; Malo et al. 2005).

Sperm competitive ability is a complex trait that is likely influenced by a number of variables, including ejaculate volume (Harcourt et al. 1981; Preston et al. 2003; Dixson and Anderson 2004), sperm motility (Gage et al. 2004), sperm morphology (Oppliger et al. 2003; Dixson and Anderson 2004), and seminal fluid proteins (reviewed in Poiani 2006). In the genus Drosophila, male accessory gland proteins (Acp's) are components of the seminal fluid, and there is abundant evidence that they are important determinants of phenotypes affecting postcopulatory sexual selection (Clark et al. 1995; Wolfner 2002; Chapman and Davies 2004; Fiumera et al. 2005). For example, both RNAi and mutational analyses have shown that Acp70A increases the rate of oviposition and decreases female receptivity to remating (Chen et al. 1988; Chapman et al. 2003; Liu and Kubli 2003). Acp26Aa increases egg-laying rate (Herndon and Wolfner 1995; Heifetz et al. 2000; Chapman et al. 2001) and Acp36DE is necessary for sperm storage (Neubaum and Wolfner 1999; Bloch Qazi and Wolfner 2003). PEB-me, a gelatinous protein product of the ejaculatory bulb, is responsible for the formation the female mating plug, which presumably acts to concentrate sperm near female storage organs (Lung and Wolfner 2001).

Many Acp's exhibit nonneutral patterns of genetic variation, suggesting they are under strong selective pressures (Aguadé et al. 1992; Aguadé 1998, 1999; Begun et al. 2000; Swanson et al. 2001; Tsaur et al. 2001; Kern et al. 2004). Postcopulatory sexual selection through sperm competition, cryptic female choice, or sexually antagonistic coevolution has often been proposed to account for the rapid evolution of male reproductive genes (see Rice 1996; Parker and Partridge 1998; Swanson and Vacquier 2002). …

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