Academic journal article Genetics

Sperm Competitive Ability in Drosophila Melanogaster Associated with Variation in Male Reproductive Proteins

Academic journal article Genetics

Sperm Competitive Ability in Drosophila Melanogaster Associated with Variation in Male Reproductive Proteins

Article excerpt

ABSTRACT

Multiple mating by females establishes the opportunity for postcopulatory sexual selection favoring males whose sperm is preferentially employed in fertilizations. Here we use natural variation in a wild population of Drosophila melanogaster to investigate the genetic basis of sperm competitive ability. Approximately 101 chromosome 2 substitution lines were scored for components of sperm competitive ability (P1', P2', fecundity, remating rate, and refractoriness), genotyped at 70 polymorphic markers in 10 male reproductive genes, and measured for transcript abundance of those genes. Permutation tests were applied to quantify the statistical significance of associations between genotype and phenotype. Nine significant associations were identified between polymorphisms in the male reproductive genes and sperm competitive ability and 13 were identified between genotype and transcript abundance, but no significant associations were found between transcript abundance and sperm competitive ability. Pleiotropy was evident in two genes: a polymorphism in Acp33A associated with both P1' and P2' and a polymorphism in CG17331 associated with both elevated P2' and reduced refractoriness. The latter case is consistent with antagonistic pleiotropy and may serve as a mechanism maintaining genetic variation.

THERE are striking differences between strict monogamy and polygamy in the opportunity for sexual selection (BIRKHEAD and MØLLER 1998). Parentage studies using highly polymorphic molecular markers indicate that at least 50% of wild-captured Drosophila melanogaster females had mated with more than a single male (OCHANDO et al. 1996; HARSHMAN and CLARK 1998). While the benefits to females are often debated (see JENNIONS and PETRIE 2000; BIRKHEAD and PIZZARI 2002), polyandry provides the opportunity for postcopulatory sexual selection to influence patterns of reproductive success. In species with internal fertilization, reproductive success will likely be determined by complex interactions between sperm competition and cryptic female choice (BIRKHEAD and PIZZARI 2002). The ultimate outcome of these interactions will impact adaptive processes within populations and may influence higher-level processes such as speciation.

D. melanogaster males can increase their reproductive success not only by gaining additional mates (BATEMAN 1948), but also by influencing patterns of polyandry or affecting the use of sperm by females with whom they have mated. A male's reproductive success increases if he can prevent his mate from remating or if he can outcompete the sperm of other males to ensure that he fertilizes the majority of the female's eggs. Females, however, are unlikely to be passive recipients since natural selection is simultaneously maximizing their own reproductive success. If the reproductive interests of males and females differ, antagonistic coevolution between the sexes may influence postcopulatory sexual selection (PARKER 1979; RICE and HOLLAND 1997). Given the large effect that variation in reproductive success will have on overall fitness, traits affecting postcopulatory sexual selection are likely to be under strong selection in natural populations.

For selection to operate, variation must exist between individuals for traits affecting postcopulatory sexual selection, and empirical studies consistently demonstrate a genetic contribution to the observed phenotypic variance. For example, testis weight, ejaculate volume, and copulation duration have high heritabilities in dung beetles (SIMMONS and KOTIAHO 2002). Both male investment in spermatogenesis (PITNICK et al. 2001b) and female remating rate (PITNICK et al. 2001a) also have strong genetic components. The effect of the male genotype (CIVETTA and CLARK 2000; NILSSON et al 2003), the female genotype (CLARK and BEGUN 1998; NILSSON et al. 2003), and the interaction between the male and female genotype (CLARK et al. 1999; NILSSON et al. 2003) on components of postcopulatory sexual selection have been shown using chromosome extraction lines. …

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