Relative effectiveness of mating success and sperm competition at eliminating deleterious mutations in Drosophila melanogaster

Abstract

Condition-dependence theory predicts that sexual selection will facilitate adaptation by selecting against deleterious mutations that affect the expression of sexually selected traits indirectly via condition. Recent empirical studies have provided support for this prediction; however, their results do not elucidate the relative effects of pre- and postcopulatory sexual selection on deleterious mutations. We used the Drosophila melanogaster model system to discern the relative contributions of pre- and postcopulatory processes to selection against deleterious mutations. To assess second-male ejaculate competition success (P2; measured as the proportion of offspring attributable to the experimental male) and mating success, mutant and wild-type male D. melanogaster were given the opportunity to mate with females that were previously mated to a standard competitor male. This process was repeated for males subjected to a diet quality manipulation to test for effects of environmentally-manipulated condition on P2 and mating success. While none of the tested mutations affected P2, there was a clear effect of condition. Conversely, several of the mutations affected mating success, while condition showed no effect. Our results suggest that precopulatory selection may be more effective than postcopulatory selection at removing deleterious mutations. The opposite result obtained for our diet manipulation points to an interesting discrepancy between environmental and genetic manipulations of condition, which may be explained by the multidimensionality of condition. Establishing whether the various stages of sexual selection affect deleterious mutations differently, and to what extent, remains an important issue to resolve.

Figure 1. Relative offensive sperm competition success, given as second-male paternity (P2; mean +/− SE), for high- and low condition males.

Sperm competition success was measured as the proportion of offspring produced by high- or low condition males relative to a standard competitor mated to a given female. High condition males showed significantly higher P2 relative to low condition males.

Figure 2. Relative offensive sperm competition success, given as second-male paternity (P2; mean +/− SE), for mutant and wild-type males (a. Adv; b. Dr; c. Gl; d. Gla; e. Ly; f. Sb).

Wild-type treatments are listed as wt(M_i), where M_i represents the paired mutant treatment. Sperm competition success was measured as in Fig. 1. There were no significant differences between mutants and wild-types for any of the paired comparisons.

Figure 3. Relative mating success of mutant and wild-type males.

Mating was deemed successful when mutant or wild-type males achieved copulation with a nonvirgin female; unsuccessful matings occurred when males failed to copulate. Black bars represent mutant (or low condition, L) males; white bars depict wild-type (or high condition, H) males. Mutant-wild-type pairs are presented according to mutant genotype. Significant differences are indicated by an asterisk.