Quantity matters: male sex pheromone signals mate quality in the parasitic wasp Nasonia vitripennis

Abstract

Sexual selection theory asserts that females are well adapted to sense signals indicating the quality of potential mates. One crucial male quality parameter is functional fertility (i.e. the success of ejaculates in fertilizing eggs). The phenotype-linked fertility hypothesis (PLFH) predicts that functional fertility of males is reflected by phenotypic traits that influence female mate choice. Here, we show for Nasonia vitripennis, a parasitic wasp with haplodiploid sex determination and female-biased sex ratios, that females use olfactory cues to discriminate against sperm-limited males. We found sperm limitation in newly emerged and multiply mated males (seven or more previous matings) as indicated by a higher proportion of sons in the offspring fathered by these males. Sperm limitation correlated with clearly reduced pheromone titres. In behavioural bioassays, females oriented towards higher doses of the synthetic pheromone and were attracted more often to scent marks of males with a full sperm load than to those of sperm-limited males. Our data support the PLFH and suggest that N. vitripennis females are able to decrease the risk of getting constrained to produce suboptimal offspring sex ratios by orienting towards gradients of the male sex pheromone.

Figure 1.

Relationship between the mating history (number of previous copulations) of Nasonia vitripennis males and (a) the lifetime offspring sex ratio (proportion of males) produced by the last mated female, and (b) the pheromone titre. Data are given as means±s.e. Asterisks indicate significant differences between treatments and the control (= 0 previous copulations) at (*) p < 0.05 or (**) p < 0.01 (Kruskal–Wallis H-test and multiple Bonferroni-corrected Mann–Whitney U-tests). Different lowercase letters indicate significant differences at p < 0.05 (one-way ANOVA followed by least significant difference tests).

Figure 2.

Relationship between the age of Nasonia vitripennis males and (a) the lifetime offspring sex ratio (proportion of males) produced by the mated female, and (b) the pheromone titre. Asterisks indicate significant differences at (***) p < 0.001 (Mann–Whitney U-test).

Figure 3.

Behavioural response of virgin Nasonia vitripennis females to natural male pheromone deposits and to different doses of synthetic pheromone in a still-air Y-olfactometer (a–i) and an open arena bioassay (j). Asterisks indicate significant differences at (***) p < 0.001, (**) p < 0.01 and (*) p < 0.05; n.s., not significant (one-tailed binominal test).