Abstract
BackgroundIn species that reproduce with sexual reproduction, males and females often have opposite strategies to maximize their own fitness. For instance, males are typically expected to maximize their number of mating events, whereas an excessive number of mating events can be costly for females. Although the risk of sexual harassment by males and resulting costs for females are expected to increase with the proportion of males, it remains unknown whether and how parasitic distorters of a host population’s sex-ratio can shape this effect on the fitness of females. Here, we addressed this question using Armadillidium vulgare and its parasite Wolbachia that alters the sex-ratio of a population. We set up Wolbachia-free and Wolbachia-infected females in experimental groups exhibiting 100, 80, 50% or 20% females for 1 year, during which we measured changes in survival, fertility and fecundity.ResultsWolbachia infection shaped the effects of both population sex-ratio and reproductive season on female fecundity. Compared to Wolbachia-free females, Wolbachia-infected females were less likely to be gravid in populations exhibiting an excess of females and did not exhibit the otherwise negative effect of seasons on this likelihood. Group sex-ratio and Wolbachia infection have independent effects on other measured traits. Male-biased populations had females both exhibiting the lowest survival rate after 6 months and producing the smallest number of offspring, independent of Wolbachia infection. Conversely, Wolbachia-infected females had the lowest likelihood of producing at least one offspring, independent of group sex-ratio. Wolbachia infection had no effect on female survival rate.ConclusionsWe demonstrated that male-biased sex-ratio and the presence of Wolbachia are costly for females due to sexual harassment by males and bacterial infection, respectively. Interestingly, Wolbachia infection triggers another negative effect. This effect does not come from an excess of males and its associated sexual harassment of females but instead from a lack of males and the associated risk for females of remaining unmated. Overall, these findings highlight the importance of social pressures and infection on female fitness and provide insights into our general understanding of the joint and opposite effects of these two parameters in the evolution of reproductive strategies.
Highlights
In species that reproduce with sexual reproduction, males and females often have opposite strategies to maximize their own fitness
Harassment by males may have a direct impact on female fitness; for instance, in the bean weevil Callosobruchus maculatus, the genitalia of males have been shown to contain many sclerotized spines, damaging genitalia of females during copulation and increasing the mortality of females after multiple mating events [4]
Female survival rates Over the first 6 months of the experiment, the survival rate of females depended on the group sex-ratio (Fig. 1a; Likelihood Ratio (LR) χ23 = 40.74, P < 0.0001) but was independent of Wolbachia infection (Fig. 1b; LR χ21 = 1.76, P = 0.1849) and the interaction between group sex-ratio and Wolbachia infection (LR χ23 = 7.04, P = 0.071)
Summary
In species that reproduce with sexual reproduction, males and females often have opposite strategies to maximize their own fitness. The risk of sexual harassment by males and resulting costs for females are expected to increase with the proportion of males, it remains unknown whether and how parasitic distorters of a host population’s sex-ratio can shape this effect on the fitness of females. Because males and females typically differ in their investment in reproduction, sexual conflict is predicted to emerge in species with sexual reproduction [1] In this context, males often improve their fitness by maximizing the number of their sexual partners, whereas females do so by being selective toward the quality of their mate [2, 3]. Direct costs have been reported in the sea lion Phocarctos hookeri, where sexual harassment by males increases both female mortality and the associated costs of pup separation [8]
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