Sperm competition and the evolution of testes size in terrestrial mammalian carnivores

Abstract

Summary 1.Understanding the factors influencing variation in the degree of sperm competition is a key question underlying the mechanisms driving sexual conflict. 2. Previous behavioural and comparative studies have indicated that carnivores appear to have evolved under sperm competition but an analysis of the predictors of the level of sperm competition is missing. 3. In this study, we use phylogenetic comparative methods to investigate life-history parameters predicted to affect the degree of sperm competition in terrestrial carnivores using variation in relative testes size (RTS, after controlling for body size allometry) as a measure of the level of sperm competition. Due to a paucity of consistent data across taxa, we used three measures of RTS: testes mass ( n = 40 species), testes and epididymes mass combined ( n = 38), and testes volume ( n = 48). We also created a derived data set ( n = 79) with testes mass estimated from regression analyses on the other measures of testes size. 4. Carnivores with shorter mating seasons had relatively larger testes, consistent with the hypothesis that sperm competition is greater when the degree of female oestrous synchrony is high. This relationship was stronger in spontaneous versus induced ovulators, suggesting higher sperm competition levels in spontaneous ovulators. This is the first comparative study to show this within mammalian taxa. Neither social mating system nor reproductive lifespan were significantly associated with variation in RTS and hence are poor predictors of sperm competition levels. 5. None of the above relationships were found to be significant for the testes and epididymes mass combined data set, but our understanding of the role of the epididymis in sperm competition is too limited to draw any conclusions. 6. Finally, we consistently found a significant phylogenetic signal in all analyses, indicating that phylogeny has played a significant role in the evolution of carnivore testes size and, therefore, in shaping levels of sperm competition. 7. Our results shed new light into the factors affecting levels of sperm competition in terrestrial carnivores by showing that the degree of oestrous synchrony and ovulation type interact to predict variation in RTS.

Sexual selection drives evolution and rapid turnover of male gene expression

“…Allometric scaling could affect relative expression levels of genes that are differentially expressed among subtissues in males and potentially contribute to the turnover in sex bias that we observe. If allometry was causing the pattern of turnover we observe, it might be expected to cause similarity in overall transcription between species with similar testis mass, as the phylogenetic signal for testis mass is lower than for many other traits (43)(44)(45). The strong phylogenetic signal that we observe in both hierarchical clustering (Fig.…”

Sexual selection explains more functional variation in the mammalian major histocompatibility complex than parasitism

“…Relative testes size (testes mass/ body mass) was used as a proxy for female promiscuity and opportunities for mate choice, as this measure has been shown to predict sexual selection and mating system across mammals (e.g. primates [27]; rodents [28]; carnivores [29]) and it is available for a large number of species. We compiled testes mass data and male body mass from the literature (see the electronic supplementary material, dataset S1).…”

“…and (iv) is there an association between parasite richness and degree of sexual selection, and how might this interaction shape the relationship with MHC polymorphism? We estimated the potential for sexual selection using relative testes size as a proxy for competition among males to produce offspring, as past work showed this measure is greater in species with promiscuous or polygynous (as opposed to monogamous) mating systems [27][28][29]. To infer selection pressures exerted by diverse parasite communities, we augmented existing data on parasites and pathogens (including viruses, bacteria, protozoa, helminths and arthropods) from free-living mammal populations [30][31][32].…”

Ovulation mode modifies paternity monopolization in mammals

“…However, induced ovulation occurs frequently in group-living species, suggesting this is unlikely to have driven its evolution. Induced ovulation decreases male intrasexual competition (Bakker & Baum 2000;Iossa et al 2008) and high levels of male competition may hinder female mate choice (Wong & Candolin 2005). Induced ovulation may have evolved as one way of decreasing male intrasexual competition, while at the same time acting as a post-copulatory selective mechanism, based on the level of stimulation (Larivière & Ferguson 2003).…”

“…To control for this, I included the male-female association pattern along with ovulation mode as variables in the alpha paternity model. For both models a phylogenetically corrected general linear model (PGLM; for details Iossa et al 2008) was used. Branch lengths were calculated from a mammalian phylogeny (Bininda-Emonds et al 2007; see the electronic supplementary material, appendix B), except for Papio cynocephalus which was missing; divergence time was taken to be the same as Papio hamadryas.…”