Coevolution of female and male genital components to avoid genital size mismatches in sexually dimorphic spiders

Abstract

BackgroundIn most animal groups, it is unclear how body size variation relates to genital size differences between the sexes. While most morphological features tend to scale with total somatic size, this does not necessarily hold for genitalia because divergent evolution in somatic size between the sexes would cause genital size mismatches. Theory predicts that the interplay of female-biased sexual size dimorphism (SSD) and sexual genital size dimorphism (SGD) should adhere to the ‘positive genital divergence’, the ‘constant genital divergence’, or the ‘negative genital divergence’ model, but these models remain largely untested. We test their validity in the spider family Nephilidae known for the highest degrees of SSD among terrestrial animals.ResultsThrough comparative analyses of sex-specific somatic and genital sizes, we first demonstrate that 99 of the 351 pairs of traits are phylogenetically correlated. Through factor analyses we then group these traits for MCMCglmm analyses that test broader correlation patterns, and these reveal significant correlations in 10 out of the 36 pairwise comparisons. Both types of analyses agree that female somatic and internal genital sizes evolve independently. While sizes of non-intromittent male genital parts coevolve with male body size, the size of the intromittent male genital parts is independent of the male somatic size. Instead, male intromittent genital size coevolves with female (external and, in part, internal) genital size. All analyses also agree that SGD and SSD evolve independently.ConclusionsInternal dimensions of female genitalia evolve independently of female body size in nephilid spiders, and similarly, male intromittent genital size evolves independently of the male body size. The size of the male intromittent organ (the embolus) and the sizes of female internal and external genital components thus seem to respond to selection against genital size mismatches. In accord with these interpretations, we reject the validity of the existing theoretical models of genital and somatic size dimorphism in spiders.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0734-9) contains supplementary material, which is available to authorized users.

Intra‐specific variation of non‐genitalic and genitalic traits in two euophryine jumping spider species

“…It is intriguing that most of the genitalic traits examined in this study show negative (lower) allometric slopes yet high degree of dispersion around the allometric line (size‐corrected intra‐specific phenotypic variation). On the one hand, the negative allometry suggests that the genitalic traits may be decoupled with the body size (Dreyer & Shingleton, 2011), which is consistent with the finding in nephilid spiders that shows the female genitalia and male intromittent genital size evolve independently from the body size (Lupše, Cheng & Kuntner, 2016). Growing evidence suggests that genitalic morphology tends to show higher canalization (robustness to genetic or environmental perturbations) than mating signals and somatic traits (Rodríguez & Al‐Wathiqui, 2011), and are less sensitive to some factors generating size variation among individuals of a population such as environmental variation (plasticity) and genetic variation (Arnqvist & Thornhill, 1998; Fairbairn, 2005; Bertin & Fairbairn, 2007; Dreyer & Shingleton, 2011).…”

Rapid differentiation and asynchronous coevolution of male and female genitalia in stink bugs

“…What is common to such studies is that the genital traits in question are exclusively internal and intromittent. Because internal genitalia are directly associated with sperm transfer, reception and storage, it is intuitive that post‐mating sexual selection should be responsible for fast divergence in such cases (Polak & Rashed, ), whereas nonintromittent genitalia would be subject to other selective mechanisms (Lupše et al ., ). External and nonintromittent sexual characters have been previously suggested to be more evolutionarily constrained when they act to maintain a tight fit in copula (Eberhard, ).…”

Golden Orbweavers Ignore Biological Rules: Phylogenomic and Comparative Analyses Unravel a Complex Evolution of Sexual Size Dimorphism

“…Therefore, SSD is best considered as an epiphenomenon of potentially complex, taxon-specific, and evolutionary changes in the size of each gender. The ratio is plausibly selected only if the direct interaction of males and females of different sizes affects fitness (Ramos et al 2005; Lupše et al 2016). Spider size variation in each gender can be caused by multiple proximate causes (Kuntner and Elgar 2014; Kuntner and Cheng 2016).…”