Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

Abstract

Background Sexual dimorphism in immunity is believed to reflect sex differences in reproductive strategies and trade-offs between competing life history demands. Sexual selection can have major effects on mating rates and sex-specific costs of mating and may thereby influence sex differences in immunity as well as associated host–pathogen dynamics. Yet, experimental evidence linking the mating system to evolved sexual dimorphism in immunity are scarce and the direct effects of mating rate on immunity are not well established. Here, we use transcriptomic analyses, experimental evolution and phylogenetic comparative methods to study the association between the mating system and sexual dimorphism in immunity in seed beetles, where mating causes internal injuries in females. Results We demonstrate that female phenoloxidase (PO) activity, involved in wound healing and defence against parasitic infections, is elevated relative to males. This difference is accompanied by concomitant sex differences in the expression of genes in the prophenoloxidase activating cascade. We document substantial phenotypic plasticity in female PO activity in response to mating and show that experimental evolution under enforced monogamy (resulting in low remating rates and reduced sexual conflict relative to natural polygamy) rapidly decreases female (but not male) PO activity. Moreover, monogamous females had evolved increased tolerance to bacterial infection unrelated to mating, implying that female responses to costly mating may trade off with other aspects of immune defence, an hypothesis which broadly accords with the documented sex differences in gene expression. Finally, female (but not male) PO activity shows correlated evolution with the perceived harmfulness of male genitalia across 12 species of seed beetles, suggesting that sexual conflict has a significant influence on sexual dimorphisms in immunity in this group of insects. Conclusions Our study provides insights into the links between sexual conflict and sexual dimorphism in immunity and suggests that selection pressures moulded by mating interactions can lead to a sex-specific mosaic of immune responses with important implications for host–pathogen dynamics in sexually reproducing organisms.

Direct and indirect effects of male genital elaboration in female seed beetles

“…This shared life-history trade-off scenario is supported by the positive direct effects of L males on female fecundity and by the negative genetic correlation between body size and spine length in males, but less so by the positive genetic correlation between female body size and male spine length (electronic supplementary material). It is also consistent with the fact that primary sexual traits in males and females show correlated evolution across Callosobruchus species [62] and comparative data suggest trade-offs between investment in primary sexual traits and other competing life-history demands, such as immunity [28], in this genus [55]. Irrespective of the underlying genetic mechanism, however, our results show that genetic variation associated with spine length in males is positively related to genetic variation in female lifetime offspring production, under the conditions in which our assays were performed.…”

“…First, our phenotypic engineering experiment confirmed that shortening of these male-benefit spines has a direct positive effect on female fitness, previously only inferred from comparative studies [ 26 , 27 ]. Previous work has demonstrated that the spines cause injuries to the female reproductive tract [ 24 , 25 , 37 ] and induce an immune response in females [ 27 , 28 , 42 ]. Genital spine length in males is correlated with female reproductive tract morphology across populations [ 27 ] and species [ 26 ], where an evolutionary thickening of the reproductive tract is associated with longer spines.…”

“…One of the most dramatic examples of an antagonistic trait, where both experimental studies and comparative studies of sexually antagonistic coevolution have been undertaken, is the remarkable spiny genitalia of seed beetles (figure 1a, inset). These genital spines cause significant internal injuries in the reproductive tract of females [24,25] and in response females have evolved a thickened reproductive tract, a very pronounced immune response and an efficient wound healing to cope with internal injuries [26][27][28]. Elaboration of the spines can be substantial [26] and it is possible that they have evolved to be costly in males and hence also reflect some aspect of male genetic quality.…”

The mating system affects the temperature sensitivity of male and female fertility

“…C. maculatus has a polyandrous mating system with documented sexual conflict over (re)mating and high remating rates, leading to both pre-and post-copulatory sexual selection on males Crudgington & Siva-Jothy, 2000;Eady, 1995;Gay et al, 2009;Hotzy & Arnqvist, 2009). Once a male manages to successfully initiate copulation, spines on its genitalia help to prevent it from being dislodged but at the same time harm the female (Bagchi et al, 2021;Edvardsson & Tregenza, 2005;Rönn et al, 2007;Rönn & Hotzy, 2012). The effects of the genital spines and the harm imposed on the females have been found to correlate with a male's sperm competitiveness (Hotzy & Arnqvist, 2009) and, in a congener that exhibits similar genital structures, also increase female oviposition rate as a response to genital scarring (Haren et al, 2017).…”

“…The selection regime protocols (Fig. 1a), outlined below, have previously been described and used in several, more long-term (up to 60 generations), experimental evolution studies in C. maculatus and have been shown to result in pronounced sex-specific adaptations (Bagchi et al, 2021;Baur et al, 2019;Baur & Berger, 2020;.…”