Increased male investment in sperm competition results in reduced maintenance of gametes

Abstract

Male animals often show higher mutation rates than their female conspecifics. A hypothesis for this male-bias is that competition over fertilization of female gametes leads to sexual selection for increased male germline replication at the expense of maintenance and repair, resulting in a trade-off between male success in sperm competition and offspring quality. Here we test this hypothesis using experimental evolution lines of the seed beetle Callosobruchus maculatus, maintained for >50 generations under three alternative mating regimes: natural and sexual selection (N+S-lines), natural selection only (N-lines) or sexual selection only (S-lines). Previous findings suggest that S-males reduce germline maintenance when engaging in reproduction compared to N- and N+S-males. Here, we first show that S-males are superior in sperm competition compared to both N- and N+S-males, suggesting that the removal of trade-offs between naturally and sexually selected male fitness components has resulted in the evolution of increased post-copulatory reproductive success. We then show that S-males produce progeny of lower quality if engaging in socio-sexual interactions with conspecifics prior to being challenged with a dose of irradiation introducing DNA-damage in their germline. We identify 18 candidate genes that showed differential expression in response to the induced germline damage. These genes also showed significant expression changes across socio-sexual treatments of fathers and predicted the reduction in quality of their offspring. Moreover, sex differences in expression of the same 18 genes indicate a substantially higher female investment in germline maintenance. Our findings provide evidence for a trade-off between male success in sperm competition and germline maintenance, suggesting that sex-differences in the relative strengths of sexual and natural selection are causally linked to male-mutation bias.

Heat stress reveals a fertility debt owing to postcopulatory sexual selection

“…5 in Baur & Berger 2020), and postcopulatory reproductive success in form of sperm defence (P1, i.e., the focal male is the first of two males to mate with the female) and sperm offense (P2, i.e., the focal male is second of two males to mate with the female), following 51 generations of experimental evolution (Fig. 1 in Koppik et al 2022). We then estimated genetic correlations between these traits and the fertility reduction induced by heat shock (i.e., the TSF) in the second mating, based on line means.…”

“…Previous studies have demonstrated that this genetic stock harbours substantial standing genetic variation for behaviour, life history and sexspecific reproductive success (Berger, Martinossi-Allibert, et al, 2016;Berger, You, et al, 2016;Grieshop et al, 2021;Grieshop & Arnqvist, 2018). The three experimental evolution regimes (outlined below) have been studied extensively and show divergence in a range of reproductive traits, including sex-specific competitive reproductive success (Martinossi-Allibert, Thilliez, et al, 2019), mating behaviour (Baur et al 2019), germline maintenance (Baur and Berger, 2020;, postcopulatory reproductive success (Koppik et al, 2022) and immunity (Bagchi et al, 2021). Three replicate lines were started per evolution regime, but one line was lost for the S regime prior to experiments.…”

“…Polyandrous species evolving in benign ancestral conditions, that devote most resources to reproductive effort and least to maintenance, are predicted to be most at risk (full blue line). Koppik et al, 2022), (c) sperm regeneration (measured as the number of sperm transferred in mating, 25 hours after sperm depletion; data from Baur & Berger, 2020), and also (d) female TSF. P1 and P2 were logit-transformed before analysis.…”

“…Previous work has shown that these regimes have evolved differences in a variety of reproductive phenotypes. For example, populations evolving under strong sexual selection and minimized natural selection show greater postcopulatory reproductive success (Koppik et al, 2022) and different sperm allocation patterns with more plastic germline maintenance (Baur & Berger, 2020). Hence, we predicted that these males would suffer increased thermal sensitivity of fertility (henceforth: TSF) compared to males that have evolved without sexual selection.…”

“…If such plasticity shifts resources away from germline maintenance in favour of investment in sperm competition, this could likewise reduce TSF under the trade-off scenario. Indeed, the studied evolution regimes of C. maculatus have previously been shown to differ in how socio-sexual interactions affect plastic changes in ejaculate traits and germline maintenance (Baur & Berger, 2020;Koppik et al, 2022). We therefore also explored the direct effects of the presence of male rivals on the plasticity of TSF across the three evolution regimes, predicting that such interactions would generally reduce male TSF.…”