Heat stress reveals a fertility debt owing to postcopulatory sexual selection

Abstract

Climates are changing rapidly, demanding equally rapid adaptation of natural populations. Whether sexual selection can aid such adaptation is under debate; while sexual selection should promote adaptation when individuals with high mating success are also best adapted to their local surroundings, the expression of sexually selected traits can incur costs. Here we asked what the demographic consequences of such costs may be once climates change to become harsher and the strength of natural selection increases. We investigated how an evolutionary history of strong postcopulatory sexual selection (sperm competition) affects male fertility under acute adult heat stress. Harnessing the empirical potential of long-term experimental evolution in the seed beetle Callosobruchus maculatus, we assessed the thermal sensitivity of fertility (TSF) in replicated lines maintained for 68 generations under three alternative mating regimes manipulating the opportunity for sexual and natural selection. We find that males evolving under strong sexual selection suffer from increased TSF, and that male success in sperm competition (P2: sperm offense) is genetically correlated to increased TSF. Interestingly, females from the regime under strong sexual selection, who experienced relaxed selection on their own reproductive effort, had high fertility in benign settings but suffered increased TSF, like their brothers. This implies that female fertility and TSF evolved through genetic correlation with reproductive traits sexually selected in males. Paternal but not maternal heat stress reduced offspring fertility with no evidence for adaptive transgenerational plasticity among heat-exposed offspring, indicating that the observed effects may compound over generations. Our results suggest that trade-offs between fertility and traits increasing success in postcopulatory sexual selection can be revealed in harsh environments. This can put polyandrous species under increased risk during extreme heat waves expected under future climate change.

Environmental complexity mitigates the demographic impact of sexual selection

“…Given that these data may have been influenced by eggs laid by the offspring generation (see Methods ) these results should be interpreted with some caution. Nevertheless, taken at face value, they may suggest that environmental complexity mainly reduced the severity of male–male competition (which has been shown to impair fertility in previous studies of C. maculatus (Baur et al., 2023; Koppik et al., 2023)), and to lesser extent male harassment of females as stronger environmental effects on fecundity would have been expected in this scenario. Current research themes suggest that male fertility is particularly sensitive to heat (Parratt et al., 2021; Walsh et al., 2019), and our results could thus in part be driven by male–male competition exacerbating such effects (see also: (Moiron et al., 2022).…”

“…Long‐term evolutionary dynamics remain less certain and depend on how particular abiotic stressors affect the relative efficacy of purifying sexual selection on genetic quality and its role in evolutionary rescue (Pilakouta & Ålund, 2021; Rowe & Rundle, 2021; Svensson, 2019). Moreover, our exact application of the experimental heat wave itself, while grounded in both empirically measured heat tolerance of this species (Berger et al., 2021) and thermal records from the founding populations sampling location (Baur et al., 2023), will have affected results by targeting certain traits and behaviours more than others (Kellermann et al., 2019; Terblanche et al., 2007). Our findings should thus not be directly extrapolated to natural populations but rather be seen as an empirical proof‐of‐concept for the tenet that environmental complexity can mould the demographic impact of sexual selection and shift the balance of population‐level costs and benefits associated with sexual selection.…”

“…However, it has also evolved excessive expression of costly pre‐ and postcopulatory male traits (Bagchi et al., 2021; Baur et al., 2019; Baur & Berger, 2020; Koppik et al., 2023). For example, N + S males suffer reductions in fertility when reared together with other conspecific males (Baur et al., 2023), and N + S females have evolved immune responses as counteradaptations to the genital scaring caused by males during mating (Bagchi et al., 2021) (Figure 1b). We, therefore, predicted that N + S populations (relative to N populations) would be able to maintain higher potential growth rates and viability during the heatwave, due to their overall greater genetic quality and investment in reproduction.…”

“…The N + S regime has evolved increased fecundity and fertility, indicative of high genetic quality (Baur et al., 2023; Martinossi‐Allibert et al., 2019). However, it has also evolved excessive expression of costly pre‐ and postcopulatory male traits (Bagchi et al., 2021; Baur et al., 2019; Baur & Berger, 2020; Koppik et al., 2023).…”

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

“…There are at least two potentially simultaneously acting processes that may explain the difference in how P1 responded to social context in S and N males. First, male-male competition is very costly in C. maculatus [70] and potentially more intense in S males than in N males [7,71], which may have impaired P1 of S males under competition (see Discussion). Second, the presence of male competitors differentially shapes both sperm and ejaculate production in S versus N males [7], which may indicate changes to the post-copulatory strategy of competing S males.…”