Male harm suppresses female fitness to affect the dynamics of adaptation and evolutionary rescue

Abstract

One of the most pressing questions we face as biologists is to understand how climate change will affect the evolutionary dynamics of natural populations and how these dynamics will in turn affect population recovery. Increasing evidence shows that sexual selection favours population viability and local adaptation. However, sexual selection can also foster sexual conflict and drive the evolution of male harm to females. Male harm is extraordinarily widespread and has the potential to suppress female fitness and compromise population growth, yet we currently ignore its net effects across taxa, or its effects on local adaptation and evolutionary rescue. We conducted a comparative meta-analysis to quantify the impact of male harm on female fitness and found an overall negative effect of male harm on female fitness. Negative effects seem to depend on proxies of sexual selection, increasing in species with larger sexual size dimorphism and strong sperm competition. We then developed theoretical models to explore how male harm affects adaptation and evolutionary rescue. We show that, when sexual conflict depends on local adaptation, population decline is reduced, but at the cost of slowing down genetic adaptation. This trade-off suggests that eco-evolutionary feedbacks on sexual conflict can act like a double-edge sword, reducing extinction risk by buffering the demographic costs of climate change, but delaying genetic adaptation. However, variation in the mating system and male harm type can mitigate this trade-off. Our work shows that male harm has widespread negative effects on female fitness and productivity, identifies potential mechanistic factors underlying variability in such costs across taxa, and underscores the importance of male harm on the demographic and evolutionary processes that impact how species adapt to environmental change.

Environmental complexity mitigates the demographic impact of sexual selection

“…Experimental evolution studies comparing populations evolving under monogamy and polygamy are a testament to the fact that these two effects often simultaneously impact population viability (Chenoweth et al., 2015; Whitlock & Agrawal, 2009) and the multivariate comparison of our experimental evolution lines confirms that evolution under sexual selection in C. maculatus follow these general predictions closely (Figure 1b). Recently, theoretical studies have highlighted the additional role of sexual selection in impacting population demography via costly sociosexual interactions arising from mating competition (Flintham et al., 2023; Gómez‐Llano et al., 2023; Martínez‐Ruiz & Knell, 2017). Such demographic impact is predicted to be particularly important when it coincides with episodes of rapid environmental change that necessitate evolutionary rescue (Martínez‐Ruiz & Knell, 2017; Svensson & Connallon, 2019).…”

“…Known examples of such male adaptations include harmful genitalia that scar females during mating (Stutt & Siva‐Jothy, 2001), or aggressive mate guarding to reassure paternity (Blum, 2012). Recent theoretical studies have shown that this type of sexual conflict could lead to increased extinction risk in already maladapted populations (Flintham et al., 2023; Gómez‐Llano et al., 2023; Martínez‐Ruiz & Knell, 2017). Moreover, as males of high genetic quality are likely to impose more harm to their female mates compared to males of low quality (Baur et al., 2022; Londoño‐Nieto et al., 2022; Yun et al., 2017), this effect could cancel out or even outweigh any potential population benefits of purifying sexual selection on male genetic quality (Chenoweth et al., 2015; Flintham et al., 2023).…”

Temperature drives the divergent evolution of male harm to females

“…Harmful male adaptations to females (male harm) are incredibly pervasive, diverse and sophisticated across the tree of life 8 . On the one hand, male harassment of females during pre-copulatory competition for mating has been documented in many vertebrate and invertebrate species 14 . On the other, post-copulatory competition has given rise to male harm adaptations that are similarly widespread and far more complex, ranging from toxic ejaculates 15 to adaptations for traumatic insemination that include seminal darts 16 , spiny penises and even genital ablation 17,18 .…”

“…Male harm thus drives antagonistic female-male co-evolution in a host of behavioural and morphological traits 8 , and may even act as an engine of speciation 19,20 . More importantly, male harm frequently leads to a "reproductive tragedy of the commons" where selection on male fitness impacts population demography by depressing net female productivity 14 , even to the point of facilitating extinction 21 . Recent theoretical models suggest that such negative effects may compound when harmful traits are linked to condition 22 , in which case good-genes selection can feed back to intensify male harm 23 and male harm can slow down evolutionary rescue 14 .…”

“…More importantly, male harm frequently leads to a "reproductive tragedy of the commons" where selection on male fitness impacts population demography by depressing net female productivity 14 , even to the point of facilitating extinction 21 . Recent theoretical models suggest that such negative effects may compound when harmful traits are linked to condition 22 , in which case good-genes selection can feed back to intensify male harm 23 and male harm can slow down evolutionary rescue 14 . In short, sexual selection acts as a doubleedge sword for populations because stronger condition-dependent selection on males, which allows for the demographically cheap purging of deleterious alleles, the genic capture of good genes, and ensuing fast adaptation, frequently turns out to be a recipe for intense sexual conflict.…”