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. Impact summaryFor species to persist in the face of climate change, adaptation needs to be fast enough to prevent extinction. If population decline is too abrupt, adaptation will be less likely to promote recovery, leading to extinction. Therefore, numerous studies have sought to determine how species can adapt and escape extinction. Sexual selection can promote genetic adaptation, but often has a by-product, sexual conflict, that promotes adaptations beneficial for one sex and detrimental to the other. Such is the case of male adaptations that increase male reproduction by harming females (male harm). Male harm is widespread and has been shown to decrease female and population productivity in some species, facilitating extinction. Furthermore, there is increasing evidence that the degree of male harm to females depends on environmental changes and how well males are adapted to them. However, we ignore how strong the effects of sexual conflict across taxa are, or how ecological feedback on sexual conflict may affect the rate of adaptation and population recovery. Here, we first conducted a meta-analysis to quantify the effect of male harm on female fitness and show, across taxa, that there is an overall negative effect that seems to be dependent on proxies of sexual selection. Then, we used a series of theoretical models to show that, although eco-evolutionary feedback on sexual conflict can limit population decline, this comes at the cost of slowing down the rate of adaptation and population recovery. Our study suggests that understanding how quick environmental changes affect sexual conflict can increase our understanding of how populations adapt and recover in the face of climate change.