Population Size Mediates the Effects of Mating Systems on Evolutionary Rescue Under Worsening Environments

Animal mating systems are hugely diverse, ranging from species where mating is essentially random to those exhibiting complex systems of mate choice by one or both sexes, with some species mating monogamously and others showing various degrees of promiscuity. There is now good evidence that if male signal traits are correlated with fitness, then polygynous female choice systems can show improved adaptation and persistence, but there has been little exploration of the ways that other types of mating systems modulate adaptation and evolutionary rescue. To address this, we developed an individual-based model that allows random mating, female-only choice, and mutual mate choice to be compared within both monogamous and polygynous frameworks and used it to explore how mating systems influence adaptive response, loss of heterozygosity, and extinction risk under changing environmental conditions. We find that mating system interacts with population size in determining extinction risk: because mate choice under polygyny lowers effective population size, accelerating the loss of heterozygosity, small polygynous populations with either mutual or female-only mate choice face higher extinction risks than randomly mating populations. In larger populations where inbreeding and genetic drift are less important, female-choice and mutual-choice polygynous systems show the greatest resilience to environmental change by allowing better-adapted males to dominate reproduction. Random mating populations show the lowest resilience to environmental change when populations are large and mutual-choice monogamous systems have intermediate resilience. Among polygynous systems, female-only choice leads to slower loss of heterozygosity and facilitates population resilience better than mutual mate choice. These findings demonstrate that mating systems can critically shape a population’s ability to adapt to environmental change and alter extinction risks, emphasizing the need to consider mating systems in designing effective conservation strategies.