Sexual selection can both increase and decrease extinction probability: reconciling demographic and evolutionary factors

Abstract

Summary1. Previous theoretical models of the effect of sexual selection on average individual fitness in a population have mostly predicted that sexually selected populations should adapt faster and clear deleterious mutations more quickly than populations where sexual selection is not operating. 2. While some laboratory studies have supported these predictions, others have not and studies of field systems have tended to find negative effects of sexual selection, or no effect. The negative effects of sexual selection found in field and other studies are usually ascribed to the costs associated with strong sexual selection acting on the population. 3. Here, using an individual-based model that allows feedback between demographic and evolutionary processes, we find that sexual selection can lead to both increases and decreases in population-level fitness measures such as extinction probability and adaptation rate. Whether fitness increases or decreases depends on a variety of environmental and demographic factors including the nature of environmental change, the carrying capacity of the environment, the average fecundity of the population in question and the strength of condition dependence. 4. In many cases, our model predicts that sexual selection leads to higher extinction probability in small populations because of an increased risk of demographic stochasticity, but lower extinction probability in larger populations because of faster adaptation rates. This is consistent with field studies that have mostly focussed on very small populations such as recently introduced birds, and tend to find negative effects, and also with laboratory studies that tend to use larger populations and have tended to find positive effects. 5. These findings go at least some way towards an understanding of the apparent contradictions between theoretical predictions, laboratory studies and field data.

Sexual selection predicts the persistence of populations within altered environments

“…introduced birds (McLain et al 1995(McLain et al , 1999Sorci et al 1998). It has been suggested that strong sexual selection could make small populations such as the ones addressed in these studies of birds particularly prone to extinction due to increased demographic stochasticity, whereas large populations would benefit from strong sexual selection (Mart ınez-Ruiz & Knell 2017), which is consistent with this study. Furthermore, generation time can influence the adaptive capacity of populations (Chevin et al 2010).…”

Male-benefit sexually antagonistic genotypes show elevated vulnerability to inbreeding

“…Whether strong sexual selection in males poses greater net benefits or detriments to population viability will depend on many interacting factors [6, 59]. Our findings add resolution to the role of SA genetic variation for fitness in determining that outcome.…”

“…Depending on the underlying mechanism (see above), this means that male-benefit SA genetic architecture, its phenotypic effects, or both pose an additional threat to population viability that has not yet been recognized. Further, in addition to selecting for female-detriment alleles that are sensitive to inbreeding depression, strong sexual selection in males should also decrease effective population size [22, 28, 59]. Thus, under certain conditions, sexual selection may set off an extinction vortex whereby these mechanisms reinforce one another.…”

Eco‐evolutionary dynamics of sexual selection and sexual conflict

“…What about classical selection through male–male competition or female choice? Here, the link between population performance measures and the intensity or direction of sexual selection is mixed (Martínez‐Ruiz & Knell, ). Sexual selection is expected to increase population fitness and local adaptation if females choose males that are in high genetic condition, that is: locally adapted males (Lorch et al, ; Rowe & Houle, ; Servedio, ).…”