Male harm offsets the demographic benefits of good genes

Abstract

Sexual conflict can arise when males evolve traits that improve their mating success but in doing so harm females. By reducing female fitness, male harm can diminish offspring production in a population and even drive extinction. Current theory on harm is based on the assumption that an individual’s phenotype is solely determined by its genotype. But the expression of most sexually selected traits is also influenced by variation in biological condition (condition-dependent expression), such that individuals in better condition can express more extreme phenotypes. Here, we developed demographically explicit models of sexual conflict evolution where individuals vary in their condition. Because condition-dependent expression readily evolves for traits underlying sexual conflict, we show that conflict is more intense in populations where individuals are in better condition. Such intensified conflict reduces mean fitness and can thus generate a negative association between condition and population size. The impact of condition on demography is especially likely to be detrimental when the genetic basis of condition coevolves with sexual conflict. This occurs because sexual selection favors alleles that improve condition (the so-called good genes effect), producing feedback between condition and sexual conflict that drives the evolution of intense male harm. Our results indicate that in presence of male harm, the good genes effect in fact easily becomes detrimental to populations.

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).…”

Increased male-induced harm in response to female-limited selection: interactive effects between intra- and interlocus sexual conflict?

“…In laboratory mice, it has recently been shown that a male's diet affects seminal fluid immune-regulatory activity, leading to changes in inflammatory responses in the female reproductive tract [ 36 ]. If the amount and/or composition of the ejaculate of males from the divergent selection lines differ, either because they had more (H-line) or less (L-line) resources available during prenatal development or because ejaculate composition is genetically linked to female reproductive investment [ 21 , 37 , 38 ], then such effects could explain how selection on a female-limited trait can generate sexual conflict (see also [ 39 ]). Similarly, the foamy substance that is produced by the proctodeal gland of quail males and transferred to females during copulation has been shown to contain prostaglandins [ 40 ].…”

Why high-condition males might be bad news for females and populations

“…So far, these opposing effects of sexual selection have been discussed in relative isolation from each other, but in natural populations both processes are likely to both be present and the consequences for population persistence and extinction risk remain to be investigated. In this issue of PNAS, Flintham et al ( 16 ) explore the interactions between these two forces and integrate them in mathematical models explicitly linking sexual selection to population demography and extinction risk. Their elegant models reconcile the conflicting empirical and theoretical results on how sexual selection can affect population viability.…”

“…Thus, males in high condition can afford to invest more in to such mating-related traits, even though this might not necessarily benefit females and can sometimes even reduce female fitness through antagonistic mating interactions. ( D ) Simplified causal diagram of the new demographic model developed by Flintham et al in this issue of PNAS ( 16 ). Male and female conditions can be influenced by both the environment and genetic factors, and often that male and female conditions are phenotypically and/or genetically correlated with each other (as showed by positive “+”-sign and double-headed arrow).…”