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

Male harm offsets the demographic benefits of good genes. Ewan O. Flintham, Vincent Savolainen, and Charles Mullon. Proceedings of the National Academy of Sciences, March 2, 2023, 120 (10) e2211668120. https://doi.org/10.1073/pnas.2211668120

Significance: Organisms vary in their biological condition. Those individuals in better condition show improved survival or fecundity, and so populations composed of such individuals should be more viable. However, high-condition individuals also express larger sexually selected phenotypes, some of which, in males, can harm females. The good genes hypothesis posits that sexual selection on condition-dependent traits indirectly increases mean condition and therefore population health. Here, using mathematical models, we show that this effect should rarely be expected when sexual traits cause harm: Instead, good genes selection leads to larger harming traits, reduced female fecundity, and potential population crashes.

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.

Discussion

Here, we have integrated key aspects from two groups of models: i) sexual conflict (e.g., refs. 18, 22–24, 27, 29) and ii) condition dependence (e.g., handicap models, 40–42, 48). In doing so, we have uncovered some surprising insights into how sexual selection shapes trait evolution and population demography.

Our analyses indicate that, like other sexually selected traits (30, 41, 42), male harm and female tolerance readily evolve condition dependence such that male and female investment into sexual conflict increases with condition. Populations in better condition thus experience more intense conflict, which impairs offspring recruitment and can jeopardize population persistence. In particular, if the severity of male harm increases more strongly with condition than does baseline female fecundity, we observe a counter-intuitive pattern whereby high mean condition is associated with low mean fitness. Such a negative association between condition and fitness is especially likely to emerge where condition has a genetic basis in males and females, as selection favors “good genes” that improve individual condition but also increase the intensity of male harm.

Our results contrast with the common view that sexual selection on good genes also improves mean fitness (43, 55, 65, 66) and mitigates the costs of sexual conflict (42). This is because for the good genes effect to work, that is, for sexual selection to increase mean condition, sexual traits must show appreciable condition-sensitivity (e.g. large κz in our model). In other words, sexual selection acts strongly on condition when good genes confer large increases in the size of sexual traits that males can afford to express. Therefore, the good genes effect is strong where a reduction in mutation load is associated with a significant increase in male sexual trait expression (e.g. in Figure 3A when κz = 1, an increase in condition, green points, is associated with a much larger increase in male trait size, blue points, see also figure 1a in (42)). Importantly, the repercussions of the good genes effect for male trait size are typically larger than for baseline female fecundity. This is because if condition genes greatly improve absolute baseline survival or fecundity, then natural selection should be intense enough to maintain them at relatively high frequency irrespective of the action of sexual selection (Figure 3C see difference between orange curves and black curve decreases with κα). The variation in genetic condition that is available for sexual selection to act upon is therefore limited, constraining the influence of the good genes effect on female fecundity relative to male trait expression. Altogether this means that, when male traits beget harm, the good genes effect has much greater scope to influence demography through sexual conflict than through baseline female fitness. Population benefits of good genes are thus easily reversed by their side-effect in exacerbating antagonistic male-female interactions.

In highlighting the relationship between condition and male harm, our results have implications for empirical work, in particular experimental evolution approaches to unpicking the consequences of sexual selection. Some studies have identified population-level benefits of sexual selection by tracking variation in condition (inferred through condition-correlated traits, e.g., body size, male mating success, offspring viability, or immune function) as a proxy of population viability (e.g., refs. 67–70 reviewed in ref. 71). Our results indicate such traits are poor indicators of population viability in species exhibiting male harm. Without measuring mean fitness, these studies therefore provide ambiguous evidence for an advantage to sexual selection. Indeed, when experimental studies do track more direct measures of mean fitness (such as female fecundity), they typically detect a weaker increase than for indirect measures such as body condition, mutation frequencies, or male mating success (71, 72). For example, a study in fruit flies found that sexual selection was associated with lower mutation load but also diminished offspring recruitment, which was attributed to the effects sexual conflict (73). Furthermore, a number of experimental studies have found evidence that sexual selection improves persistence in populations experiencing environmental stress (e.g., temperature variation in refs. 74–76, reviewed in refs. 77 and 43). This has been attributed to the idea that sexual and natural selection should be more closely aligned in such cases, i.e., that condition genes are more likely to benefit both sexual and nonsexual fitness when both sexes are poorly adapted (78–80). However, our analyses provide an additional explanation here: Environmental stress, by lowering male condition, may reduce the expression of male harm and so increase mean female fitness. More generally, we suggest that condition dependence provides a mechanism for the strength of sexual conflict to diverge in different environments a pattern, for example, observed in drosophila (81), and water striders (82).

To produce tractable results, our baseline model makes a number of simplifying assumptions. We assumed a well-mixed population (i.e., no effects of spatial subdivision); the absence of genetic constraints that affect condition- or sex-specific phenotypic expression; that males direct their mating attention indiscriminately toward high- and low-condition females; and that females express a tolerance trait that mitigates harm but does not impact male mating success. Relaxing these assumptions may alter the ecoevolutionary dynamics of sexual conflict through kin selection (27, 29), the strength of natural selection on females (70, 83), and the presence of coevolutionary intersexual arms races that escalate sexual conflict (24, 28, 84). Moreover, we considered two forms of condition variation, with condition either 1) a purely environmental trait or 2) purely genetic, while in nature, condition may frequently be an intermediate of these two scenarios (46). To relax some of these assumptions, in SI Appendix, Appendices C and D we also analyzed extended versions of our baseline model that allowed us to consider alternative bases of condition and multiple ecological settings for sexual conflict. In certain cases, such as where condition-dependent plasticity is prevented by genetic constraints, or where genotype × environment interactions depress male condition, we find that male harm can be diminished, so aiding population persistence (SI Appendix, Appendix D). However, our main results remain robust, that is, sexual conflict generates a negative relationship between average condition (e.g., good genes) and population size in the vast majority of the cases considered. In fact, we find that the costs of condition-dependent harm for population persistence may be strongly exacerbated in many common scenarios of sexual conflict, such as where female resistance drives evolutionary arms races, or where male and female conditions are encoded by different genes. We therefore suggest that the effects of condition variation found in our model will be general features found across most forms of sexual conflict (SI Appendix, Appendix D for a deeper discussion of extensions to our baseline model and of modeling choice and implications).

Finally, while our study was presented in the context of sexual conflict, our results are also more broadly applicable to the evolution of competitive traits with demographic effects. For example, antagonistic social interactions commonly drive the evolution of weapon phenotypes in both sexes (85, 86). These traits, which are often condition dependent, can influence the survival of interacting conspecifics (12, 13, 20, 33, 87, 88), and so their expression may also diminish mean fitness in high-condition populations.