Natural selection increases female fitness by reversing the exaggeration of a male sexually selected trait

Abstract

Theory shows how sexual selection can exaggerate male traits beyond naturally selected optima and also how natural selection can ultimately halt trait elaboration. Empirical evidence supports this theory, but to our knowledge, there have been no experimental evolution studies directly testing this logic, and little examination of possible associated effects on female fitness. Here we use experimental evolution of replicate populations of broad-horned flour beetles to test for effects of sex-specific predation on an exaggerated sexually selected male trait (the mandibles), while also testing for effects on female lifetime reproductive success. We find that populations subjected to male-specific predation evolve smaller sexually selected mandibles and this indirectly increases female fitness, seemingly through intersexual genetic correlations we document. Predation solely on females has no effects. Our findings support fundamental theory, but also reveal unforseen outcomes—the indirect effect on females—when natural selection targets sex-limited sexually selected characters.

Recurrent evolution of small body size and loss of the sword ornament in Northern Swordtail fish

“…Our whole-genome dataset allows us to address certain hypotheses about the genetic mechanisms underlying the recurrent evolution of small, unornamented males in Xiphophorus. Introgression has been shown to underlie patterns of recurrent phenotypic evolution in other species groups (Heliconius Genome, 2012;Jones et al, 2018;Oziolor et al, 2019), and past work has underscored the frequency of hybridization in Xiphophorus (Cui et al, 2013). We reexamined patterns of gene flow in Northern swordtails using our whole-genome dataset, and recapitulate several patterns of genetic exchange found by previous studies (Cui et al, 2013;Schumer et al, 2016).…”

Genomic evidence that a sexually selected trait captures genome-wide variation and facilitates the purging of genetic load

“…That we do not observe an overall increase in female fecundity in F-lines may be reconciled if the benefits of purging deleterious mutations are counteracted by an increase in the strength of intra-locus sexual conflict (IASC) occurring between females and males with greatest expression of SST [39][40][41] . This increased strength of IASC has previously been described in R. robini inbred lines founded by fighters or scramblers 67 and within populations selected for each male morph 39 , in which females derived from fighter treatments had decreased fitness compared to those from scrambler treatments.…”

“…These genome-wide purifying effects of sexual selection may bolster population resilience to environmental and genetic stress as some empirical work has found 45,[78][79][80][81][82][83] (also see refs. 50,55,56,[84][85][86][87] for counter examples), but our phenotypic data show that despite purging, population fitness does not necessarily improve under benign environmental conditions, possibly due to sexually antagonistic effects associated with SST evolution [39][40][41]67 . While such effects were proposed to promote balancing selection, thus possibly helping to maintain potentially adaptive genetic variance, we have not found support for signals of balancing selection associated with weapon evolution.…”

“…In opposition, recent theory has highlighted that sexual selection may promote balancing selection 30 , due to negative pleiotropic effects of SSTs on other components of fitness 31,32 or due to sexual antagonism [33][34][35] caused by differences between the sexes in the direction of selection on shared traits, a common consequence of sexual selection 36 . In species with ARPs, the scope for balancing selection may be further increased by alleles being selected in opposing directions between ARPs 37,38 or if sexual antagonism is stronger between males expressing SSTs and females [39][40][41] . Therefore, by increasing the scope for antagonistic selection, sexual selection may augment the amount of genetic variance segregating in natural populations 42,43 .…”

The stagnation paradox: the ever-improving but (more or less) stationary population fitness

“…There are numerous examinations of how sexual selection and sexual conflict relate to growth or stability, resilience against extinction via inbreeding, or other proxies of population fitness (review: [69], newer work: [59][60][61][62][63][64][65][70][71][72][73][74]). To make sense of the diverse mess, systematic approaches appear welcome.…”