Evolutionary Consequences of Sex-Specific Selection in Variable Environments: Four Simple Models Reveal Diverse Evolutionary Outcomes

Abstract

The evolutionary trajectories of species with separate sexes depend on the effects of genetic variation on female and male traits as well as the direction and alignment of selection between the sexes. Classical theory has shown that evolution is equally responsive to selection on females and males, with natural selection increasing the product of the average relative fitness of each sex over time. This simple rule underlies several important predictions regarding the maintenance of genetic variation, the genetic basis of adaptation, and the dynamics of "sexually antagonistic" alleles. Nevertheless, theories of sex-specific selection overwhelmingly focus on evolution in constant environments, and it remains unclear whether they apply under changing conditions. We derived four simple models of sex-specific selection in variable environments and explored how conditions of population subdivision, the timing of dispersal, sex differences in dispersal, and the nature of environmental change mediate the evolutionary dynamics of sex-specific adaptation. We find that these dynamics are acutely sensitive to ecological, demographic, and life-history attributes that vary widely among species, with classical predictions breaking down in contexts of environmental heterogeneity. The evolutionary rules governing sex-specific adaptation may therefore differ between species, suggesting new avenues for research on the evolution of sexual dimorphism.

The interaction between sex-specific selection and local adaptation in species without separate sexes

“…Although interactions between sex-specific selection and environmental heterogeneity have received some attention in separate-sexed species (e.g. [30,91,92]), they have yet to be examined in hermaphrodites. To guide intuition and future research, we have developed a simple theoretical model of spatially variable sex-specific selection in hermaphrodites, emphasizing the effects of self-fertilization on the invasion of rare alleles and the maintenance of genetic variation.…”

“…Consequently, many of the unique population genetic features of hermaphrodites have received little attention in the context of local adaptation. In particular, it remains unclear how self-fertilization and spatially variable selection through both sex-functions jointly impact local adaptation and the maintenance of genetic variation, given that both sex-specific selection and environmental variation are thought to promote the maintenance of variation [7,8,22,25,29,30], while selfing is expected to constrain it [9,14,15,18,19]. This raises several important questions, on which we elaborate below: How does the hermaphrodite mating system influence opportunities for local adaptation through different fitness components?…”

A gene's-eye view of sexual antagonism

“…By considering in turn how different biological contexts may modulate fitness effects, reproductive values and relatedness, we can more easily generate new testable hypotheses about sexually antagonistic selection and intragenomic conflicts (some examples are given in table 1 ). While sexual antagonism and sex chromosome evolution have been historically well-studied topics [ 9 , 13 – 16 ], there remain significant gaps in theoretical understanding [ 49 – 52 ]. Here, we have shown how a gene's-eye--view approach may facilitate incorporation of salient aspects of real-world biology into future models, making them more empirically informative.…”

The search for sexually antagonistic genes: Practical insights from studies of local adaptation and statistical genomics

“…1977; Connallon and Chenoweth 2019), which can be influenced by spatial and temporally varying selection (Connallon et al. 2019), and effective population size (Connallon and Clark, 2012, 2014a; Mullon et al. 2012).…”