Abstract
Sexually antagonistic (SA) genetic variation—in which alleles favored in one sex are disfavored in the other—is predicted to be common and has been documented in several animal and plant populations, yet we currently know little about its pervasiveness among species or its population genetic basis. Recent applications of genomics in studies of SA genetic variation have highlighted considerable methodological challenges to the identification and characterization of SA genes, raising questions about the feasibility of genomic approaches for inferring SA selection. The related fields of local adaptation and statistical genomics have previously dealt with similar challenges, and lessons from these disciplines can therefore help overcome current difficulties in applying genomics to study SA genetic variation. Here, we integrate theoretical and analytical concepts from local adaptation and statistical genomics research—including F ST and F IS statistics, genome‐wide association studies, pedigree analyses, reciprocal transplant studies, and evolve‐and‐resequence experiments—to evaluate methods for identifying SA genes and genome‐wide signals of SA genetic variation. We begin by developing theoretical models for between‐sex F ST and F IS, including explicit null distributions for each statistic, and using them to critically evaluate putative multilocus signals of sex‐specific selection in previously published datasets. We then highlight new statistics that address some of the limitations of F ST and F IS, along with applications of more direct approaches for characterizing SA genetic variation, which incorporate explicit fitness measurements. We finish by presenting practical guidelines for the validation and evolutionary analysis of candidate SA genes and discussing promising empirical systems for future work.
Highlights
A population’s evolutionary capacity for adaptation hinges upon the nature and extent of the genetic variation it harbours (Fisher 1930)
“Sexually antagonistic” (SA) genetic variation—wherein alleles that are beneficial when expressed in one sex are harmful when expressed in the other—represents a common form of genetic trade-off (Rice and Chippindale 2001; Bonduriansky and Chenoweth 2009; Van Doorn 2009)
SA genetic variation arises from sex differences in selection (a.k.a., sex-specific selection) on traits that are genetically correlated between the sexes (Connallon and Clark 2014b), and may contribute substantially to fitness variation
Summary
A population’s evolutionary capacity for adaptation hinges upon the nature and extent of the genetic variation it harbours (Fisher 1930). Whereas the study of SA loci is still in its infancy, the fields of local adaptation and statistical genomics have already grappled intensively with many of the conceptual and methodological challenges that research on sex-specific selection faces (Hoban et al 2016; Visscher et al 2017). Lessons from local adaptation and statistical genomics research can sharpen hypothesis framing, guide statistical methodology, and inform best practices for disentangling signal, noise, and artefacts in studies of sex-specific selection. We evaluate several direct approaches for characterising sex-specific genetic variation for fitness, which combine elements from quantitative genetics, reciprocal transplant studies and experimental evolution These direct approaches have been extensively employed to study the genetic basis of locally adapted phenotypes and quantitative traits, but rarely to identify SA loci. We outline approaches that can support the biological validity of candidate genes and discuss best practices for the analysis and interpretation of their evolutionary histories
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