Abstract
Linking genotype to phenotype is a primary goal for understanding the genomic underpinnings of evolution. However, little work has explored whether patterns of linked genomic and phenotypic differentiation are congruent across natural study systems and traits. Here, we investigate such patterns with a meta‐analysis of studies examining population‐level differentiation at subsets of loci and traits putatively responding to divergent selection. We show that across the 31 studies (88 natural population‐level comparisons) we examined, there was a moderate (R 2 = 0.39) relationship between genomic differentiation (F ST) and phenotypic differentiation (PST ) for loci and traits putatively under selection. This quantitative relationship between P ST and F ST for loci under selection in diverse taxa provides broad context and cross‐system predictions for genomic and phenotypic adaptation by natural selection in natural populations. This context may eventually allow for more precise ideas of what constitutes “strong” differentiation, predictions about the effect size of loci, comparisons of taxa evolving in nonparallel ways, and more. On the other hand, links between P ST and F ST within studies were very weak, suggesting that much work remains in linking genomic differentiation to phenotypic differentiation at specific phenotypes. We suggest that linking genotypes to specific phenotypes can be improved by correlating genomic and phenotypic differentiation across a spectrum of diverging populations within a taxon and including wide coverage of both genomes and phenomes.
Highlights
Quantifying the relationship between genomic and phenomic (Box 1) population differentiation is fundamental to characterizing the genomic basis for phenotypic evolution (Rodríguez-Verdugo et al, 2017)
Recent technological advances have made sequencing large or whole portions of genomes possible for many nonmodel species (Bolger et al, 2019; Cuperus & Queitsch, 2020; Davey et al, 2011; Goodwin et al, 2016; Russell et al, 2017; Whibley et al, 2021), but are the patterns from these studies generalizable? does this growing body of literature support the premise that greater phenotypic differentiation corresponds with greater genomic differentiation in natural organisms? Here, we examine this link via standardized measures of genomic differentiation (FST) and phenotypic differentiation (PST)— while assessing potential interacting effects associated with different study designs (Box 2)
We address two main questions: How does genomic differentiation at loci under selection explain phenotypic differentiation, both across and within studies? Under ideal conditions, when all the loci underlying a phenotypic trait are identified and the phenotype is accurately quantified, we would expect a strong, positive relationship between PST and FST for loci under selection (Brommer, 2011; Kaeuffer et al, 2012; Raeymaekers et al, 2007)
Summary
Quantifying the relationship between genomic and phenomic (Box 1) population differentiation is fundamental to characterizing the genomic basis for phenotypic evolution (Rodríguez-Verdugo et al, 2017). Genome-wide association studies (GWAS) provide one avenue to explore genotype–phenotype relationships in natural populations, but are often plagued by high false-positive rates and commonly struggle to detect the small genetic effect sizes of many polygenic traits (Chen et al, 2021; Evangelou & Ioannidis, 2013). This growing body of studies has attempted to associate genomic and phenotypic aspects of adaptation in the same diverging populations of organisms. Common-rearing experiments may avoid some of these challenges by isolating genetic differences in phenotypes, but they remove gene-by-environment interactions, which are important genetically based sources of phenotypic variation (Via & Lande, 1985)
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