What can genome‐wide association studies tell us about the evolutionary forces maintaining genetic variation for quantitative traits?

Abstract

Contents 21I.21II.22III.24IV.25V.2930References30 Summary Understanding the evolutionary forces that shape genetic variation within species has long been a goal of evolutionary biology. Integrating data for the genetic architecture of traits from genome‐wide association mapping studies (GWAS) along with the development of new population genetic methods for identifying selection in sequence data may allow us to evaluate the roles of mutation–selection balance and balancing selection in shaping genetic variation at various scales. Here, we review the theoretical predictions for genetic architecture and additional signals of selection on genomic sequence for the loci that affect traits. Next, we review how plant GWAS have tested for the signatures of various selective scenarios. Limited evidence to date suggests that within‐population variation is maintained primarily by mutation–selection balance while variation across the landscape is the result of local adaptation. However, there are a number of inherent biases in these interpretations. We highlight these challenges and suggest ways forward to further understanding of the maintenance of variation.

Severe inbreeding depression is predicted by the “rare allele load” inMimulus guttatus*

“…; Josephs et al. ), which are the cause of ID under the dominance model. Allele frequencies should be intermediate with overdominance, and thus it is noteworthy that we found no evidence of heterozygote superiority at individual SNPs (Supporting Information Appendix 1).…”

“…In principle, sequencing allows direct evaluation of the models by attributing fitness effects to individual loci. Unfortunately, genome-wide association studies (GWAS) struggle to estimate the effects of rare alleles (Myles et al 2009;Josephs et al 2017), which are the cause of ID under the dominance model. Allele frequencies should be intermediate with overdominance, and thus it is noteworthy that we found no evidence of heterozygote superiority at individual SNPs (Supporting Information Appendix 1).…”

Genomic associations with bill length and disease reveal drift and selection across island bird populations

“…Combining trait mapping and genome scans is a particularly powerful approach, as it potentially allows us to simultaneously identify novel candidate traits under selection, determine the genetic basis of traits, and investigate how those traits have evolved over ecological and evolutionary timescales (Stinchcombe and Hoekstra ; Gagnaire and Gaggiotti ; Josephs et al. ). A number of studies have now combined top‐down and bottom‐up approaches to study adaptation in the wild (Nadeau et al.…”

“…Alternatively, using "bottom-up" (or genome-scanning) approaches, it is possible to statistically detect loci under divergent selection between populations, and to use this information to identify candidate phenotypes previously not known to be under selection (Turner et al 2010;Fumagalli et al 2015;Kardos et al 2015;Manel et al 2016). Combining trait mapping and genome scans is a particularly powerful approach, as it potentially allows us to simultaneously identify novel candidate traits under selection, determine the genetic basis of traits, and investigate how those traits have evolved over ecological and evolutionary timescales (Stinchcombe and Hoekstra 2008;Gagnaire and Gaggiotti 2016;Josephs et al 2017). A number of studies have now combined topdown and bottom-up approaches to study adaptation in the wild (Nadeau et al 2012;Gompert et al 2013;Johnston et al 2014;Brachi et al 2015;Bourgeois et al 2017), but few have been carried out in bottlenecked or isolated populations (Hohenlohe et al 2010).…”

Resequencing of massive pine genomes helps to unlock the genetic underpinning of quantitative traits in conifer trees

“…Conversely, expression variation of genes involved in xylem development was associated with SNPs occurring at intermediate frequency, a signature of balancing selection. This and other studies (Burgarella et al ., ; Lu et al ., ) show that balancing selection could be relatively common in conifers, as opposed to the few variants at intermediate frequency described in angiosperms (Josephs et al ., ).…”