Long-term balancing selection contributes to adaptation in Arabidopsis and its relatives

Qiong Wu,Ya-Long Guo,Zi-Wen Li,Jia-Fu Chen,Ting-Shen Han,Yong-Chao Xu,Yu-Pan Zou,Xi Chen

doi:10.1186/s13059-017-1342-8

Abstract

BackgroundIn contrast to positive selection, which reduces genetic variation by fixing beneficial alleles, balancing selection maintains genetic variation within a population or species and plays crucial roles in adaptation in diverse organisms. However, which genes, genome-wide, are under balancing selection and the extent to which these genes are involved in adaptation are largely unknown.ResultsWe performed a genome-wide scan for genes under balancing selection across two plant species, Arabidopsis thaliana and its relative Capsella rubella, which diverged about 8 million generations ago. Among hundreds of genes with shared coding-region polymorphisms, we find evidence for long-term balancing selection in five genes: AT1G35220, AT2G16570, AT4G29360, AT5G38460, and AT5G44000. These genes are involved in the response to biotic and abiotic stress and other fundamental biochemical processes. More intriguingly, for these genes, we detected significant ecological diversification between the two haplotype groups, suggesting that balancing selection has been very important for adaptation.ConclusionsOur results indicate that beyond the well-known S-locus genes and resistance genes, many loci are under balancing selection. These genes are mostly correlated with resistance to stress or other fundamental functions and likely play a more important role in adaptation to diverse habitats than previously thought.

Highlights

In contrast to positive selection, which reduces genetic variation by fixing beneficial alleles, balancing selection maintains genetic variation within a population or species and plays crucial roles in adaptation in diverse organisms
In plants, beyond the well-known S-locus genes and R genes, many loci are under balancing selection
Shared polymorphisms are abundant between A. thaliana and C. rubella In a population of 80 A. thaliana accessions [25], there were 4,902,039 SNPs, among which 2,044,731 had a minor allele frequency (MAF) of > 0.05

Summary

Introduction

In contrast to positive selection, which reduces genetic variation by fixing beneficial alleles, balancing selection maintains genetic variation within a population or species and plays crucial roles in adaptation in diverse organisms. Which genes, genome-wide, are under balancing selection and the extent to which these genes are involved in adaptation are largely unknown. Balancing selection maintains advantageous genetic variation within a population [1,2,3,4,5,6] and has received long-term attention in evolutionary biology [7]. A novel gene involved in resistance to severe malaria was found in a region of Despite rapid progress in the understanding of balancing selection, confirmed cases are rather limited. A question naturally follows, namely, what other genes in the genome are under balancing selection? One convenient signature of ancient balancing selection is trans-species polymorphisms (TSPs) [2, 17], i.e. ancestral polymorphisms that arose before species diverged from a common ancestor, survived the split, and segregate in the present populations of different species

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