A Genome Scan for Genes Underlying Microgeographic-Scale Local Adaptation in a Wild Arabidopsis Species.

Shosei Kubota,Motomi Ito,Yutaka Suzuki,Shin-Ichi Morinaga,Kouki Hikosaka,Asao Fujiyama,Kousuke Hanada,Atsushi Toyoda,Takaya Iwasaki,Atsushi J Nagano,Sumio Sugano,Rodney Mauricio

doi:10.1371/journal.pgen.1005361

Abstract

Adaptive divergence at the microgeographic scale has been generally disregarded because high gene flow is expected to disrupt local adaptation. Yet, growing number of studies reporting adaptive divergence at a small spatial scale highlight the importance of this process in evolutionary biology. To investigate the genetic basis of microgeographic local adaptation, we conducted a genome-wide scan among sets of continuously distributed populations of Arabidopsis halleri subsp. gemmifera that show altitudinal phenotypic divergence despite gene flow. Genomic comparisons were independently conducted in two distinct mountains where similar highland ecotypes are observed, presumably as a result of convergent evolution. Here, we established a de novo reference genome and employed an individual-based resequencing for a total of 56 individuals. Among 527,225 reliable SNP loci, we focused on those showing a unidirectional allele frequency shift across altitudes. Statistical tests on the screened genes showed that our microgeographic population genomic approach successfully retrieve genes with functional annotations that are in line with the known phenotypic and environmental differences between altitudes. Furthermore, comparison between the two distinct mountains enabled us to screen out those genes that are neutral or adaptive only in either mountain, and identify the genes involved in the convergent evolution. Our study demonstrates that the genomic comparison among a set of genetically connected populations, instead of the commonly-performed comparison between two isolated populations, can also offer an effective screening for the genetic basis of local adaptation.

Highlights

Recent advances in next-generation sequencing (NGS) technologies have enabled a genomescale analysis to infer the phylogenetic history, demography, and selection of natural populations
Where does a local adaptation take place? In general, an adaptive divergence is predicted to occur between isolated populations because gene flow will erode and prevent the divergence
If an adaptive divergence is to be found within a small spatial scale, such case may favor the screening for the adaptive genes

Summary

Introduction

Recent advances in next-generation sequencing (NGS) technologies have enabled a genomescale analysis to infer the phylogenetic history, demography, and selection of natural populations. Ecological genomics has been applied to various study systems, screening methods to detect the selected loci can be represented by two approaches: those that focus on the adaptive differentiation, and those that focus on the genotype-environment correlations. The former differentiation-based approach assumes neutral genetic drift to affect the entire genome, so that unusual differentiation at a particular locus should indicate a presence of selection. FST-based outlier tests are among the earliest and most common method to detect the selected loci [2] The latter correlation-based approach compares a set of subpopulations at heterogeneous environments to detect the loci with correlation between allele frequency and environmental variables [3]. Complex demographic histories and entailing genetic structures are the major issues that challenge the genome-wide screening for adaptive genes, and a combination of different approaches is preferred to avoid false detections [6]

Methods

Results

Conclusion