Does selection occur at the intermediate zone of two insufficiently isolated populations? A whole-genome analysis along an altitudinal gradient

Abstract

\n Adaptive divergence would occur even between the insufficiently isolated populations when there is a great difference in the environments of their habitats. The individuals present in the intermediate zone of the two divergent populations are expected to have an admixed genetic structure due to gene flow. A selective pressure that acts on the genetically admixed individuals may limit the gene flow and promote the adaptive divergence. Here, we addressed a question whether the selection occurs in the genetically admixed individuals between the divergent populations and assessed its effects on the population divergence. We obtained the whole-genome sequences of a perennial montane plant, Arabidopsis halleri, which has clear phenotypic dimorphisms between altitudes, along an altitudinal gradient of 359–1,317 m with a high spatial resolution (mean altitudinal interval of 20 m). We found the zone where the highland and lowland genes were mixing. Using the FST approach, we found that 35 and 13 genes in the admixed zone had a high frequency of alleles that are accumulated in highland and lowland subpopulations, respectively, suggesting that these genes have been selected in the admixed zone. This selection might limit the gene flow and contribute to the adaptive divergence along the altitudes. In the single-nucleotide polymorphism (SNP)-based analysis, 3,000 out of 27,792 Altitude-Dependent SNPs had extremely high homozygosity in the admixed zone. In 84.7% of these SNPs, the frequency of homozygotes of highland alleles was comparable to that of lowland alleles, suggesting that these alleles are neutral but the heterozygotes were selectively eliminated. The distribution of highland and lowland alleles of these SNPs was not clearly separated between altitudes, implying that such selection did not impede the gene flow. We conclude that the selection occurring at the intermediate altitude affects the genetic structure in the admixed zone and adaptive divergence along the altitudes.