Standing genetic variation as the predominant source for adaptation of a songbird

Abstract

What kind of genetic variation contributes the most to adaptation is a fundamental question in evolutionary biology. By resequencing genomes of 80 individuals, we inferred the origin of genomic variants associated with a complex adaptive syndrome involving multiple quantitative traits, namely, adaptation between high and low altitudes, in the vinous-throated parrotbill (Sinosuthora webbiana) in Taiwan. By comparing these variants with those in the Asian mainland population, we revealed standing variation in 24 noncoding genomic regions to be the predominant genetic source of adaptation. Parrotbills at both high and low altitudes exhibited signatures of recent selection, suggesting that not only the front but also the trailing edges of postglacial expanding populations could be subjected to environmental stresses. This study verifies and quantifies the importance of standing variation in adaptation in a cohort of genes, illustrating that the evolutionary potential of a population depends significantly on its preexisting genetic diversity. These findings provide important context for understanding adaptation and conservation of species in the Anthropocene.

Keywords: adaptation; population genomics; postglacial expansion; standing variation.

Fig. 1.

(A) The vinous-throated parrotbill and four sites (red dots) on an east–west section of central Taiwan at which vinous-throated parrotbills were sampled and (B) the distribution of the F_ST and ΔF_ST in the east and west high-/low-altitude local population pairs of each 10-kb nonoverlapping genomic window that was aligned with the published genome of the zebra finch. Red dots on top of and within each panel represent candidate regions on the genome (n = 24); red horizontal lines indicate the top 1% of F_ST and ΔF_ST. EH, high-altitude population east of CMR; EL, low-altitude population east of CMR; WH, high-altitude population west of CMR; WL, low-altitude population west of CMR.

Fig. 2.

(A) The proportion of polymorphic SNPs shared with the mainland population is significantly higher for candidate SNPs inferred in both high-and low-altitude population pairs than that of the entire genome and SNPs within 1 Mb downstream and upstream regions of all genes in the genome (within 1 mb) of the Taiwan population (East, east population pair; West, west population pair; Fisher’s exact test, candidate SNPs: P = 1.6 × 10⁻⁵ and P = 0.002 for the east and west high-/low-altitude population pairs, respectively; all of the SNPs within 1 Mb regions: P < 0.00001 for both east and west high-/low-altitude population pairs). (B) The minimum allele frequency (MAF) of candidate SNPs in the mainland population is significantly higher than that of noncandidate SNPs (Welch two-sample t test: t = −10.524, df = 63, P = 1.644 × 10⁻¹⁵). (C) The MAF of shared variants is significantly higher than private variants (Welch two-sample t test, t = −2,909.8, df = 19,750,000, P < 2.2e-16). PV, private variants; SV, shared variants.

Fig. 3.

The proportion of candidate SNPs that are fixed or nearly fixed (90% ≤ the major allele frequency < 100%) in the low- and high-altitude populations.