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Standing Genetic Variation As the Predominant Source for Adaptation of a Songbird

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Standing Genetic Variation As the Predominant Source for Adaptation of a Songbird Standing genetic variation as the predominant source for adaptation of a songbird Yu-Ting Laia, Carol K. L. Yeungb, Kevin E. Omlandc, Er-Li Pangd, Yu Haod, Ben-Yang Liaoe, Hui-Fen Caof, Bo-Wen Zhangd, Chia-Fen Yeha, Chih-Ming Hungg, Hsin-Yi Hunga, Ming-Yu Yangh, Wei Liangi, Yu-Cheng Hsuj, Cheng-Te Yaok, Lu Dongd, Kui Lind, and Shou-Hsien Lia,1 aSchool of Life Science, National Taiwan Normal University, 11677 Taipei, Taiwan; bNovogene Bioinformatics Institute, 100083 Beijing, People’s Republic of China; cDepartment of Biological Sciences, University of Maryland, Baltimore County, MD 21250; dMinistry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, 100875 Beijing, People’s Republic of China ; eInstitute of Population Health Sciences, National Health Research Institutes, Zhunan, 35053 Miaoli County, Taiwan; fInstitute of Genomics, School of Biomedical Sciences, Huaqiao University, 361021 Xiamen, People’s Republic of China ; gBiodiversity Research Center, Academia Sinica, 11529 Taipei, Taiwan; hSchool of Life Sciences, Peking University, 100080 Beijing, People’s Republic of China ; iMinistry of Education Key Laboratory for Ecology of Tropical Islands, College of Life Sciences, Hainan Normal University, 571158 Haikou, People’s Republic of China ; jDepartment of Natural Resources and Environmental Studies, National Dong Hwa University, 97401 Hualien, Taiwan; and kDivision of Zoology, Endemic Species Research Institute, 55244 Nantou, Taiwan Edited by Scott V. Edwards, Harvard University, Cambridge, MA, and approved December 17, 2018 (received for review August 7, 2018) What kind of genetic variation contributes the most to adaptation is suggests that it exhibits no seasonal altitudinal migration and a fundamental question in evolutionary biology. By resequencing may only range within 100 m in altitude (15). genomes of 80 individuals, we inferred the origin of genomic To evaluate the relative contribution of different sources of adap- variants associated with a complex adaptive syndrome involving tive genetic variants, we inferred the relative age of genetic variants multiple quantitative traits, namely, adaptation between high and across the entire genome. As a continental island, Taiwan was peri- low altitudes, in the vinous-throated parrotbill (Sinosuthora webbi- odically connected with the Asian mainland when land bridges sur- ana) in Taiwan. By comparing these variants with those in the Asian faced during the Pleistocene glacial periods (16), allowing Taiwan and mainland population, we revealed standing variation in 24 noncod- mainland populations to resume gene flow. Consequently, genetic ing genomic regions to be the predominant genetic source of variants shared by the two populations are likely to represent standing adaptation. Parrotbills at both high and low altitudes exhibited variation inherited from their most recent common ancestors. In signatures of recent selection, suggesting that not only the front contrast, new mutations which have arisen since the latest episode but also the trailing edges of postglacial expanding populations of gene flow would only be found in either one of the populations. could be subjected to environmental stresses. This study verifies Since the last glacial period, temperatures in Taiwan have and quantifies the importance of standing variation in adaptation risen by about 9.6 °C (17), likely driving species to shift or expand in a cohort of genes, illustrating that the evolutionary potential of a their ranges from lowland glacial refugia toward higher altitudes population depends significantly on its preexisting genetic diversity. (18, 19). While populations that expanded to higher altitudes These findings provide important context for understanding adap- faced challenges such as lower temperature and oxygen partial tation and conservation of species in the Anthropocene. pressure, those that remained in the lowlands would also have found themselves in a warmer environment, an aspect that has standing variation | population genomics | adaptation | been little investigated. Knowledge of how species adapted to postglacial expansion Significance daptation lies at the heart of Darwinian evolution. It re- quires the presence of advantageous alleles that are either A It is a tenet of modern biology that species adapt through nat- new mutations (1, 2) or preexisting standing variants (3, 4). ural selection to cope with the ever-changing environment. By Population genetic theory conventionally considers novel muta- comparing genetic variants between the island and mainland tions to be the genetic source of adaptation (1, 5), and their populations of a passerine, we inferred the related age of ge- significance has been highlighted in various empirical studies (6, netic variants across its entire genome and suggest that preex- 7). However, a high level of standing variation may allow a faster isting standing variants played the predominant role in local response to environmental changes than waiting for appropriate adaptation. Our findings not only resolve a long-standing fun- mutations to arise. Recent genomic studies also provide evidence damental problem in biology regarding the genetic sources of for the role of standing variation in adaptation (8, 9). Never- adaptation, but imply that the evolutionary potential of a pop- theless, the relative contribution of new mutations and standing ulation is highly associated with its preexisting genetic variation. variation to adaption has rarely been evaluated. This is funda- mental to the identification of the major driver underpinning this Author contributions: K.L. and S.-H.L. designed research; Y.-T.L., W.L., Y.-C.H., C.-T.Y., and critical evolutionary process and to the forecast of the fate of L.D. performed research; W.L., Y.-C.H., C.-T.Y., and L.D. contributed new reagents/analytic species in the Anthropocene, as the ability to adapt is central to tools; Y.-T.L., E.-L.P., Y.H., B.-Y.L., H.-F.C., B.-W.Z., C.-F.Y., C.-M.H., and M.-Y.Y. analyzed ’ data; and Y.-T.L., C.K.L.Y., K.E.O., B.-Y.L., B.-W.Z., C.-M.H., H.-Y.H., M.-Y.Y., and S.-H.L. species survival in changing environments (10). wrote the paper. Evaluating the relative contribution of standing and new ge- The authors declare no conflict of interest. netic variation to adaptation requires assessing a cohort of genes This article is a PNAS Direct Submission. that are under directional selection. Screening for the genetic This open access article is distributed under Creative Commons Attribution-NonCommercial- basis underlying a complex adaptive syndrome is likely to yield a NoDerivatives License 4.0 (CC BY-NC-ND). set of such genes. Here, we screened for genetic variants that Data deposition: The sequence reported in this paper has been deposited in the National underlie adaptation between high and low altitudes that likely Center for Biotechnology Information Sequence Read Archive (accession nos. SRX5087906 involves many quantitative traits (11) of the vinous-throated to SRX5087990; BioProject ID PRJNA504683). parrotbill (Sinosuthora webbiana), one of the most widely dis- 1To whom correspondence should be addressed. Email: [email protected]. tributed nonmigrant passerines in East Asia (12). In Taiwan, this This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. bird is found from sea level up to 3,100 m (13). Individual par- 1073/pnas.1813597116/-/DCSupplemental. rotbills only disperse within a limited distance (14). Field data Published online January 18, 2019. 2152–2157 | PNAS | February 5, 2019 | vol. 116 | no. 6 www.pnas.org/cgi/doi/10.1073/pnas.1813597116 Downloaded by guest on September 30, 2021 global warming in the past may help us understand the chal- Comparing with the reference genome, 20,017,403 polymorphic lenges they face in a continuously warming planet. sites (S) within the 40 resequenced genomes were found. The levels of intrapopulation genetic diversity are similar (π and mean indi- De Novo Assembly of a Draft Genome for the Parrotbill. We first vidual heterozygosity, H, SI Appendix,TablesS3andS5). However, sequenced and assembled de novo a reference genome of a male the number of polymorphic sites (S), a demographically sensitive Taiwanese vinous-throated parrotbill. The assembled genome, 1.06 index, is about 12% greater in the low-altitude (mean S = 11,329,479) Gb in length (genomic coverage = 110×, SI Appendix,TableS1), than in the high-altitude populations (mean S = 10,132,251). This is contains 6,508 scaffolds (2,034 scaffolds > 10 kb) with N50 size of consistent with the conjecture that populations at or near glacial 1.94 Mb. This draft genome includes a total of 72 Mb (6.8%) of refugia retain more stable and larger effective population sizes (Ne) repetitive sequences (SI Appendix,TableS2). We found 20,149 (hence more genetic variants) than populations at the expanding predicted genes, 9,581 of which could be functionally annotated. In edges during postglacial expansion (20, 21). total, we obtained 278 Mb of genes (26% of total genome) con- The population structure was revealed in an unrooted sisting of 253 Mb of introns and 25 Mb of coding regions. neighbor-joining population tree (SI Appendix, Fig. S3) based on genome-wide FST (fixation index, a genetic measurement of Genetic Variation and Geographic Structure of Parrotbills in Taiwan. population differential) values among all four populations (SI We resequenced the genomes of 40 parrotbill individuals that Appendix, Table S6), which indicates that pairs of populations on were collected from four populations (10 individuals per pop- the same side of the CMR are clustered together. Thus, the two ulation; Fig. 1A) with an average depth of 5.8× genome coverage population pairs can serve as independent samples for illustrat- (SI Appendix, Table S3). They formed two high- (>2,000 m) and ing parallel adaptation along altitudinal gradients (22). low- (<100 m) altitudinal comparison pairs, one from the east side of the Central Mountain Range (CMR) in Taiwan and one from Demographic History of the Vinous-Throated Parrotbill in Taiwan.
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