Parallel genomic responses to historical climate change and high elevation in East Asian songbirds

Yalin Cheng, Matthew J. Miller, Dezhi Zhang, Ying Xiong, Yan Hao, Chenxi Jia, Tianlong Cai, Shou Hsien Li, Ulf S. Johansson, Yang Liu, Yongbin Chang, Gang Song, Yanhua Qu, Fumin Lei*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

13 Citations (Scopus)

Abstract

Parallel evolution can be expected among closely related taxa exposed to similar selective pressures. However, parallelism is typically stronger at the phenotypic level, while genetic solutions to achieve these phenotypic similarities may differ. For polygenic traits, the availability of standing genetic variation (i.e., heterozygosity) may influence such genetic nonparallelism. Here, we examine the extent to which high-elevation adaptation is parallel—and whether the level of parallelism is affected by heterozygosity—by analyzing genomes of 19 Paridae species distributed across East Asia with a dramatic east–west elevation gradient. We find that western highlands endemic parids have consistently lower levels of heterozygosity—likely the result of late-Pleistocene demographic contraction—than do parids found exclusively in eastern lowlands, which remained unglaciated during the late Pleistocene. Three widespread species (east to west) have high levels of heterozygosity similar to that observed in eastern species, although their western populations are less variable than eastern ones. Comparing genomic responses to extreme environments of the Qinghai–Tibet Plateau, we find that the most differentiated genomic regions between each high-elevation taxon and its low-elevation relative are significantly enriched for genes potentially related to the oxygen transport cascade and/or thermogenesis. Despite no parallelism at particular genes, high similarity in gene function is found among comparisons. Furthermore, parallelism is not higher in more heterozygous widespread parids than in highland endemics. Thus, in East Asian parids, parallel functional response to extreme elevation appears to rely on different genes, with differences in heterozygosity having no effect on the degree of genetic parallelism.

Original languageEnglish
Article numbere2023918118
JournalProceedings of the National Academy of Sciences of the United States of America
Volume118
Issue number50
DOIs
Publication statusPublished - 2021 Dec 14

Keywords

  • Climate change
  • Demographic history
  • Genetic diversity
  • High-elevation adaptation
  • Parallel evolution

ASJC Scopus subject areas

  • General

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