Divergent and parallel routes of biochemical adaptation in high-altitude passerine birds from the Qinghai-Tibet Plateau

Xiaojia Zhu, Yuyan Guan, Anthony V. Signore, Chandrasekhar Natarajan, Shane G. DuBay, Yalin Cheng, Naijian Han, Gang Song, Yanhua Qu, Hideaki Moriyama, Federico G. Hoffmann, Angela Fago, Fumin Lei, Jay F. Storz

Research output: Contribution to journalArticle

22 Scopus citations


When different species experience similar selection pressures, the probability of evolving similar adaptive solutions may be influenced by legacies of evolutionary history, such as lineage-specific changes in genetic background. Here we test for adaptive convergence in hemoglobin (Hb) function among high-altitude passerine birds that are native to the Qinghai-Tibet Plateau, and we examine whether convergent increases in Hb–O2 affinity have a similar molecular basis in different species. We documented that high-altitude parid and aegithalid species from the Qinghai-Tibet Plateau have evolved derived increases in Hb–O2 affinity in comparison with their closest lowland relatives in East Asia. However, convergent increases in Hb–O2 affinity and convergence in underlying functional mechanisms were seldom attributable to the same amino acid substitutions in different species. Using ancestral protein resurrection and site-directed mutagenesis, we experimentally confirmed two cases in which parallel substitutions contributed to convergent increases in Hb–O2 affinity in codistributed high-altitude species. In one case involving the ground tit (Parus humilis) and gray-crested tit (Lophophanes dichrous), parallel amino acid replacements with affinity-enhancing effects were attributable to nonsynonymous substitutions at a CpG dinucleotide, suggesting a possible role for mutation bias in promoting recurrent changes at the same site. Overall, most altitude-related changes in Hb function were caused by divergent amino acid substitutions, and a select few were caused by parallel substitutions that produced similar phenotypic effects on the divergent genetic backgrounds of different species.

Original languageEnglish (US)
Pages (from-to)1865-1870
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Issue number8
StatePublished - Feb 20 2018


  • Biochemical adaptation
  • Convergence
  • Hemoglobin
  • Hypoxia
  • Mutation bias

ASJC Scopus subject areas

  • General

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