Genomic signatures of high-altitude adaptation and chromosomal polymorphism in geladas

Kenneth L. Chiou, Mareike C. Janiak, India A. Schneider-Crease, Sharmi Sen, Ferehiwot Ayele, Idrissa S. Chuma, Sascha Knauf, Alemayehu Lemma, Anthony V. Signore, Anthony M. D’Ippolito, Belayneh Abebe, Abebaw Azanaw Haile, Fanuel Kebede, Peter J. Fashing, Nga Nguyen, Colleen McCann, Marlys L. Houck, Jeffrey D. Wall, Andrew S. Burrell, Christina M. BergeyJeffrey Rogers, Jane E. Phillips-Conroy, Clifford J. Jolly, Amanda D. Melin, Jay F. Storz, Amy Lu, Jacinta C. Beehner, Thore J. Bergman, Noah Snyder-Mackler

Research output: Contribution to journalArticlepeer-review

Abstract

Primates have adapted to numerous environments and lifestyles but very few species are native to high elevations. Here we investigated high-altitude adaptations in the gelada (Theropithecus gelada), a monkey endemic to the Ethiopian Plateau. We examined genome-wide variation in conjunction with measurements of haematological and morphological traits. Our new gelada reference genome is highly intact and assembled at chromosome-length levels. Unexpectedly, we identified a chromosomal polymorphism in geladas that could potentially contribute to reproductive barriers between populations. Compared with baboons at low altitude, we found that high-altitude geladas exhibit significantly expanded chest circumferences, potentially allowing for greater lung surface area for increased oxygen diffusion. We identified gelada-specific amino acid substitutions in the alpha-chain subunit of adult haemoglobin but found that gelada haemoglobin does not exhibit markedly altered oxygenation properties compared with lowland primates. We also found that geladas at high altitude do not exhibit elevated blood haemoglobin concentrations, in contrast to the normal acclimatization response to hypoxia in lowland primates. The absence of altitude-related polycythaemia suggests that geladas are able to sustain adequate tissue-oxygen delivery despite environmental hypoxia. Finally, we identified numerous genes and genomic regions exhibiting accelerated rates of evolution, as well as gene families exhibiting expansions in the gelada lineage, potentially reflecting altitude-related selection. Our findings lend insight into putative mechanisms of high-altitude adaptation while suggesting promising avenues for functional hypoxia research.

Original languageEnglish (US)
Pages (from-to)630-643
Number of pages14
JournalNature Ecology and Evolution
Volume6
Issue number5
DOIs
StatePublished - May 2022
Externally publishedYes

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Ecology

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