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

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

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. [Abstract copyright: © 2022. The Author(s), under exclusive licence to Springer Nature Limited.]

Citation

Chiou, K. L., Janiak, M., Schneider-Crease, I. A., Sen, S., Ayele, F., Chuma, I. S., …Snyder-Mackler, N. (2022). Genomic signatures of high-altitude adaptation and chromosomal polymorphism in geladas. Nature Ecology and Evolution, 6, 630-643. https://doi.org/10.1038/s41559-022-01703-4

• Journal Article Type: Article
• Acceptance Date: Feb 15, 2022
• Publication Date: Mar 24, 2022
• Deposit Date: May 9, 2022
• Publicly Available Date: May 12, 2022
• Journal: Nature ecology & evolution
• Print ISSN: 2397-334X
• Publisher: Nature Research
• Volume: 6
• Pages: 630-643
• DOI: https://doi.org/10.1038/s41559-022-01703-4
• Publisher URL: https://doi.org/10.1038/s41559-022-01703-4
• Related Public URLs: https://www.nature.com/articles/s41559-022-01703-4
• Additional Information: Funders : Deutsche Forschungsgemeinschaft (German Research Foundation);National Science Foundation (NSF);U.S. Department of Health & Human Services | NIH | National Heart, Lung, and Blood Institute (NHLBI); Projects : DFG KN1097/3-1;1736249;2114465;1723228;1255974;0715179;1848900;2013888;1723237;2010309;R01HL087216