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Evolution of the Mitochondrial Genome in Mammals Living at High Altitude: New Insights from a Study of the Tribe Caprini (Bovidae, Antilopinae)

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Abstract

Organisms living at high altitude are exposed to severe environmental stress associated with decreased oxygen pressure, cold temperatures, increased levels of UV radiation, steep slopes, and scarce food supplies, which may have imposed important selective constraints on the evolution of the mitochondrial genome. Within mammals, the tribe Caprini is of particular interest for studying the evolutionary effects of life at high altitude, as most species live in mountain regions, where they developed morphological and physiological adaptations for climbing. In this report, we analyzed the complete mitochondrial genome of 24 ruminants, including 20 species of Caprini. The phylogenetic analyses based on 16,117 nucleotides suggested the existence of a new large clade, here named subtribe Caprina, containing all genera, but Pantholops (Pantholopina), Capricornis, Naemorhedus, and Ovibos (Ovibovina). The alignment of the control region showed that all Caprini have between two and four tandem repeats of ~75 bp in the RS2 region, and that several of these copies emerged from recent and independent duplication events. We proposed therefore that the maintenance of at least two RS2 repeats in the control region of Caprini is positively selected, probably for producing a higher number of D-loop strands 3′-ending at different locations. The analyses of base composition at third-codon positions of protein-coding genes revealed that Caprini have the highest percentage of A nucleotide and the lowest percentage of G nucleotide, a pattern which suggests increased rates of cytosine deamination (C→T transitions) on the H strand of mtDNA. Two nonexclusive hypotheses related to high-altitude life can explain such a mutational pattern: more severe oxidative stress (ROS) and higher metabolic rates. By comparing the relative rates of nonsynonymous and synonymous substitutions in protein-coding genes, we identified that Caprini have higher levels of adaptive variation in the ATPase complex. In addition, we detected several changes in mitochondrial genes that should be tested for their potential role in mountain adaptation.

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Acknowledgments

We are very grateful to the individuals who provided tissue samples: Alexis Lécu, Bruno Guffond, Céline Canler, Claire Rejaud, Françoise Hergueta-Claro, Géraldine Pothet, Gérard Dousseau, Jacob Mwanzia, Jacques Rigoulet, Jean-François Marjarie, Jean-Luc Berthier, Kevin Budsberg, Nhek Ratanapich, Nhim Thy, Nick Marx, Norin Chai, Perry S. Barboza, Samer Alasaad, Sheikh Zayed, Sir Bani Yas, Stéphane Ostrowski, Sylvie Laidebeure, and Vitaly Volobouev. This work was supported by the Muséum national d′Histoire naturelle (MNHN), CNRS, PPF ”Etat et structure phylogénétique de la biodiversité actuelle et fossile,” and “Consortium National de Recherche en Génomique.” It is part of agreement No. 2005/67 between the Genoscope and the MNHN on the project “Macrophylogeny of Life,” directed by Guillaume Lecointre.

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  1. Muséum national d’Histoire naturelle (MNHN), Département Systématique et Evolution, UMR 7205—Origine, Structure et Evolution de la Biodiversité, Case postale No. 51, 55 rue Buffon, 75005, Paris , France

    Alexandre Hassanin & Anne Ropiquet

  2. MNHN, Département Systématique et Evolution, Service de Systématique Moléculaire, Paris, France

    Alexandre Hassanin & Anne Ropiquet

  3. Genoscope, Centre National de Sequençage, 91057, Evry, France

    Arnaud Couloux & Corinne Cruaud

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  1. Alexandre Hassanin
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  2. Anne Ropiquet
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  4. Corinne Cruaud
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Correspondence to Alexandre Hassanin.

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Hassanin, A., Ropiquet, A., Couloux, A. et al. Evolution of the Mitochondrial Genome in Mammals Living at High Altitude: New Insights from a Study of the Tribe Caprini (Bovidae, Antilopinae). J Mol Evol 68, 293–310 (2009). https://doi.org/10.1007/s00239-009-9208-7

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