The mitochondrial genome of the mountain wooly tapir, Tapirus pinchaque and a formal test of the effect of altitude on the adaptive evolution of mitochondrial protein coding genes in odd-toed ungulates

Abstract

Background The harsh conditions of high-altitude environments are known to drive the evolution of physiological and morphological traits in endothermic animals. These conditions are expected to result in the adaptive evolution of protein coding genes encoded in mitochondrial genomes that are vital for the oxidative phosphorylation pathway. In this study, we formally tested for signatures of adaptive evolution on mitochondrial protein coding genes in Tapirus pinchaque and other odd-toed ungulates inhabiting high-elevation environments. Results The AT-rich mitochondrial genome of T. pinchaque is 16,750 bp long. A phylomitogenomic analysis supports the monophyly of the genus Tapirus and families in the Perissodactyla. The ratio of non-synonymous to synonymous substitutions demonstrated that all mitochondrial genes undergo purifying selection in T. pinchaque and other odd ungulates living at high elevations. Over this negative background selection, Branch Models suggested that cox3 and nad6 might be undergoing stronger purifying selection than other mitochondrial protein coding genes. Furthermore, Site Models suggested that one and four sites in nad2 and nad5, respectively, could be experiencing positive selection. However, these results were supported by Likelihood Ratio Tests but not Bayesian Empirical Bayes posterior probabilities. Additional analyses (in DataMonkey) indicated a relaxation of selection strength in nad6, evidence of episodic diversifying selection in cob, and revealed episodic positive/diversifying selection signatures for two sites in nad1, and one site each in nad2 and nad4. Conclusion The mitochondrial genome of T. pinchaque is an important genomic resource for conservation of this species and this study contributes to the understanding of adaptive evolution of mitochondrial protein coding genes in odd-toed ungulates inhabiting high-altitude environments.

Stronger evidence for relaxed selection than adaptive evolution in high-elevation animal mtDNA

“…However, relaxed selection on mtDNA should be explicitly tested in a phylogenetic framework, as some studies have begun to do (i.e. Gutiérrez et al, 2023).…”

“…In contrast to the nuclear genome, animal mtDNA lacks recombination, is uniparentally inherited, and is effectively haploid, making it more susceptible to genetic drift than nuclear loci according to classic theory (Lynch & Blanchard, 1998; Neiman & Taylor, 2009; but see Bazin et al 2006, Edwards et al, 2021). Formal tests that can disentangle positive from relaxed selection are now available (Wertheim et al, 2015) and can be used to investigate molecular patterns of adaptation related to altitude (e.g., Gutiérrez et al, 2023; Figure 1A ).…”

Mitochondrial genome structure and composition in 70 fishes: a key resource for fisheries management in the South Atlantic

“…Expanding geographic sampling and increasing sample size would not only enable the study of adaptation of Sardinella aurita to cold water, required to cross the Benguela barrier in southern Africa [83], but also complement the resources provided in this study. Furthermore, mitochondrial genomes have proven to be a valuable source for the study of adaptation genomics, particularly concerning metabolic responses [84][85][86].…”