Abstract
BackgroundMitochondria play a key role in the balance of energy and heat production, and therefore the mitochondrial genome is under natural selection by environmental temperature and food availability, since starvation can generate more efficient coupling of energy production. However, selection over mitochondrial DNA (mtDNA) genes has usually been evaluated at the population level. We sequenced by NGS 12 mitogenomes and with four published genomes, assessed genetic variation in ten penguin species distributed from the equator to Antarctica. Signatures of selection of 13 mitochondrial protein-coding genes were evaluated by comparing among species within and among genera (Spheniscus, Pygoscelis, Eudyptula, Eudyptes and Aptenodytes). The genetic data were correlated with environmental data obtained through remote sensing (sea surface temperature [SST], chlorophyll levels [Chl] and a combination of SST and Chl [COM]) through the distribution of these species.ResultsWe identified the complete mtDNA genomes of several penguin species, including ND6 and 8 tRNAs on the light strand and 12 protein coding genes, 14 tRNAs and two rRNAs positioned on the heavy strand. The highest diversity was found in NADH dehydrogenase genes and the lowest in COX genes. The lowest evolutionary divergence among species was between Humboldt (Spheniscus humboldti) and Galapagos (S. mendiculus) penguins (0.004), while the highest was observed between little penguin (Eudyptula minor) and Adélie penguin (Pygoscelis adeliae) (0.097). We identified a signature of purifying selection (Ka/Ks < 1) across the mitochondrial genome, which is consistent with the hypothesis that purifying selection is constraining mitogenome evolution to maintain Oxidative phosphorylation (OXPHOS) proteins and functionality. Pairwise species maximum-likelihood analyses of selection at codon sites suggest positive selection has occurred on ATP8 (Fixed-Effects Likelihood, FEL) and ND4 (Single Likelihood Ancestral Counting, SLAC) in all penguins. In contrast, COX1 had a signature of strong negative selection. ND4 Ka/Ks ratios were highly correlated with SST (Mantel, p-value: 0.0001; GLM, p-value: 0.00001) and thus may be related to climate adaptation throughout penguin speciation.ConclusionsThese results identify mtDNA candidate genes under selection which could be involved in broad-scale adaptations of penguins to their environment. Such knowledge may be particularly useful for developing predictive models of how these species may respond to severe climatic changes in the future.
Highlights
Mitochondria play a key role in the balance of energy and heat production, and the mitochondrial genome is under natural selection by environmental temperature and food availability, since starvation can generate more efficient coupling of energy production
The Ka/Ks ratio patterns for ATP8 varied widely among genera and there was only weak or no evidence of a correlation between genetic diversity of ATP8 and measured environmental factors. These results identify mitochondrial DNA (mtDNA) candidate genes under selection which could be involved in broad-scale adaptations of penguins to their environment
Here, we identify mtDNA candidate genes under selection which could be involved in broad-scale adaptations of penguins to their environment
Summary
Mitochondria play a key role in the balance of energy and heat production, and the mitochondrial genome is under natural selection by environmental temperature and food availability, since starvation can generate more efficient coupling of energy production. The mitochondrial genome (mtDNA) is under continuous selection since the 13 protein-coding genes produce polypeptide products that work in association with nuclear-encoded subunits of protein complexes involved in oxidative phosphorylation (OXPHOS) [1]. Three types of hypotheses have been proposed to explain mitogenome evolution: 1) mitochondrial OXPHOS generates both energy and heat, and environmental temperature imposes a selective trade off between ATP production and heat [2,3,4,5,6]; 2) risk of starvation is associated with restricted food availability, since starvation can generate more efficient coupling of energy production by OXPHOS pathway [7,8,9,10]; 3) a more recent and debated hypothesis of immune response to pathogens [11,12,13,14,15]. It is possible that selection may operate among species in similar environments or it may drive adaptations in different genes
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