Searching for signatures of positive selection in cytochrome b gene associated with subterranean lifestyle in fast-evolving arvicolines (Arvicolinae, Cricetidae, Rodentia)

Abstract

Background Mitochondrial genes encode proteins involved in oxidative phosphorylation. Variations in lifestyle and ecological niche can be directly reflected in metabolic performance. Subterranean rodents represent a good model for testing hypotheses on adaptive evolution driven by important ecological shifts. Voles and lemmings of the subfamily Arvicolinae (Rodentia: Cricetidae) provide a good example for studies of adaptive radiation. This is the youngest group within the order Rodentia showing the fastest rates of diversification, including the transition to the subterranean lifestyle in several phylogenetically independent lineages. Results We evaluated the signatures of selection in the mitochondrial cytochrome b (cytB) gene in 62 Arvicolinae species characterized by either subterranean or surface-dwelling lifestyle by assessing amino acid sequence variation, exploring the functional consequences of the observed variation in the tertiary protein structure, and estimating selection pressure. Our analysis revealed that: (1) three of the convergent amino acid substitutions were found among phylogenetically distant subterranean species and (2) these substitutions may have an influence on the protein complex structure, (3) cytB showed an increased ω and evidence of relaxed selection in subterranean lineages, relative to non-subterranean, and (4) eight protein domains possess increased nonsynonymous substitutions ratio in subterranean species. Conclusions Our study provides insights into the adaptive evolution of the cytochrome b gene in the Arvicolinae subfamily and its potential implications in the molecular mechanism of adaptation. We present a framework for future characterizations of the impact of specific mutations on the function, physiology, and interactions of the mtDNA-encoded proteins involved in oxidative phosphorylation.

Signatures of Adaptation in Mitochondrial Genomes of Palearctic Subterranean Voles (Arvicolinae, Rodentia)

“…The CYTB gene shows a significant difference in ω levels between subterranean and aboveground species and confirmed selection relaxation for Ellobius species and L. mandarinus . These results reproduce our earlier findings performed in the analysis of the CYTB alone and with a different set of compared species [ 34 ]. In addition to those previously reported, we have now detected positively selected sites for P. schaposchnikowi , Ellobius species, L. mandarinus, and H. fertilis .…”

“…Finally, Tomasco and Lessa [ 66 ] found increased values of ω in COX2 of subterranean coruros Spalacopus (almost 30×) and tuco-tucos Ctenomys (11×) relative to aboveground octodontoids. Our previous studies on the Arvicolinae subfamily also showed the relaxation of selection strength in CYTB reflecting an increased ratio (ω) in subterranean lineages compared to non-subterranean lineages [ 34 ]. Later, indicated changes were demonstrated for all mitochondrial protein-coding genes.…”

“…Phylogenetic reconstructions were carried out in MrBayes 3.2.2 [ 51 ] using either seven nuclear genes (6421 bp) (see methods in [ 34 ]) or 13 protein-coding mitochondrial genes (11,391 bp) in the case of H. fertilis (since nuclear genes are not available for this species). At this taxonomic level, the topology did not differ depending on nuclear or mitochondrial data on which the phylogenetic reconstruction was built.…”

“…It showed that habitat associated with the colonization of the subterranean niche, especially the transition from oxygen-rich to hypoxic atmospheres had led to the changes in the selective regimes of proteins involved in respiration. Our previous study [ 34 ] showed the relaxation of selection at the mitochondrial CYTB gene in Arvicolinae subterranean species by several computational approaches.…”

How voles adapt to subterranean lifestyle: Insights from RNA-seq

“…Moreover, the transition to the subterranean lifestyle within this subfamily occurred more than once. Our previous studies showed that selection pressure is relaxed at the mitochondrial CYTB gene in particular (Bondareva et al, 2021a), and in mitochondrial genomes for most subterranean Arvicolinae species (Bondareva et al, 2021b). The recent and phylogenetically independent transition of Arvicolinae voles to subterranean lifestyle makes it possible to trace adaptive events at a smaller evolutionary scale, in contrast to the analysis of classical ancient subterranean species such as Heterocephalus Rüppell, 1842, Nannospalax Palmer, 1903, and Fukomys Ogilby, 1838.…”