A mitochondrial genome phylogeny of voles and lemmings (Rodentia: Arvicolinae): Evolutionary and taxonomic implications

Abstract

Arvicolinae is one of the most impressive placental radiations with over 150 extant and numerous extinct species that emerged since the Miocene in the Northern Hemisphere. The phylogeny of Arvicolinae has been studied intensively for several decades using morphological and genetic methods. Here, we sequenced 30 new mitochondrial genomes to better understand the evolutionary relationships among the major tribes and genera within the subfamily. The phylogenetic and molecular dating analyses based on 11,391 bp concatenated alignment of protein-coding mitochondrial genes confirmed the monophyly of the subfamily. While Bayesian analysis provided a high resolution across the entire tree, Maximum Likelihood tree reconstruction showed weak support for the ordering of divergence and interrelationships of tribal level taxa within the most ancient radiation. Both the interrelationships among tribes Lagurini, Ellobiusini and Arvicolini, comprising the largest radiation and the position of the genus Dinaromys within it also remained unresolved. For the first time complex relationships between genus level taxa within the species-rich tribe Arvicolini received full resolution. Particularly Lemmiscus was robustly placed as sister to the snow voles Chionomys in the tribe Arvicolini in contrast with a long-held belief of its affinity with Lagurini. Molecular dating of the origin of Arvicolinae and early divergences obtained from the mitogenome data were consistent with fossil records. The mtDNA estimates for putative ancestors of the most genera within Arvicolini appeared to be much older than it was previously proposed in paleontological studies.

Fig 1. Base composition in mitochondrial PCG of Arvicolinae.

The frequency of the four bases (A, C, G, and T) at each codon position (first, second and third) in concatenated alignment was used as 12 variables for PCA. Tribes are indicated by colours. Species names are given only for taxa that differ in their nucleotide composition. Details with percentages for each position are given in S6 Table.

Fig 2. Time-calibrated mitochondrial phylogeny of Arvicolinae.

Node labels display the following supports: BI complete / BI RY-coded 3rd codon position / ML complete / ML RY-coded 3rd codon position. Black circles show nodes with 0.95–1.0 BI and 95–100 ML support. All letters at nodes correspond to fossil constraints in S3 Table. Traditional tribal designations are also given above the branches and corresponding branches distinguished by different colors.