Conflicting nuclear and mitogenome phylogenies reveal ancient mitochondrial replacement between two North American species of collared lemmings (Dicrostonyx groenlandicus, D. hudsonius)

Abstract

Collared lemmings (Dicrostonyx) are cold adapted rodents, keystone animals in the tundra communities and the model taxa in studies of Arctic genetic diversity and Quaternary paleontology. We examined mitochondrial and nuclear genomic variation to reconstruct phylogenetic relationships among the Eurasian D. torquatus and North American D. groenlandicus, D. hudsonius and evaluate biogeographic hypothesis of the two colonization events of North America from Eurasia based on morphological variation in dental traits. The nuclear and mitogenome phylogenies support reciprocal monophyly of each species but reveal conflicting relationships among species. The mitogenome tree likely reflects ancient mitochondrial replacement between currently isolated D. groenlandicus and D. hudsonius. The nuclear genome phylogeny reveals species cladogenesis and supports the hypothesis that D. hudsonius with primitive and distinct molar morphology represents a relic of the first migration event from Eurasia to North America. Species widely distributed in the North American Arctic, D. groenlandicus, with advanced dental morphology originated from a later colonization event across the Bering Land Bridge. This study shows ancient mitochondrial capture between two Arctic species and emphasizes the importance of multilocus approaches for phylogenetic inference.

Keywords: Arctic; Dicrostonyx; Introgression; Mitogenome; RAD-seq.

Fig. 1.

Species distributions, sampling locations and geographic ranges of the phylogeographic groups (Fig. 2, 3) in the Eurasian D. torquatus (Fedorov et al., 2020). The UPGMA species trees are based on Dxy distances, numbers on the branches are the mean distances between species.

Fig. 2.

The maximum credibility tree based on mitogenome sequences of collared lemmings. Stars indicate major nodes supported with posterior probability 1.

Fig. 3

The ML tree based on nucleotide distances across concatenated nuclear RAD loci. Stars indicate major nodes supported by the bootstrap test (> 95%)

Fig.4

The Treemix reconstruction based on allele frequencies of RAD loci. Arrow indicates 1 event of admixture in D. torquatus.