The importance of ice ages in diversification of arctic collared lemmings (Dicrostonyx): evidence from the mitochondrial cytochrome b region

Variation in the nucleotide sequence of the mitochondrial cytochrome b region (804 bp) was examined for 24 individuals of collared lemmings Dicrostonyx sampled over the circumpolar distribution range of this genus. The mtDNA phylogeny supports the division of Dicrostonyx into four species suggested on the basis of karyotypes and hybridisation experiments, the Eurasian D. torquatus and the North American D. groenlandicus, D. hudsonius and D. richardsoni. The interspecific divergence estimates (mean 4.89%) suggest that radiation took place during the Pleistocene and gives support for the importance of vicariant events generated by the glacial-interglacial periods for speciation in the chromosomally variable Dicrostonyx. The monophyly of the North America species group indicates one dispersion event across the Bering Land Bridge and does not support the hypothesis that the morphologically primitive D. hudsonius is a relict of an earlier invasion from Eurasia while D. groenlandicus represents a later dispersion event. The division of the North America D. groenlandicus in the two phylogeographic groups with limited divergence (0.63%) across the Mackenzie river is consistent with separation of this species in more than one refugial area located to the north west of the Laurentide ice sheet during the last glaciation. Within the Eurasian D. torquatus, the group of haplotypes from the area to the east of the Kolyma river has the basal position. This gives support for the importance of the Asian Beringia as a refugial area for the tundra specialist, D. torquatus, during one of the warm interglacials in the late Pleistocene.