The Importance of Ice Ages in Diversification of Arctic Collared Lemmings (Dicrostonyx): Evidence from the Mitochondrial Cytochrome B Region

Abstract

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.

Multiple glacial refugia in the North American Arctic: inference from phylogeography of the collared lemming (Dicrostonyx groenlandicus)

“…It is notable that all eight haplotypes from the Canadian high Arctic (to the north of Parry Channel) and Greenland (figures 1b and 2) form a distinct lineage within the Canadian phylogroup. Although with limited bootstrap support, the high Arctic phylogroup is defined by the unique 621 A → G transition, which was found in all 23 cytochrome b sequences studied from the Canadian high Arctic and Greenland but not observed in the 34 other sequences sampled over the circumpolar distribution range of the genus Dicrostonyx (Fedorov & Goropashnaya 1999). Consistent with the cytochrome b data, all 78 control region sequences studied in lemmings from the Canadian high Arctic except for individuals from Prince Patrick Island (locality 25) and Greenland (locality 29) had the unique 99 G → A transition which was not observed in the 242 other control region sequences studied over the circumpolar distribution of the genus (Ehrich et al 2000;V.…”

“…Therefore, variation in the cytochrome b gene is suitable for approximate dating of historical events. From the net nucleotide divergence (6%) between the North American and Eurasian collared lemmings (Fedorov & Goropashnaya 1999) and the first occurrence of Dicrostonyx fossil records in North America (1.2 Myr ago; cf. Repenning 2001), the divergence rate for the cytochrome b gene is estimated to be 5% per million years.…”

“…Low mtDNA diversity has previously been found within populations of collared lemmings, Dicrostonyx (Fedorov & Goropashnaya 1999;Ehrich et al 2000). Therefore, in order to examine phylogeographical structure on a continental scale only one or two individuals were studied from each locality.…”

“…Finally, museum skins from the four high Arctic localities (localities 22, 25, 27 and 28) were provided by the Canadian Museum of Nature. Sequences from some localities in eastern Beringia (localities 1, 4, 6 and 8) and the Canadian Arctic (localities 9, 14, 15, 19 and 29) were published elsewhere (Fedorov & Goropashnaya 1999;Ehrich et al 2000).…”

“…The segment (915 bp) of the cytochrome b gene and 300 bp from the 5Ј-end of the control region were amplified by PCR and manually sequenced using several sets of primers as described elsewhere (Fedorov & Goropashnaya 1999;Ehrich et al 2000). We amplified the same part of the cytochrome b gene from the museum skin DNA samples in four overlapping segments using AmpliTaq Gold (PerkinElmer) and specially designed pairs of primers: D1L, TGAAACTTGAAACATAGGCAT-3Ј and D1H, TGTTAGA GAGCCTGTTTCGTGAA-3Ј (280 bp); D2L, TGAAATT TCGGCTCCCTACT-3Ј and D2H, GCACATACCCTAT GAATGCT-3Ј (307 bp); D3L, TCTACCCTTCATCATTA CAGC-3Ј and D3H, AGATCGTAAAATGGCGTAGGC-3Ј (297 bp); D6L, CCACCCCTATTACACAATCA-3Ј and D6H, GAATGTTAGGCCTCGTTGTT-3Ј (272 bp).…”