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Complete Mitochondrial Genome of an Arctic Collared Lemming Subspecies Endemic to the Novaya Zemlya Archipelago, Russia

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Complete Mitochondrial Genome of an Arctic Collared Lemming Subspecies Endemic to the Novaya Zemlya Archipelago, Russia Ecologica Montenegrina 40: 133-139 (2021) This journal is available online at: www.biotaxa.org/em http://dx.doi.org/10.37828/em.2021.40.12 Complete mitochondrial genome of an Arctic Collared Lemming subspecies endemic to the Novaya Zemlya Archipelago, Russia VITALY M. SPITSYN1,*, ALEXANDER V. KONDAKOV1,2,3, ELSA FROUFE4, MIKHAIL Y. GOFAROV1, ANDRÉ GOMES-DOS-SANTOS4,5, JOÃO TEIGA-TEIXEIRA4, ELIZAVETA A. SPITSYNA1, NATALIA A. ZUBRII1,3, MANUEL LOPES-LIMA4,6 & IVAN N. BOLOTOV1,2,3 1N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences, Arkhangelsk, Russia 2Saint Petersburg State University, Saint Petersburg, Russia 3Northern Arctic Federal University, Arkhangelsk, Russia 4CIIMAR/CIMAR – Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Matosinhos, Portugal 5Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre, Porto, Portugal 6CIBIO/InBIO – Research Center in Biodiversity and Genetic Resources, University of Porto, Vairão, Portugal *Corresponding author: [email protected] Received: 17 March 2021│ Accepted by V. Pešić: 20 March 2021 │ Published online: 22 March 2021. In this study, we present an announcement of Novaya Zemlya Collared Lemming Dicrostonyx torquatus ungulatus (von Baer, 1841) complete mitogenome. This rodent was described historically as an Arctic Collared Lemming subspecies endemic to Novaya Zemlya (Arctic Russia) but its taxonomic status was unclear due to the lack of available molecular data. Based on a comprehensive mitogenomic phylogeny of the Arctic Collared Lemming, we show that this insular population shares a highly divergent mtDNA sequence (total length 16,341 bp). Hence, it should be considered a valid subspecies of the Arctic Collared Lemming. Our findings support the hypothesis that the Novaya Zemlya Archipelago had served as a cryptic polar refugium for cold-tolerant terrestrial and freshwater taxa since the mid-Pleistocene or even earlier. The Arctic Collared Lemming Dicrostonyx torquatus (Pallas, 1779) (Mammalia: Rodentia: Cricetidae) is one of the most abundant rodent species in Northern Eurasia, and is an appropriate model object for phylogeographic and paleogeographic reconstructions (Palkopoulou et al. 2016; Fedorov et al. 2020). Currently, three subspecies of Arctic Collared Lemming are recognized (Burgin et al. 2020). The nominate subspecies occurs from the Kanin Peninsula to the Yenisei River, while the East Siberian subspecies Dicrostonyx torquatus chionopaes G. M. Allen, 1914 ranges from the Yenisei River to the northeastern edge of the continent. Finally, the Novaya Zemlya subspecies Dicrostonyx torquatus ungulatus (von Baer, 1841) appears to be an insular lineage endemic to the Novaya Zemlya Archipelago. The two mainland subspecies are indeed divergent genetic lineages that were isolated at least 64 Kyr ago (Fedorov et al. 2020), while the Novaya Zemlya subspecies was a somewhat enigmatic taxon due to the lack of available molecular data. Ecologica Montenegrina, 40, 2021, 133-139 COMPLETE MITOCHONDRIAL GENOME OF NOVAYA ZEMLYA COLLARED LEMMING Figure 1. Morphology of Novaya Zemlya Collared Lemming Dicrostonyx torquatus ungulatus (von Baer, 1841) from Novaya Zemlya Archipelago, Arctic Russia [topotype No. RMBH Lem16]: (A, B) specimen: (A) dorsal view, (B) ventral view; (C, D, E) crania: (C) dorsal view, (D) ventral view, (E) lateral view; (F, G) lower jaw: (F) outer lateral view, (G) inner lateral view; (H, I) molar rows: (H) maxillary, and (I) mandibular. Scale bars = 10 mm. (Photos: Elizaveta A. Spitsyna). 134 SPITSYN ET AL. Here, we present the complete mitogenome of Novaya Zemlya Collared Lemming Dicrostonyx torquatus ungulatus and briefly discuss its phylogenetic position in a broader biogeographic context. A specimen of this subspecies [voucher RMBH Lem16] was collected on 28 July 2015 near the Polar Station Malye Karmakuly, 72.3615°N, 52.7719°E, Yuzhny (Southern) Island, Novaya Zemlya, Russia (collector: V. M. Spitsyn) (Fig. 1). The specimen was deposited in the RMBH – Russian Museum of Biodiversity Hotspots, N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences, Arkhangelsk, Russia. All applicable international, national, and/or institutional guidelines for the care and use of animals were strictly followed. The sampling procedures were approved by the Ethics Committee on Animal Research of the Institute of Ecological Problems of the North of Ural Branch of the Russian Academy of Sciences, Arkhangelsk, Russia (order no. 001-05/15 of May 10, 2015). Figure 2. Gene map of Novaya Zemlya Collared Lemming Dicrostonyx torquatus ungulatus (von Baer, 1841) mitochondrial genome [topotype No. RMBH Lem16; GenBank accession No. MW401673]. Genes positioned inside the circle are encoded on the heavy strand, and genes outside the circle are encoded on the light strand. Color codes: Small and large ribosomal RNAs (red), transfer RNAs (purple), control region and OriL-strand (yellow), and PCGs genes (green). Ecologica Montenegrina, 40, 2021, 133-139 135 COMPLETE MITOCHONDRIAL GENOME OF NOVAYA ZEMLYA COLLARED LEMMING Figure 3. Bayesian Inference phylogenetic tree of the concatenated protein coding and rRNA genes based on available mitogenomes of Arctic Collared Lemming Dicrostonyx torquatus. The red font indicates the Novaya Zemlya subspecies D. torquatus ungulatus. The numbers near nodes represent Bayesian Posterior Probabilities (BPP) of MrBayes / Bootstrap Support (BS) values of IQ-Tree. The values above 95% for both BPP/BS are replaced with an asterisk. Outgroup taxa (Dicrostonyx hudsonius and D. groenlandicus) are not shown. 136 SPITSYN ET AL. Genomic DNA was extracted using a standard high-salt protocol (Sambrook et al. 1989) and thereafter sequenced using MiSeq Illumina runs. Resulting reads were trimmed in Trimmomatic (Bolger et al. 2014). The mitogenome was assembled using MITObim (Hahn et al. 2013) and annotated in MITOS (Bernt et al. 2013). A complete mitogenome of Dicrostonyx torquatus ungulatus was submitted to GenBank under the accession number MW401673. The mitogenome was mapped using GenomeVx (Conant & Wolfe 2008). This sequence contains 16,341 bps and is composed of 13 protein-coding genes (PCGs), 2 rRNAs, and 22 tRNAs (Fig. 2). The mitogenome has an A + T content of 60.0% (A 32.7%; T 27.3%; C 13.1%; G 26.8%), which is a typical structure of Arctic Collared Lemming mitogenomes (Fedorov et al. 2020). To reconstruct Dicrostonyx torquatus phylogeny, all the available mitogenome sequences [N = 54; acc. no. MN792931–MN792983, and KX066190] were downloaded from GenBank. Additionally, Labrador Collared Lemming Dicrostonyx hudsonius (Pallas, 1778) [N = 1; acc. no. KX683880] and Nearctic Collared Lemming D. groenlandicus (Traill, 1823) [N = 6; acc. no. MN792984–MN792988, and KX712239] mitogenomes were used as outgroup. Individual PCG and rRNA genes were separately aligned with the MUSCLE algorithm of MEGA7 (Kumar et al. 2016). The single gene sequence alignments were joined into a combined alignment that was collapsed into unique haplotypes using an online FASTA sequence toolbox FaBox 1.41 (Villesen, 2007). The maximum likelihood (ML) phylogenetic analyses were computed with W- IQ-TREE v. 1.6.11 with an automatic detection of the best evolutionary model (TPM2u+F+R2) through an online web server (http://iqtree.cibiv.univie.ac.at) (Nguyen et al. 2015; Trifinopoulos et al. 2016). Node support values were calculated using an ultrafast bootstrapping algorithm with 10,000 replications (Hoang et al. 2018). Bayesian inference (BI) analyses were performed in MrBayes v. 3.2.6 (Ronquist et al. 2012) at the San Diego Supercomputer Center through the CIPRES Science Gateway (Miller et al. 2010). Two runs, each with three heated (temperature = 0.1) and one cold Markov chain, were conducted for 30 million generations. Trees were sampled every 1000th generation. After completion of the MCMC analysis, the first 15% of trees were discarded as burn-in, and the majority rule consensus tree was calculated from the remaining trees. The ML and BI trees returned the same topology that agrees with an earlier mitogenomic phylogeny of Arctic Collared Lemming (Fedorov et al. 2020). The Novaya Zemlya’s lemming represents a divergent mtDNA lineage (uncorrected p-distance from other samples of 0.7–1.2% based on complete mitogenomes). This lineage sisters to a mainland clade containing samples from Northeastern Europe (Pechora River mouth) and Arctic Siberia (Yamal and Taymyr peninsulas) (Fig. 3). Hence, our results confirm that Novaya Zemlya harbors a valid endemic subspecies of Arctic Collared Lemming. The same pattern was discovered recently in other lemming species that is known to occur on the archipelago (Spitsyn et al. 2021). In particular, a Lemmus population from Novaya Zemlya was found to be an insular subspecies of Norwegian Lemming, i.e. L. lemmus chernovi Spitsyn, Bolotov & Kondakov, 2021 (Spitsyn et al. 2021). Overall, these findings support the hypothesis that the Novaya Zemlya Archipelago was a cryptic polar refugium for cold-adapted animal and plant species during the Pleistocene and Holocene epochs (Serebryanny & Malyasova 1998; Potapov et al. 2018; Makhrov et al. 2019; Spitsyn et al. 2021). Acknowledgements The Russian Foundation for Basic Research supported the morphological study of collared lemming samples (projects 19-34-90012 to V.M.S. and 18-44-292001 to I.N.B.). The Russian Science Foundation funded the phylogenetic
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