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Molecular Phylogeny and Taxonomy of the Genus Mustela

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Molecular Phylogeny and Taxonomy of the Genus Mustela Mammal Study 33: 25–33 (2008) © the Mammalogical Society of Japan Molecular phylogeny and taxonomy of the genus Mustela (Mustelidae, Carnivora), inferred from mitochondrial DNA sequences: New perspectives on phylogenetic status of the back-striped weasel and American mink Naoko Kurose1, Alexei V. Abramov2 and Ryuichi Masuda3,* 1 Department of Biological Sciences, Faculty of Science, Kanagawa University, Kanagawa 259-1293, Japan 2 Zoological Institute, Russian Academy of Sciences, Saint-Petersburg 199034, Russia 3 Creative Research Initiative “Sousei”, Hokkaido University, Sapporo 060-0810, Japan Abstract. To further understand the phylogenetic relationships among the mustelid genus Mustela, we newly determined nucleotide sequences of the mitochondrial 12S rRNA gene from 11 Eurasian species of Mustela, including the domestic ferret and the American mink. Phylogenetic relationships inferred from the 12S rRNA sequences were similar to those based on previously reported mitochondrial cytochrome b data. Combined analyses of the two genes demonstrated that species of Mustela were divided into two primary clades, named “the small weasel group” and “the large weasel group”, and others. The Japanese weasel (Mustela itatsi) formerly classified as a subspecies of the Siberian weasel (M. sibirica), was genetically well-differentiated from M. sibirica, and the two species clustered with each other. The European mink (M. lutreola) was closely related to “the ferret group” (M. furo, M. putorius, and M. eversmanii). Both the American mink of North America and the back-striped weasel (M. strigidorsa) of Southeast Asia were more closely related to each other than to other species of Mustela, indicating that M. strigidorsa originated from an independent lineage that differs from other Eurasian weasels. Based on biochemical, cytogenetic, and molecular differences as well as morphological evidence, it is proposed that the American mink be elevated to a distinct mustelid genus, Neovison. Key words: American mink, mitochondrial DNA phylogeny, Mustela, Mustela strigidorsa, 12S rRNA. The family Mustelidae, which consists of 59 species, is least weasel (M. nivalis), Malaysian weasel (M. nudipes), the most species rich family in the order Carnivora European polecat (M. putorius), Siberian weasel (M. (Wozencraft 2005). In this family, the genus Mustela sibirica) and back-striped weasel (M. strigidorsa). Some (mammalian group generally called ‘weasels’) is a poly- of these species have a Holarctic (M. erminea and M. typic genus widely distributed in Europe, Northern nivalis) or a Eurasian (M. eversmanii, M. putorius and M. Africa, Asia, North America, and northern parts of South lutreola) distribution. The distribution range of the other America. These small or middle-sized weasels occur in species is restricted to Asia (M. altaica, M. kathiah and diverse habitats from tropical rainforests to tundra and M. sibirica), and some species have small (or insular) from steppe and desert to riparian biotopes and coastal distribution areas (M. strigidorsa, M. nudipes, M. itatsi, waters. Mustela is the largest genus of Carnivora and is M. lutreolina). The American mink (M. vison) was comprised 17 species (Abramov 2000a; Wozencraft introduced to the Old World from North America, and 2005). In Eurasia, 12 species of Mustela are known: naturalized in Eurasia: from the British Islands to Sibe- mountain weasel (M. altaica), ermine (M. erminea), ria, China, and the Japanese Islands. steppe polecat (M. eversmanii), Japanese weasel (M. Relationships among the species of Mustela have not itatsi), yellow-bellied weasel (M. kathiah), European been fully clarified. The grouping of species within the mink (M. lutreola), Indonesian weasel (M. lutreolina), genus differ in the classifications of different authors. *To whom correspondence should be addressed. E-mail: [email protected] 26 Mammal Study 33 (2008) Some authors divided the genus Mustela into two genetic relationships among Mustela species, we newly (Ellerman and Morrison-Scott 1951; Heptner et al. determined partial sequences (about 960 base-pairs, bp) 1967), four (Pavlinov et al. 1995), or five subgenera of the 12S rRNA gene of the mitochondrial DNA (Youngman 1982; Anderson 1989). Recently, Abramov (mtDNA) genome from 11 species of Mustela of Eura- (2000a) divided this genus to nine subgenera and re- sia, including the domestic ferret and the American garded the American mink as a separate genus, Neovison. mink. The poorly studied back-striped weasel (M. Many studies have been performed to understand the strigidorsa) from Southeast Asia was included in the phylogenetic relationships within this group. These genetic study for the first time. Combining the data with studies are based upon the analysis of morphological char- previously reported cytochrome b gene data, we present acters (Youngman 1982; Anderson 1989; Baryshnikov here the molecular phylogeny of Eurasian representa- and Abramov 1997; Abramov 2000a), biochemical data tives of Mustela and discuss evolutionary and taxonomic (Belyaev et al. 1980; Taranin et al. 1991) and genetic relationships among species. data (Graphodatsky et al. 1976; Lushnikova et al. 1989; Masuda and Yoshida 1994a; Davison et al. 1999, 2000; Materials and methods Hosoda et al. 2000; Kurose et al. 2000a; Sato et al. 2003). However, the overall phylogeny of Mustela is still Samples and DNA extraction unresolved. Species of Mustela examined are listed in Table 1. In the present study, to further understand the phylo- Muscle tissue from animals were preserved in 70–100% Table 1. Profiles of samples examined in the present study & Code Chromosome Sampling locality Accession Number Species Common name # Tissue (individual no.) No. (2n) if known 12S rRNA Cytochrome b Mustela nivalis Least weasel MNI (5) 42# muscle Hokkaido, Japan AB119065 AB026106* (38$) Mustela altaica Mountain weasel MAL (RMNG1) 44# muscle Great Hingan Mts, AB119064 AB026100* Mongolia (ZIN C.83033)@ Mustela erminea Ermine MER (1) 44# muscle Hokkaido, Japan AB119066 AB026101* Mustela itatsi Japanese weasel MIT (MR1) 38$ muscle Iwate, Japan AB119071 AB026104* Mustela sibirica Siberian weasel MSI (KYO1) 38# muscle Kyoto, Japan AB119072 AB026108* Mustela Steppe polecat MEV (RURA1) 38# muscle Chelyabinsk Province, AB119068 AB026102* eversmanii Russia (ZIN O.34843)@ Mustela putorius European polecat MPU (RLEN1) 40# muscle Leningrad Province, AB119067 AB026107* Russia (ZIN O.34838)@ Mustela furo Ferret MFU (2) 40! hair Domestic AB119069 AB026103* Mustela lutreola European mink MLU (RPSK1) 38# muscle Pskov Province, AB119070 AB026105* Russia (ZIN C.55065)@ Mustela Back-striped weasel MST (1) – muscle Vinh Phuc Province, AB119073 AB119078 strigidorsa Vietnam (ZIN C.85042)@ Mustela vison American mink MVI (1) 30# muscle Domestic AB119074 AB026109* Martes melampus Japanese marten MME (1) 38$ muscle Iwate, Japan AB119075 AB012351* Martes zibellina Sable MZI (1) 38+ muscle Hokkaido, Japan AB119076 AB012360* Meles anakuma Japanese badger MEL (K6) 44$ muscle Kitakyushu, Japan AB119077 AB049800** # Cited from Graphodatsky et al. (1976). $ Obara (1991) reported 38 chromosomes specific to the population of the Honshu Island (Japan). + Cited from Graphodatsky et al. (1977). ! Cited from Fredga and Mandahl (1973). @ Specimen no. of Zoological Institute of Russian Academy of Sciences, St. Petersburg (ZIN). & The nucleotide sequence data reported in the present study will appear in the DDBJ, EMBL, and GenBank nucleotide sequence databases with these accession numbers. * Cited from Kurose et al. (2000a). ** Cited from Kurose et al. (2001). Kurose et al., Molecular phylogeny of Mustela 27 ethanol at room temperature until use. As outgroup, the using the cycle labeling system Catalyst (Perkin-Elmer Japanese marten (Martes melampus), sable (Martes Cetus) and sequenced using the ABI PrismTM 377 auto- zibellina) and Japanese badger (Meles anakuma) were mated sequencer. analyzed in addition to cytochrome b (accession no. X82296) and 12S rRNA (AY012149) sequences of the Sequence analysis domestic cat (Felis catus). Total genomic DNAs were Sequence alignment was done using the GeneWorks extracted using the phenol/proteinase K/sodium dodecyl computer software (Intelligenetics). Molecular phylo- sulfate method of Sambrook et al. (1989) with some genetic analyses were perfomed using PAUP* version simplified modifications as indicated by Masuda and 4.0b10 (Swofford 2001). The phylogenetic trees were Yoshida (1994b). DNA extracts of M. lutreola (muscle constructed by three methods: neighbor-joining (NJ: tissues preserved in 70% ethanol for about 30 years) Saitou and Nei 1987) using Kimura’s (1980) two- and M. altaica (muscle tissues preserved in 70% ethanol parameter distances, maximum parsimony (MP) and the for about 100 years) were concentrated to approximate- maximum likelihood (ML). Because phylogenetic rela- ly 100 fold using Centricon-30 microconcentrators tionships of species were very similar among separate (Amicon), because these tissues contained fragmented analyses of cytochrome b and 12S rRNA as well as DNAs. DNA from hairs was extracted from M. furo analyses in which the two genes were combined, we using the method of Walsh et al. (1991). An aliquot (1– used the combined sequences (about 2,110 bp) and 10 µl) of each DNA extract was used as template for excluded insertions or deletions (indels) for analysis. the subsequent polymerase chain reaction (PCR). The MP trees were obtained using the heuristic search option with random sequence
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