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Multilocus Phylogeny and Taxonomy of East Asian Voles Alexandromys (Rodentia, Arvicolinae)

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Multilocus Phylogeny and Taxonomy of East Asian Voles Alexandromys (Rodentia, Arvicolinae) Received: 3 June 2017 | Accepted: 8 September 2017 DOI: 10.1111/zsc.12261 ORIGINAL ARTICLE Multilocus phylogeny and taxonomy of East Asian voles Alexandromys (Rodentia, Arvicolinae) Andrey A. Lissovsky1 | Tatyana V. Petrova2 | Svetlana P. Yatsentyuk3 | Fedor N. Golenishchev2 | Nikolay I. Putincev4 | Irina V. Kartavtseva5 | Irina N. Sheremetyeva5 | Natalia I. Abramson2 1Zoological Museum, Moscow State University, Moscow, Russia Phylogenetic relationships, taxonomy and nomenclature issues within East Asian Alexandromys 2Zoological Institute, Russian Academy of voles were addressed using comprehensive species samples, including Science, Saint Petersburg, Russia all 12 valid species of the genus, and multilocus analysis. We examined the mito- 3The All-Russian State Center for Quality chondrial cytochrome b (cytb) gene and three nuclear genes in 36 specimens. and Standardization of Veterinary Drugs Additionally, we examined a data set of 106 specimens using only the cytb gene. Our and Feed, Moscow, Russia results did not confirm the aggregation of A. kikuchii, A. montebelli and A. oecono- 4Tuva State University, Kyzyl, Tuva Republic, Russia mus into a separate clade, namely the subgenus Pallasiinus. Analysis of incomplete 5Federal Scientific Center of the East Asia lineage sorting using JML software highlighted both the cases of mitochondrial intro- Terrestrial Biodiversity, Far Eastern Branch gression and incomplete lineage sorting within the genus. Thus, the sister position of of the Russian Academy of Sciences (FEB A. sachalinensis A. maximowiczii RAS), Vladivostok, Russia and in mitochondrial trees could be explained by mitochondrial introgression, while the sister position of A. limnophilus and A. fortis Correspondence in mitochondrial trees could be successfully explained by incomplete lineage sorting. Andrey A. Lissovsky, Zoological Museum, Moscow State University, Moscow, Russia. Very short genetic distances, together with an absence of monophyly, of the three Email: [email protected] species, A. evoronensis, A. mujanensis and A. maximowiczii, is supported by multiple Funding information morphological data, which indicates that these three taxa should be one species— Russian Foundation for Basic Research, A. maximowiczii. Analysis of genetic distances and tree topology revealed that three Grant/Award Number: 14-04-00163, A. middendorffii A. mongolicus A. gromovi 15-04-04602 and 16-04-00983; MSU species of short- tailed voles— , and —are Zoological Museum, Grant/Award Number: more closely related to each other than to other established species of Alexandromys. AAAA-A16-116021660077-3; Theriology The lacustrine vole, A. limnophilus, is closely related to the group of short- tailed laboratory of ZIN RAS, Grant/Award Number: AAAA-A17-117022810195-3 voles. Analysis of the type specimens of limnophilus and flaviventris confirmed that these taxa form one species together with A. l. malygini. Our results suggest that the [Version of Record, published online on 20 October 2017; urn:lsid:zoobank. mountains of western Mongolia are inhabited by a new taxon of short- tailed voles of org:act:640F3AA1-6EEB-4068-8CCBC the same rank as middendorffii, mongolicus and gromovi—A. m. alpinus ssp. n. 64EFC30BAB0 KEYWORDS Alexandromys, multilocus analysis, phylogeny, taxonomy, 1 | INTRODUCTION North America. East Asian voles generally prefer wet habi- tats along rivers or lake shores, wetlands within taiga, steppe, Voles of the Alexandromys Ognev, 1914 genus are widely dis- semidesert and desert zones, often inhabiting higher eleva- tributed in the Eastern Palaearctic. One species, the root vole tions in mountains. Such discontinuous distributions can A. oeconomus (Pallas, 1776) penetrates to Western Europe, potentially lead to separation of various geographical forms, and east to the Alaska Peninsula and adjacent regions of including those worthy of a taxonomic rank. Zoologica Scripta. 2018;47:9–20. wileyonlinelibrary.com/journal/zsc © 2017 Royal Swedish Academy of Sciences | 9 10 | LISSOVSKY ET AL. Due to the high level of morphological similarity in after the morphological and genetic analysis of a larger data grey voles (tribe Arvicolini Gray, 1821), Alexandromys was set (Lissovsky et al., 2010). This taxon should be consid- not recognised as a monophyletic group for a long time. ered as a junior synonym of A. middendorffii. Several taxo- Following modern splitting tendency, the taxonomic status of nomic issues remain unresolved. The taxonomic integrity of Alexandromys was elevated from subgeneric within the genus A. limnophilus across the distribution range was predicted by of Microtus Schrank, 1798 to full generic rank (Abramson karyological studies (Courant et al., 1999; Malygin, Orlov, & Lissovsky, 2012). Currently, the genus Alexandromys is & Yatsenko, 1990); morphological variation within this spe- considered to include 12 species: A. evoronensis Kovalskaya cies was studied on the basis of very limited samples only et Sokolov, 1980; A. fortis Büchner, 1889; A. gromovi (Lissovsky & Obolenskaya, 2011), while molecular studies Vorontsov et al. 1988; A. kikuchii Kuroda, 1920; A. limnoph- did not address different geographical forms of the species. ilus Büchner, 1889; A. maximowiczii Schrenk, 1859; A. mid- The putative taxon M. arvalis baicalensis Fetisov, 1941 occu- dendorffii Poljakov, 1881; A. mongolicus Radde, 1861; pies an indefinite taxonomic position, as its holotype was lost; A. montebelli Milne- Edwards, 1872; A. mujanensis Orlov meanwhile, this name could be a potential senior synonym for et Kovalskaya, 1978; and A. oeconomus and A. sachalinen- short- tailed voles from southern Siberia and adjacent regions. sis Vasin, 1955. Previously, these species were assigned to In summary, it must be highlighted that despite that East different subgenera—Microtus, Pallasiinus Kretzoi, 1964, Asian vole systematics and phylogeny being addressed earlier proper Alexandromys—and even to a separate genus Volemys by various authors, many issues remain unclear. Moreover, all Zagorodnyuk, 1990 (Gromov & Erbajeva, 1995; Gromov & previous studies on Alexandromys with the application of ge- Polyakov, 1977; Meyer, Golenishchev, Radjabli, & Sablina, netic analyses used only sequences of mitochondrial DNA frag- 1996; Pavlinov & Rossolimo, 1998; Zagorodnyuk, 1990). ments (Bannikova et al., 2010; Conroy & Cook, 2000; Haring Studies based on the mitochondrial cytochrome b (cytb) et al., 2011). Thus, this study aimed to elucidate the phyloge- gene (Bannikova et al., 2010; Conroy & Cook, 2000) netic relationships in a multilocus approach and to clarify tax- showed the existence of two separate phylogenetic lineages onomy and nomenclature issues within the genus Alexandromys within East Asian voles: Pallasiinus (A. kikuchii, A. mon- analysing the most comprehensive species sample, including all tebelli, A. oeconomus) and Alexandromys s. str., including recognised species of the genus. We also sequenced partial se- the remaining nine species. Within Alexandromys s. str., quences of the cytochrome b gene from a number of old type two clusters (A. maximowiczii together with A. sachalin- specimens to solve some nomenclatorial issues. ensis; and A. middendorffii, A. mongolicus, together with A. gromovi) obtained high support values. The sister posi- tion of A. maximowiczii and A. sachalinensis was supported 2 | MATERIAL AND METHODS in the study of the mitochondrial control region (Haring, Sheremetyeva, & Kryukov, 2011). Despite the phylogenetic Analysis was performed on the basis of two data sets. The signal in conventional morphological data being obscure, re- main analysis included 36 specimens of Alexandromys voles sults of morphological analysis of the group (Lissovsky & (Table S1; Figure 1) that were studied using four genes, listed Obolenskaya, 2011) highlighted some contradictive points in below. The second, larger data set with 106 specimens was mitochondrial- based phylogeny. If the clade of short-tailed analysed using the cytb gene only. This data set included se- voles (A. middendorffii, A. mongolicus and A. gromovi) is quences from type specimens of nominal taxa limnophilus in a good agreement with their morphological similarity, the and flaviventris, paratypes of baicalensis, and topotypes of association of A. maximowiczii and A. sachalinensis is con- kharanurensis. Myodes rutilus (Pallas, 1779), Arvicola am- tradictory. Alexandromys sachalinensis displays very high phibius (Linnaeus, 1758) and Microtus arvalis (Pallas, 1778) cranial similarity with another species of the genus, A. fortis. were used as an outgroup in each data set. Most samples were Morphological studies performed on various species represented by fresh tissues fixed in ethanol; the second data within the genus showed the following: morphological dif- set also included fragments of skin from specimens from ferences between A. evoronensis, A. mujanensis and A. max- old museum collections. The majority of examined speci- imowiczii are very shallow (Lissovsky & Obolenskaya, 2011; mens were identified on the basis of morphological features Meyer et al., 1996; Voyta, Golenishchev, & Tiunov, 2013); according to Lissovsky and Obolenskaya (2011). Some spec- A. mongolicus consists of two morphologically distinct geo- imens were karyotyped (Table S1). graphical forms (Lissovsky & Obolenskaya, 2011); the sub- Sequences of the cytochrome b (cytb) gene (1,140 bp); species of the root vole A. o. kharanurensis Courant et al., exon 11 of breast cancer 1 nuclear gene (BRCA1) (alignment 1999 is very
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