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Molecular Phylogeny of East and Southeast Asian Fossorial Moles (Lipotyphla, Talpidae)

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Molecular Phylogeny of East and Southeast Asian Fossorial Moles (Lipotyphla, Talpidae) Journal of Mammalogy, 95(3):455–466, 2014 Molecular phylogeny of East and Southeast Asian fossorial moles (Lipotyphla, Talpidae) AKIO SHINOHARA,* SHIN-ICHIRO KAWADA,NGUYEN TRUONG SON,CHIHIRO KOSHIMOTO,HIDEKI ENDO,DANG NGOC CAN, AND HITOSHI SUZUKI Division of Bio-resources, Department of Biotechnology, Frontier Science Research Center, University of Miyazaki, Downloaded from https://academic.oup.com/jmammal/article-abstract/95/3/455/876160 by guest on 13 September 2019 Kihara 5200, Kiyotake, Miyazaki 889-1692, Japan (AS, CK) Department of Zoology, National Museum of Nature and Science, 4-1-1, Amakubo, Tsukuba, Ibaraki 305-0005, Japan (SK) Department of Vertebrate Zoology, Institute of Ecology and Biological Resources (IEBR), Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet Road, Hanoi, Vietnam (NTS, DNC) The University Museum, The University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 113-0033, Japan (HE) Graduate School of Environmental Science, Hokkaido University, Kita-ku, Sapporo 060-0810, Japan (HS) * Correspondent: [email protected] The diversity of fossorial moles in East and Southeast Asia is contained in the 2 species-rich genera Mogera (8 species) and Euroscaptor (8 or more species), and the 3 monospecific genera Scapanulus, Scaptochirus, and Parascaptor. To better understand the evolution and biogeography of these fossorial moles, we conducted molecular phylogenetic analyses using mitochondrial cytochrome-b (Cytb; 1,140 base pairs [bp]) and 12S rRNA (approximately 830 bp) and nuclear recombination activating gene 1 (Rag1; 1,010 bp) gene sequences from 5 species of Euroscaptor,6ofMogera, and the single species of Scaptochirus. Phylogenetic estimates revealed 5 distinct lineages of East and Southeast Asian fossorial moles: Mogera, Scaptochirus, Euroscaptor mizura, E. parvidens, and E. malayana–E. klossi–E. longirostris. Our results support the monophyly of Mogera but not Euroscaptor, indicating a need for taxonomic revision of the latter genus. We hypothesize that Mogera originated in the central portion of its range and then dispersed to peripheral islands, such as Taiwan and the Japanese Islands. The fragmented distribution of Southeast Asian Euroscaptor presumably arose from habitat competition (invasion) from Mogera species, long-range dispersal, vicariance events, or a combination of these, explaining the high species richness of fossorial moles in this region. Key words: Euroscaptor, Insectivora, Lipotyphla, Mogera, molecular phylogeny, phylogeography, Scaptochirus, Soricomorpha, Talpidae Ó 2014 American Society of Mammalogists DOI: 10.1644/13-MAMM-A-135 The diversity of fossorial moles in East and Southeast Asia (Allen 1938; Ziegler 1971; Motokawa 2004; Kawada and is contained in the 2 species-rich genera Mogera (8 species) Yokohata 2009; see also Sa´nchez-Villagra et al. 2006). and Euroscaptor (8 or more species), and the 3 monospecific The genus Mogera is widely distributed in East Asia (eastern genera Scapanulus, Scaptochirus, and Parascaptor (Hutterer China, Taiwan, Korea, Japan, and Primorye) and Southeast 2005; Kawada et al. 2008, 2012). Four of these genera Asia (southeastern China to northern Vietnam). Of the 8 (Mogera, Euroscaptor, Scaptochirus, and Parascaptor) belong currently recognized species, the large Japanese mole (M. wogura) and La Touche’s mole (M. latouchei) have wide to the tribe Talpini (Hutterer 2005), and have been predom- distributions in East Asia and Southeast Asia, respectively inantly classified by their dental formula: 44 teeth in (Allen 1938). The remaining 6 species are each confined to Euroscaptor (i 3/3, c 1/1, p 4/4, m 3/3, total 44), 42 in rather small geographic areas. The insular mole (M. insularis) Mogera (i 3/2, c 1/1, p 4/4, m 3/3, total 42), 42 in Parascaptor and Kano’s mole (M. kanoana) are endemic to Taiwan. The (i 3/3, c 1/1, p 3/4, m 3/3, total 42), and 40 in Scaptochirus (i 3/ 3, c 1/1, p 3/3, m 3/3, total 40). Because of different combinations of tooth loss, it has been suggested that the dental formula observed in Euroscaptor is the ancestral condition www.mammalogy.org 455 456 JOURNAL OF MAMMALOGY Vol. 95, No. 3 remaining 4 species are endemic to Japan. The lesser Japanese surveys of Southeast Asian fossorial mole populations are mole (M. imaizumii) occurs in eastern Japan (Abe 1974, 2005; needed to elucidate the evolutionary history of fossorial taxa in Ohdachi et al. 2009). The Sado mole (M. tokudae) and the Asia. Etigo mole (M. etigo) are confined to Sado Island and the In our previous studies, we examined the phylogenetic Echigo Plain, respectively. The Senkaku mole (M. uchidai)is relationships of 21 talpid species, including 8 Asian fossorial restricted to Uotsuri Island in the Senkaku Islands (Abe 2005; mole species, and showed that the Asian fossorial moles Ohdachi et al. 2009). formed a monophyletic group to the exclusion of the European Phylogenetic analyses of the genus Mogera are available for Talpa species group (Shinohara et al. 2003, 2004a, 2004b, the East Asian taxa. In particular, the Japanese species, except 2008; Kawada et al. 2007; see also Cabria et al. 2006; for M. uchidai, have been subjected to analyses using Colangelo et al. 2010; Crumpton and Thompson 2013). The Downloaded from https://academic.oup.com/jmammal/article-abstract/95/3/455/876160 by guest on 13 September 2019 mitochondrial DNA (mtDNA) sequences (Okamoto 1999; phylogenetic relationships both among and within the genera Tsuchiya et al. 2000) and nuclear gene sequences (Shinohara et examined, however, have not yet been completely resolved, al. 2004a, 2005; Kirihara et al. 2013). In addition, phylogeo- partly due to ambiguous relationships (Shinohara et al. 2008). graphic analyses of M. imaizumii (Iwasa et al. 2006), M. To obtain finer resolution of Asian talpine phylogeny, we insularis, M. kanoana (Kawada et al. 2007), and M. wogura conducted molecular phylogenetic analyses focusing on the from the Korean Peninsula and adjacent regions (M. w. Southeast Asian fossorial moles. coreana and M. w. robusta—Koh et al. 2012) also have been documented using mtDNA sequences. These recent molecular phylogenetic and phylogeographic studies suggested that the MATERIALS AND METHODS species richness of the modern Mogera lineage is the result of a DNA extraction and sequencing.—The species examined in combination of multiple migration events from mainland Asia this study are listed in Table 1 and mapped in Fig. 1. Details of to the peripheral islands and vicariance events (Tsuchiya et al. collecting localities and species identification of the 2000; Shinohara et al. 2004a, 2005; Iwasa et al. 2006; Kawada Vietnamese and Thai specimens were given in Kawada et al. et al. 2007; Kirihara et al. 2013); however, none of these (2009) and Kawada et al. (2006), respectively. The specimens studies included the Southeast Asian member of the genus, M. of Taiwanese moles used in this study were the same as in latouchei. Kawada et al. (2007). La Touche’s mole (M. latouchei)is The genus Euroscaptor is distributed mainly in Southeast sometimes considered a synonym of the insular mole (M. Asia, with at least 8 species described. One species, the insularis), but recent studies (Kawada et al. 2007, 2009) based Japanese mountain mole (E. mizura), occurs on the Japanese on morphological and karyological characteristics have Islands, whereas all others occur in mainland Asia and indicated that M. latouchei is a distinct species. In this study Southeast Asia (Hutterer 2005). The 7 Southeast Asian species we follow Kawada et al. (2007, 2009). The nomenclature and are the Kloss’s mole (E. klossi) from Thailand; the greater classification follows Ohdachi et al. (2009) for Japanese moles Chinese mole (E. grandis) from Mt. Emei, China; the long- and Hutterer (2005) for other species. We used the species nosed mole (E. longirostris) from southern China to northern name E. malayana for the Malaysian mole; the history of the Vietnam; the small-toothed mole (E. parvidens) from central species name for this mole was reported in Kawada et al. Vietnam; the Malaysian mole (E. malayana) from peninsular (2003, 2008). Malaysia; the Himalayan mole (E. micrura) from the Genomic DNA from preserved liver, spleen, or muscle, or a Himalayas; and a recently described species from northern combination of these, was extracted by proteinase-K digestion Vietnam, E. subanura (Hutterer 2005; Can et al. 2008; Kawada and phenol–chloroform–isoamyl alcohol extraction procedures, et al. 2008, 2012). Their habitats are extremely fragmented and followed by ethanol precipitation to purify extracted DNA. The usually restricted to highlands, although the ranges of these polymerase chain reaction method for amplification of Southeast Asian species are not well documented. To date, complete mitochondrial cytochrome-b (Cytb; 1,140 base pairs genetic studies to reconstruct the evolutionary history and [bp]), partial mitochondrial 12S rRNA (12S; approximately explain the current species diversity of Euroscaptor have not 900 bp), and partial nuclear recombination activating gene 1 been conducted. Motokawa (2004) examined the skulls of 2 (Rag1; 1,010 bp) genes followed our previous study (Shino- Euroscaptor species and reported that the genus is not hara et al. 2004a). The Cytb gene was first amplified using the monophyletic. By using molecular genetic markers, Shinohara universal primer pair L-14724 and H-15915 (Irwin et al. 1991) et al. (2004b, 2008) reported the phylogenetic position of the and then nested amplifications were carried out using 2 primer Malaysian mole (reported as E. micrura, but specified as E. pairs: L-14724 (Suzuki et al. 1997) and SNH-570, and H- malayana in Kawada et al. [2008]) and the short-faced mole 15916 (Suzuki et al. 2000) and SNL-491. Amplification of 12S (Scaptochirus moschatus), which is widely distributed in was performed using the universal primer pair L-613 (Mindell China; this analysis also supported a paraphyletic origin of et al. 1991) and H-1478 (Kocher et al. 1989), with nested Euroscaptor.
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