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Genetic Variations of the Masked Palm Civet Paguma Larvata, Inferred from Mitochondrial Cytochrome B Sequences

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Genetic Variations of the Masked Palm Civet Paguma Larvata, Inferred from Mitochondrial Cytochrome B Sequences Mammal Study 33: 19–24 (2008) © the Mammalogical Society of Japan Genetic variations of the masked palm civet Paguma larvata, inferred from mitochondrial cytochrome b sequences Ryuichi Masuda1,*, Yayoi Kaneko2, Boripat Siriaroonrat3, Vellayan Subramaniam4 and Masaharu Hamachi5 1 Department of Genome Dynamics, Creative Research Initiative “Sousei”, Hokkaido University, Sapporo 060-0810, Japan 2 Yamazaki College of Animal Health Technology, 4-7-2 Minami-osawa, Hachiouji 192-0046, Japan 3 Research and Conservation Division, Zoological Park Organization, Dusit, Bangkok 10300, Thailand 4 Zoo Negara Malaysia, 68000 Ampang, Selangor, Malaysia 5 Fukuoka Zoo, Fukuoka 810-0037, Japan Abstract. It is still unclear whether the masked palm civet (Paguma larvata) is native to the Japanese islands or introduced from the outside via human activities. In the present study, we sequenced the whole region (1,140 base-pairs) of the mitochondrial cytochrome b gene for 29 masked palm civets from Japan and Southeast Asia, and investigated their molecular phylogeography. Nine haplotypes were identified from the animals. Five halpotypes identified from 24 animals of Japan were clustered and separated from four haplotypes from five animals of Southeast Asia, showing clear differentiation between Japanese and Southeast Asian lineages. Sequence differences within Japanese haplotypes were smaller than those within Southeast Asian haplotypes and those between Japanese and Southeast Asian haplotypes. Within Japanese animals, all haplotypes found in eastern Honshu (Kanto district) were different from those of central Honshu (Chubu district). The present study highlighted the problem whether the Japanese Paguma larvata is an introduced species showing multiple original routes, or whether it is a native species genetically differentiated from Southeast Asian populations and even within Japan. Key words: cytochrome b, genetic variation, masked palm civet, Paguma larvata. The masked palm civet (Paguma larvata) is included in Torii (1993) reported no intraspecific variations of the family Viverridae and distributed widely in East, karyotypes and morphology within Japanese individuals Southeast, and West Asia (Lekagul and McNeely 1988; of Paguma larvata, and they presumed that introduction Corbet and Hill 1992). This animal is an only viverrid of this species through multiple routes resulted in the species currently living on the main islands of Japan current irregular distribution in Japan. In addition, (Abe et al. 2005). Since 1943 when their occurrence was Harada and Torii (1993) reported the morphological first recorded from Shizuoka Prefecture (Nawa 1965), difference of the Y chromosome of the Japanese animals, Paguma larvata has been found from various localities compared with that of the Chinese animals reported by of Japan (Kuroda 1955; Imaizumi 1960; Obara 1961) Wang et al. (1984), and showed occurrence of geographic and is currently distributed in eastern Honshu and variations of the Y chromosome. Despite these previous Shikoku (Torii 1996; Abe et al. 2005). However, at studies, there has not been enough data to conclude present there are no fossil nor archaeological records of whether Paguma larvata is native to the Japanese islands this species from the Japanese islands. In order to or introduced from the outside. In order to understand uncover the origins of the Japanese populations, some the origin and status of Paguma larvata of Japan, it is researchers have investigated their ecological character- essential to further investigate their phylogeographical istics (Torii 1986; Torii and Miyake 1986). Harada and and zoogeographical characteristics, compared with *To whom correspondence should be addressed. E-mail: [email protected] 20 Mammal Study 33 (2008) native populations living outside of Japan. In the present study, we report the findings from sequencing of the whole region (1,140 base-pairs, bp) of the mitochondrial DNA (mtDNA) cytochrome b gene for Paguma larvata from several areas of Japan and South- east Asia, and then discuss their genetic variations and the phylogenetic relationships. Materials and methods Samples and DNA extraction Muscle or hair samples were obtained from 24 indi- viduals collected from five localities (13 animals from Tokyo, one from Saitama, four from Ibaraki, four from Gifu, and two from Aichi Prefectures) of Japan and five individuals from Southeast Asia (four from Thailand and one from the Malay Peninsula: the precise locality in these countries was unknown) (Fig. 1). Muscle tissues of Japanese animals were collected from roadkill animals or pest control, and preserved in 70–99% ethanol at room temperature. Hair roots were obtained from living ani- mals during the course of ecological survey in Japan, and Fig. 1. Sampling localities of the masked palm civet Paguma larvata in Japan and haplotypes JA1, JA2, JA3, JA4 and JA5 iden- from zoo animals of Thailand (Duzit Zoo and Khao tified in the present study. Numerals in parentheses show numbers of Khew Open Zoo) and Malaysia (Zoo Negara Malaysia), animals having those haplotypes. and preserved at room temperature. Total DNA was extracted from muscle tissues (about 2 × 2 × 2 mm) using the DNeasy Tissue kit (Qiagen) and from hair sam- (Felsenstain 1985) and for the unrooted phylogenetic tree ples (about 30 hair roots per individual) using the DNA construction of haplotypes due to the neighbor-joining Micro kit (Qiagen), both in accordance with manufac- method (Saitou and Nei 1987). A parsimony network of turer’s instructions. The DNA extracts were subjected to haplotypes were constructed using the computer program polymerase chain reaction (PCR) analysis described TCS ver. 1.21 (Clement et al. 2000). One only sequence below. (accession no. AF125151: Veron and Heard 2000) of the whole region of the Paguma larvata cytochrome b PCR, nucleotide sequencing and data analysis available in DDBJ/Genebank/EMBL databases was also The PCR amplification of the whole region (1,140 bp) included for analysis, although the nucleotide site 1,113 of the cytochrome b gene and sequencing were per- of this sequence was reported to be “Y (C or T)” and its formed using the method same as Tamada et al. (2005). sampling locality was not available in the reference. In the present study, four additional sequencing primers labeled at the 5' end with the Texas Red were newly Results and discussion designed as follows: PLCBIN-1A (5'-TTTCAGAGAC- ATGAAACATTGG-3'); PCBIN-2 (5'-TAGCAATCAT- Variations of cytochrome b sequences identified from CCCACTACTAC-3'); PLCBIN-3 (5'-TCTGACTCAG- Paguma larvata ACAAAATCCC-3'); and PLCB-R1 (5'-GGCAAATAT- For the present study, we identified five haplotypes GGGTTACTGATG-3'). Sequence alignment was done (JA1, JA2, JA3, JA4 and JA5) of the cytochrome b from using GeneWorks (Intelligenetics). Molecular evolu- Japanese animals, and four haplotypes (SE1, SE2, SE3 tionary analysis was carried out using MEGA version 3.1 and SE4) were from Southeast Asian animals (Table 1). (Kumar et al. 2004) for calculations such as nucleotide The sequence alignment showed that all of the nucleotide compositions, sequence differences, genetic distances of substitutions were transitions (Table 1), except that the Kimura’s (1980) two-parameter model, bootstrap values sequence (accession no. AF125151: Veron and Heard Masuda et al., Genetic variations of Paguma larvata 21 Table 1. Nucleotide sequences of cytochrome b of the masked palm civet Paguma larvata Nucleotide site no. Accession Haplotype no.* 46 123 178 179 252 280 285 297 312 315 333 342 408 417 471 519 591 741 749 840 891 947 1113 JA1 GCATTTTACTGCCCACGTTTGTT AB303951 JA2 ••••••••TC•••••••••••••AB303952 JA3 ••••C••••••••••••••••••AB303953 JA4 A••••••••••••••••••••••AB303954 JA5 ••••••••••••••••A••••••AB303955 SE1 •T••••••••••••GT•••••••AB303956 SE2 •T••••••••••••GT•••••C•AB303957 SE3 •T•C•••••••T••GT••C••••AB303958 SE4 •T•••••••••••••T••••A••AB303959 AF125151•TG• •CCC• •A•AA•T•C•A• •Y Haplotypes JA1, JA2, JA3, JA4, JA5, SE1, SE2, SE3 and SE4 were identified in the present study. The sequence (accession no. AF125151; Veron and Heard 2000) has Y (C or T) at site 1113. Dots indicate identities with nucleotides of JA1. * Accession numbers will appear in the DDBJ nucleotide database. Table 2. Pairwise comparisons of cytochrome b haplotypes of Paguma larvata Haplotype JA1 JA2 JA3 JA4 JA5 SE1 SE2 SE3 SE4 AF125151 JA1 2111346311 JA20.18333568513 JA30.090.2622457412 JA40.090.260.182457412 JA50.090.260.180.18457412 SE1 0.26 0.44 0.35 0.35 0.35 1 3 2 10 SE2 0.35 0.53 0.44 0.44 0.44 0.09 4 3 11 SE3 0.53 0.70 0.61 0.61 0.61 0.26 0.35 5 13 SE4 0.26 0.44 0.35 0.35 0.35 0.18 0.26 0.44 10 AF125151 0.97 1.14 1.05 1.05 1.05 0.88 0.97 1.14 0.88 Percentage differences are shown below the digonal and numbers of different nucleotides are indicated above diagonal. 2000) available in the DNA databases had some trans- The sequence differences varied 0.09–0.26% (0.18% on versions to all haplotypes (JA1, JA2, JA3, JA4, JA5, average) within the Japanese haplotypes, 0.09–0.44% SE1, SE2, SE3 and SE4) identified in the present study. (0.26% on average) within the Southeast Asian haplo- All transitions among haplotypes occurred at 13 sites types and 0.26–0.70% (0.34% on average) between the (Table 1). When AF125151 was included, five transi- Japanese and Southeast Asian haplotypes (Table 2). tional and four transversional sites were observed, in These values of sequence differences within obtained addition to the 13 polymorphic sites (Table 1). The aver- haplotypes of Paguma larvata show a degree similar to age relative nucleotide frequencies among the obtained intraspecific differences of the cytochrome b gene of sequences (except AF125151) was A = 30.8%, G = other small carnivore species in Japan: less than 1.58% 12.2%, C = 26.7% and T = 30.3%. These values were in the Japanese marten (Martes melampus) and less than similar to those of the Owston’s palm civet (Chrotogale 0.35% in the sable (Martes zibellina) (Kurose et al.
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