Biodiversity Science ›› 2016, Vol. 24 ›› Issue (6): 694-700.doi: 10.17520/biods.2016003

• Orginal Article • Previous Article     Next Article

The taxonomic status of badgers in the Qinghai Lake area and evolutionary history of Meles

Xiao Luo1, 2, Feng Li1, 3, Jing Chen1, 2, Zhigang Jiang1, 2, *()   

  1. 1 Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101
    2 University of Chinese Academy of Sciences, Beijing 100049
    3 The 4th Affiliated Hospital of Jiangsu University, Zhenjiang, Jiangsu 212001
  • Received:2016-01-03 Accepted:2016-05-13 Online:2016-06-20
  • Jiang Zhigang

To investigate the phylogenetic status of badgers (Meles sp.) in the Qinghai Lake area and to estimate the divergence time within Eurasian badgers, the cytochrome b gene and the partial control region (CR) of mitochondrial DNA were examined as genetic markers. Our results indicated that Meles is divided into four species. Twenty one haplotypes were identified in 23 combined sequences (1,652 bp) of Cyt b and CR sequences. Results showed that Eurasian badgers were clearly divided into two major lineages: one of Western lineage, composed of badgers from Europe and Southwest Asia, and the other of Eastern lineage, composed of badgers from North and East Asia (including Japan). Furthermore, the Bayesian tree and the haplotype network indicated that the badgers in the Qinghai Lake area are Asian badgers (M. leucurus). The estimated divergence time was consistent with palaeontological evidence. The first split between the Western lineage and Eastern lineage occurred approximately 2.24 Ma. After the separation, the Southwest Asia clade split from Europe approximately 1.27 Ma and the Japan clade split from continental Asia approximately 0.99 Ma.

Key words: badger, Meles, Qinghai Lake area, cytochrome b, control region, phylogenetic relationship

Fig. 1

Geographic distribution of Eurasian badger. The grey area shows the range of Eurasian badger, the black lines represent geographic boundaries of each phylogenetic group and the black triangle indicates our sampling locality."

Table 1

The mitochondrial DNA sequences information in this study"

Sample code
Sample no.
Sampling locality
序列号 Accession no.
Cyt b Control region
H1 QH1 B1 中国青海 Qinghai, China KU361236 KU361238
H2 QH2 B2 中国青海 Qinghai, China KU361237 KU361239
H2 QH3 B3 中国青海 Qinghai, China KU361237 KU361239
H3 QH4 B4 中国青海 Qinghai, China - KU361239
H4 QH5 B5 中国青海 Qinghai, China - KU361240
H4 QH6 B6 中国青海 Qinghai, China - KU361240
H5 China - 中国黑龙江 Heilongjiang, China KU052604 KU052604
H6 Sweden - 瑞典 Sweden AM711900 AM711900
H7 Mongolia 45Mo 蒙古 Mongolia HQ711950 AJ563694
H8 Greece 80Cr 希腊克里特岛 Crete Island, Greece HQ711947 GU247573
H9 Israel1 49Is 以色列 Israel HQ711946 AJ563686
H10 Israel2 48Is 以色列 Israel HQ711945 AJ563685
H11 Spain 35Sp 西班牙 Spain HQ711943 AJ563676
H12 Russia1 ZIS33 俄罗斯外贝加尔地区 Transbaikalia, Russia AB049807 AB538995
H13 Russia2 ZIS36 俄罗斯列宁格勒州 Leningrad Province, Russia AB049808 AB538997
H14 Russia3 ZIS35 俄罗斯列宁格勒州 Leningrad Province, Russia AB049809 AB538998
H15 Japan1 K1 日本九州大分县 Oita, Kyushu, Japan AB049806 AB538971
H16 Japan2 K6 日本九州大分县 Oita, Kyushu, Japan AB049800 AB538971
H17 Japan3 K7 日本九州大分县 Oita, Kyushu, Japan AB049802 AB538971
H18 Japan4 K8 日本九州福冈县 Fukuoka, Kyushu, Japan AB049799 AB538971
H19 Japan5 YMG1 日本本州山口县 Yamaguchi, Honshu, Japan AB049795 AB538983
H20 Japan6 MR1 日本九州岩手县 Iwate, Kyushu, Japan AB049791 AB538977
H21 Japan7 KPM-NF1002945 日本本州神奈川县 Kanagawa, Honshu, Japan AB291075 AB291075
Arctonyx collaris YP6001 HM106329 HM106329

Fig. 2

Phylogenetic tree of mitochondrial DNA obtained from Bayesian analysis. The sample codes correspond with those in Table 1, in which QH1-6 represent badgers of Qinghai Lake area. The numbers on the branch indicate Bayesian posterior probability and estimated divergence time (with 95% HPD)."

Table 2

Genetic distances among different Eurasian badger groups"

M. canescens
M. meles
M. anakuma
M. leucurus
欧洲狗獾 M. meles 0.034 ± 0.007
日本狗獾 M. anakuma 0.042 ± 0.009 0.043 ± 0.008
亚洲狗獾 M. leucurus 0.040 ± 0.008 0.041 ± 0.008 0.021 ± 0.005
Badger in the Qinghai Lake area
0.038 ± 0.008 0.041 ± 0.008 0.020 ± 0.006 0.017 ± 0.004

Fig. 3

The network based on 21 haplotypes of Eurasian badgers mitochondrial DNA. H1-4 represent Qinghai badgers (in grey). All haplotypes are displayed in Table 1. The black circles represent missing haplotypes. The sizes of the white circles in the network represent the frequencies of each haplotype. Four badger’s groups are circled by dotted line."

[1] Abramov AV (2001) Notes on the taxonomy of the Siberian badgers (Mustelidae: Meles). Proceedings of the Zoological Institute, Russian Academy of Sciences, 288, 221-233.
[2] Abramov AV (2002) Variation of the baculum structure of the Palaearctic badger (Carnivora, Mustelidae, Meles). Russian Journal of Theriology, 1, 57-60.
[3] Abramov AV, Puzachenko AY (2005) Sexual dimorphism of craniological characters in Eurasian badgers, Meles spp. (Carnivora, Mustelidae). Zoologischer Anzeiger, 244, 11-29.
[4] Abramov AV, Puzachenko AY (2006) Geographical variability of skull and taxonomy of Eurasian badgers (Mustelidae, Meles). Zoologicheskii Zhurnal, 85, 641-655. (in Russian with English abstract)
[5] Abramov AV, Puzachenko AY (2013) The taxonomic status of badgers (Mammalia, Mustelidae) from Southwest Asia based on cranial morphometrics, with the redescription of Meles canescens. Zootaxa, 3681(1), 044-058.
[6] Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37-48.
[7] Baryshnikov GF, Potapova OR (1990) Variability of the dental system in badgers (Meles, Carnivora) of the USSR fauna. Zoologicheskii Zhurnal, 69, 84-97. (in Russian with English abstract)
[8] Corbet GB (1978) The Mammals of the Palaearctic Region: A Taxonomic Review. Cornell University Press, London and Ithaca.
[9] Del Cerro I, Marmi J, Ferrando A, Chashchin P, Taberlet P, Bosch M (2010) Nuclear and mitochondrial phylogenies provide evidence for four species of Eurasian badgers (Carnivora). Zoologica Scripta, 39, 415-425.
[10] Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.
[11] Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969-1973.
[12] Frantz AC, McDevitt AD, Pope LC, Kochan J, Davison J, Clements CF, Elmeros M, Molina-Vacas G, Ruiz-Gonzalez A, Balestrieri A, Berge KVD, Breyne P, Do Linh San E, Gren E, Suchentrunk F, Schley L, Kowalczyk R, Kostka BI, Cirovic D, Sprem N, Colyn M, Ghirardi M, Racheva V, Braun C, Oliveira R, Lanszki J, Stubbe A, Stubbe M, Stier N, Burke T (2014) Revisiting the phylogeography and demography of European badgers (Meles meles) based on broad sampling, multiple markers and simulations. Heredity, 113, 443-453.
[13] Gao YT (1987) Fauna Sinica, Mammalia: Vol. 8, Carnivora, pp. 214-223. Science Press, Beijing. (in Chinese)
[高耀亭 (1987) 中国动物志·兽纲: 第八卷, 食肉目, 214-223页. 科学出版社, 北京.]
[14] Koepfli KP, Deere KA, Slater GJ, Begg C, Begg K, Grassman L, Lucherini M, Veron G, Wayne RK (2008) Multigene phylogeny of the Mustelidae: resolving relationships, tempo and biogeographic history of a mammalian adaptive radiation. BMC Biology, 6, 1-22.
[15] Koh HS, Kryukov A, Oh JG, Bayarkhagva D, Yang BG, Ahn NH, Bazarsad D (2014) Two sympatric phylogroups of the Asian badger Meles leucurus (Carnivora: Mammalia) identified by mitochondrial DNA cytochrome b gene sequences. Russian Journal of Theriology, 13, 1-8.
[16] Kurose N, Abramov AV, Masuda R (2000) Intrageneric diversity of the cytochrome b gene and phylogeny of Eurasian species of the genus Mustela (Mustelidae, Carnivora). Zoological Science, 17, 673-679.
[17] Kurten B (1968) The Pleistocene Mammals of Europe. Weidenfeld & Nicolsan, London.
[18] Li F, Jiang ZG (2014) Is nocturnal rhythm of Asian badger (Meles leucurus) caused by human activity? A case study in the eastern area of Qinghai Lake. Biodiversity Science, 22, 758-763. (in Chinese with English abstract)
[李峰, 蒋志刚 (2014) 狗獾夜间活动节律是受人类活动影响而形成的吗? 基于青海湖地区的研究实例. 生物多样性, 22, 758-763.]
[19] Li F, Luo ZH, Li CL, Li CW, Jiang ZG (2013) Biogeographical patterns of the diet of Palearctic badger: Is badger an earthworm specialist predator? Chinese Science Bulletin, 58, 2255-2261.
[20] Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
[21] Lynch JM (1994) Morphometric variation in the badger (Meles meles): clinal variation in cranial size and shape across Eurasia. Small Carnivore Conservation, 10, 6-7.
[22] Madurell-Malapeira J, Alba DM, Marmi J, Aurell J, Moyà-Solà S (2011) The taxonomic status of European Plio-Pleistocene badgers. Journal of Vertebrate Paleontology, 31, 885-894.
[23] Marmi J, López-Giráldez F, MacDonald DW, Calafell E, Zholnerovskaya E, Domingo-Roura X (2006) Mitochondrial DNA reveals a strong phylogeographic structure in the badger across Eurasia. Molecular Ecology, 15, 1007-1020.
[24] Marmi J, López-Giráldez JF, Domingo-Roura X (2004) Phylogeny, evolutionary history and taxonomy of the Mustelidae based on sequences of the cytochrome b gene and a complex repetitive flanking region. Zoologica Scripta, 33, 481-499.
[25] Neal E, Cheeseman C (1996) Badgers. T & AD Poyser Ltd., London.
[26] Nowak RM, Paradiso JL (1999) Walker’s Mammals of the World. Cambridge University Press, London.
[27] Petter G (1971) Origine, phylogenie et systematique des blaireaux. Mammalia, 35, 567-597. (in French)
[28] Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics, 14, 817-818.
[29] Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572-1574.
[30] Song G, Qu Y, Yin Z, Li S, Liu N, Lei F (2009) Phylogeography of the Alcippe morrisonia (Aves: Timaliidae): long population history beyond late Pleistocene glaciations. BMC Evolutionary Biology, 9, 143.
[31] Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725-2729.
[32] Tashima S, Kaneko Y, Anezaki T, Baba M, Yachimori S, Abramov AV, Saveljev AP, Masuda R (2011a) Phylogeographic sympatry and isolation of the Eurasian badgers (Meles, Mustelidae, Carnivora): implications for an alternative analysis using maternally as well as paternally inherited genes. Zoological Science, 28, 293-303.
[33] Tashima S, Kaneko Y, Anezaki T, Baba M, Yachimori S, Abramov AV, Saveljev AP, Masuda R (2011b) Identification and molecular variations of CAN-SINEs from the ZFY gene final intron of the Eurasian badgers (genus Meles). Mammal Study, 36, 41-48.
[34] Thompson JD, Gibson T, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Current Protocols in Bioinformatics, Chapter 2 (Unit 2.3), doi: 10.1002/0471250953.bi0203s00.
[35] Vaidya G, Lohman DJ, Meier R (2011) SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics, 27, 171-180.
[36] Viret J (1950) Meles thorali n. sp. du loess villafranchien de Saint-Vallier (Drôme). Eclogae Geologicae Helvetiae, 43, 274-287. (in French with English abstract)
[37] Wozencraft WC (1993) Order Carnivora. In: Mammal Species of the World: A Taxonomic and Geographic Reference, 2nd edn. (eds Wilson DE, Reeder DM), pp. 279-348. Smithsonian Institution Press, Washington, DC.
[38] Wozencraft WC (2005) Order Carnivora. In: Mammal Species of the World: A Taxonomic and Geographic Reference, 3rd edn. (eds Wilson DE, Reeder DM), pp. 532-628. Johns Hopkins University Press, Baltimore.
[39] Xie ZG (2011) Studies on the Population Ecology of Badger (Meles meles) in Shanghai. PhD dissertation, East China Normal University, Shanghai. (in Chinese with English abstract)
[谢志刚 (2011) 上海地区狗獾生态学研究. 博士学位论文, 华东师范大学, 上海.]
[40] Xu X, Xie ZG, Cui YY, Chu KL, Jiang WZ, Pei EL, Xu HF (2012) Activity patterns of reintroduced badgers in seminatural area. Chinese Journal of Zoology, 47(3), 49-52. (in Chinese with English abstract)
[徐循, 谢志刚, 崔勇勇, 褚可龙, 蒋文忠, 裴恩乐, 徐宏发 (2012) 重引入狗獾秋冬季行为的初步研究. 动物学杂志, 47(3), 49-52.]
[41] Yang HT, Liu ZS, Xu K, Song CL, Wu MF, Sun JH (2010) Autumn habitat selection of Eurasian badgers (Meles meles amurensis): a case of Fangzheng Forestry Bureau, Heilongjiang Province, China. Acta Ecologica Sinica, 30, 1875-1881. (in Chinese with English abstract)
[杨会涛, 刘振生, 徐坤, 宋丛亮, 吴木芬, 孙景海 (2010) 狗獾秋季对生境的选择——以黑龙江省方正林业局为例. 生态学报, 30, 1875-1881.]
[42] Ye XD, Ma Y, Wang RH, Dong AY (2000) Review of the diet of Eurasian badgers. Chinese Journal of Zoology, 35(2), 43-50. (in Chinese)
[叶晓堤, 马勇, 王润海, 董安渝 (2000) 欧亚大陆狗獾食性的研究概述. 动物学杂志, 35(2), 43-50.]
[43] Zhou WW, Yu L, Tan BY, Liu YT, Zhang L, Hua Y (2015) Phylogenetic relationship of Asian badger Meles leucurus amurensis revealed by complete mitochondrial genome. Mitochondrial DNA, published online, doi: 10.3109/ 19401736.2015.1127365.
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