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

doi:10.17520/biods.2016003

Abstract

Abstract:

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

Xiao Luo, Feng Li, Jing Chen, Zhigang Jiang. The taxonomic status of badgers in the Qinghai Lake area and evolutionary history of Meles[J]. Biodiv Sci, 2016, 24(6): 694-700.

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URL: https://www.biodiversity-science.net/EN/10.17520/biods.2016003

https://www.biodiversity-science.net/EN/Y2016/V24/I6/694

Figures/Tables 5

References 43

[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.

单倍型 Haplotype	样本代码 Sample code	样本编号 Sample no.	采样点 Sampling locality	序列号 Accession no.
单倍型 Haplotype	样本代码 Sample code	样本编号 Sample no.	采样点 Sampling locality	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

单倍型 Haplotype	样本代码 Sample code	样本编号 Sample no.	采样点 Sampling locality	序列号 Accession no.
单倍型 Haplotype	样本代码 Sample code	样本编号 Sample no.	采样点 Sampling locality	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

	西南亚狗獾 M. canescens	欧洲狗獾 M. meles	日本狗獾 M. anakuma	亚洲狗獾 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
青海湖地区狗獾 Badger in the Qinghai Lake area	0.038 ± 0.008	0.041 ± 0.008	0.020 ± 0.006	0.017 ± 0.004

	西南亚狗獾 M. canescens	欧洲狗獾 M. meles	日本狗獾 M. anakuma	亚洲狗獾 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
青海湖地区狗獾 Badger in the Qinghai Lake area	0.038 ± 0.008	0.041 ± 0.008	0.020 ± 0.006	0.017 ± 0.004