Genetic structure of wild boar (Sus scrofa) populations from East Asia based on microsatellite loci analyses

BMC Genetics

Kyung Seok Kim³  Hang Lee⁷  Ya-Ping Zhang¹  Li Yu^1,11  Naotaka Ishiguro^1,10  Ivan Seryodkin⁸  Nickolay Markov⁹  Tae-Hun Kim⁶  Jang Geun Oh²  Alexander Myslenkov⁴  Inna Voloshina⁴  Mi-Sook Min⁷  Young-Jun Kim⁵  Ji-Eun Lee⁷  Sung Kyoung Choi⁷ 

[1] State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China;Research Institute for Hallasan, Jeju Special Self-Governing Province, Jeju, Republic of Korea;Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA, USA;Lazovsky State Nature Reserve, Lazo, Primorsky Krai, Russia;National Institute of Ecology, Seocheon-gun, Chungcheongnam-do, Republic of Korea;Division of Animal Genomics and Bioinformatics, National Institute of Animal Science, Rural Development Administration, Suwon, Gyeonggi-do, Republic of Korea;College of Veterinary Medicine, Seoul National University, Seoul, Republic of Korea;Pacific Geographical Institute Far Eastern Branch of Russian Academy of Sciences, Vladivostok, Russia;Institute of Plant and Animal Ecology Urals Branch of Russian Academy of Sciences, Yekaterinburg, Russia;Laboratory of Food and Environmental Hygiene, Veterinary Medicine, Gifu University, Gifu, Japan;Laboratory for Conservation and Utilization of Bio-resource and Key Laboratory for Microbial Resources of the Ministry of Education, Yunnan University, Kunming, China

关键词: Wild boar;    Genetic structure;    Genetic diversity;    East Asia;    Microsatellites;   

Others  :  869593
DOI  :  10.1186/1471-2156-15-85

 received in 2014-03-04, accepted in 2014-07-10,  发布年份 2014

【 摘 要 】

Background

Wild boar, Sus scrofa, is an extant wild ancestor of the domestic pig as an agro-economically important mammal. Wild boar has a worldwide distribution with its geographic origin in Southeast Asia, but genetic diversity and genetic structure of wild boar in East Asia are poorly understood. To characterize the pattern and amount of genetic variation and population structure of wild boar in East Asia, we genotyped and analyzed microsatellite loci for a total of 238 wild boar specimens from ten locations across six countries in East and Southeast Asia.

Results

Our data indicated that wild boar populations in East Asia are genetically diverse and structured, showing a significant correlation of genetic distance with geographic distance and implying a low level of gene flow at a regional scale. Bayesian-based clustering analysis was indicative of seven inferred genetic clusters in which wild boars in East Asia are geographically structured. The level of genetic diversity was relatively high in wild boars from Southeast Asia, compared with those from Northeast Asia. This gradient pattern of genetic diversity is consistent with an assumed ancestral population of wild boar in Southeast Asia. Genetic evidences from a relationship tree and structure analysis suggest that wild boar in Jeju Island, South Korea have a distinct genetic background from those in mainland Korea.

Conclusions

Our results reveal a diverse pattern of genetic diversity and the existence of genetic differentiation among wild boar populations inhabiting East Asia. This study highlights the potential contribution of genetic variation of wild boar to the high genetic diversity of local domestic pigs during domestication in East Asia.

【 授权许可】

   
2014 Choi et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Oliver WLR, Brisbin IL Jr, Takahashi S: The Eurasian Wild Pig (Sus scrofa). In Status Survey and Conservation Action Plan: Pigs, Peccaries and Hippos. Chapter 5.2. Edited by Oliver WLR. Gland, Switzerland: IUCN; 1993:112-121.
• [2]Randi E: Conservation genetics of the genus Sus. IBEX J M E 1995, 3:6-12.
• [3]Larson G, Dobney K, Albarella U, Fang M, Matisoo-Smith E, Robins J, Lowden S, Finlayson H, Brand T, Willerslev E, Rowley-Conwy P, Andersson L, Cooper A: Worldwide phylogeography of wild boar reveals multiple centers of pig domestication. Science 2005, 307:1618-1621.
• [4]Wu GS, Yao YG, Qu KX, Ding ZL, Li H, Palanichamy MG, Duan ZY, Li N, Chen YS, Zhang YP: Population phylogenomic analysis of mitochondrial DNA in wild boars and domestic pigs revealed multiple domestication events in East Asia. Genome Biol 2007, 8:R245. BioMed Central Full Text
• [5]Luetkemeier ES, Sodhi M, Schook LB, Malhi RS: Multiple Asian pig origins revealed through genomic analyses. Mol Phylogenet Evol 2010, 54:680-686.
• [6]Giuffra E, Kijas JM, Amarger V, Carlborg O, Jeon JT, Andersson L: The origin of the domestic pig: independent domestication and subsequent introgression. Genetics 2000, 154:1785-1791.
• [7]Manunza A, Zidi A, Yeghoyan S, Balteanu VA, Carsai TC, Scherbakov O, Ramírez O, Eghbalsaied S, Castelló A, Mercadé A, Amills M: A high throughput genotyping approach reveals distinctive autosomal genetic signatures for European and Near Eastern wild boar. PLoS ONE 2013, 8:e55891.
• [8]Hongo H, Ishiguro N, Watanobe T, Shigehara N, Anezaki T, Long VT, Binh DV, Tien NT, Nam NH: Variation in mitochondrial DNA of Vietnamese pigs: relationships with Asian domestic pigs and Ryukyu wild boars. Zoolog Sci 2002, 19:1329-1335.
• [9]Cho IC, Han SH, Fang M, Lee SS, Ko MS, Lee H, Lim HT, Yoo CK, Lee JH, Jeon JT: The robust phylogeny of Korean wild boar (Sus scrofa coreanus) using partial D-loop sequence of mtDNA. Mol Cells 2009, 28:423-430.
• [10]Ramayo Y, Shemeret’eva IN, Pérez-Enciso M: Mitochondrial DNA diversity in wild boar from the Primorsky Krai Region (East Russia). Anim Genet 2010, 42:96-99.
• [11]Ji Y-Q, Wu D-D, Wu G-S, Wang G-D, Zhang Y-P: Multi-locus analysis reveals a different pattern of genetic diversity for mitochondrial and nuclear DNA between wild and domestic pigs in East Asia. PLoS ONE 2011, 6:e26416.
• [12]Larson G, Liu R, Zhao X, Yuan J, Fuller D, Barton L, Dobney K, Fan Q, Gu Z, Liu X-H, Luo Y, Lv P, Andersson L, Li N: Patterns of East Asian pig domestication, migration, and turnover revealed by modern and ancient DNA. Proc Natl Acad Sci U S A 2010, 107:7686-7691.
• [13]Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 2005, 14:2611-2620.
• [14]Frantz LA, Schraiber JG, Madsen O, Megens HJ, Bosse M, Paudel Y, Semiadi G, Meijaard E, Li N, Crooijmans RP, Archibald AL, Slatkin M, Schook LB, Larson G, Groenen MA: Genome sequencing reveals fine scale diversification and reticulation history during speciation in Sus. Genome Biol 2013, 14:R107. BioMed Central Full Text
• [15]Groves CP, Grubb P: The Eurasian Suids Sus and Babyrousa. In Status Survey and Conservation Action Plan: Pigs, Peccaries and Hippos. Chapter 5.1. Edited by Oliver WLR. Gland, Switzerland: IUCN; 1993:107-111.
• [16]Larson G, Cucchi T, Dobney K: Genetic Aspects of Pig Domestication. In The Genetics of the Pig. Chapter 2. 2nd edition. Edited by Rothschild MF, Ruvinsky A. Oxfordshire: CAB International; 2011:14-37.
• [17]Ramírez O, Ojeda A, Tomás A, Gallardo D, Huang LS, Folch JM, Clop A, Sánchez A, Badaoui B, Hanotte O, Galman-Omitogun O, Makuza SM, Soto H, Cadillo J, Kelly L, Cho IC, Yeghoyan S, Pérez-Enciso M, Amills M: Integrating Y-Chromosome, mitochondrial, and Autosomal data to analyze the origin of pig breeds. Mol Biol Evol 2009, 26:2061-2072.
• [18]Scandura M, Iacolina L, Crestanello B, Pecchioli E, Di Benedetto MF, Russo V, Davoli R, Apollonio M, Bertorelle G: Ancient vs. recent processes as factors shaping the genetic variation of the European wild boar: are the effects of the last glaciation still detectable? Mol Ecol 2008, 17:1745-1762.
• [19]Vilaça ST, Biosa D, Zachos F, Iacolina L, Kirschning J, Alves PC, Paule L, Gortazar C, Mamuris Z, Jedrzejewska B, Borowik T, Sidorovich VE, Kusak J, Costa S, Schley L, Hartl GB, Apollonio M, Bertorelle G, Scandura M: Mitochondrial phylogeography of the European wild boar: the effect of climate on genetic diversity and spatial lineage sorting across Europe. J Biogeogr 2014, 41:987-998.
• [20]Alexandri P, Triantafyllidis A, Papakostas S, Chatzinikos E, Platis P, Papageorgiou N, Larson G, Abatzopoulos TJ, Triantaphyllidis C: The Balkans and the colonization of Europe: the post-glacial range expansion of the wild boar, Sus scrofa. J Biogeogr 2012, 39:713-723.
• [21]Norton CJ: The current state of Korean paleoanthropology. J Hum Evol 2000, 38:803-825.
• [22]Kim YK, Hong YJ, Min MS, Kim KS, Kim YJ, Voloshina I, Myslenkov A, Smith GJD, Cuong ND, Tho HH, Han SH, Yang DH, Kim CB, Lee H: Genetic status of Asiatic black bear (Ursus thibetanus) reintroduced into South Korea based on mitochondrial DNA and microsatellite loci analysis. J Hered 2011, 102:165-174.
• [23]Shin T, Jin J, Lee C: Archaeological study of animal bones excavated from Cheju Kimnyungri cave site. Korean J Vet Res 1996, 36:757-761. (in Korean with English abstract)
• [24]Kim H-L, Kang C-H, Shin T-K: Comparative anatomical study on animal bones excavated from the Jongdal-ri shell mound archaeological site IV on Jeju Island. Korean J Vet Res 2002, 42:309-320. (in Korean with English abstract)
• [25]Caley P: Movements, activity patterns and habitat use of feral pigs (Sus scrofa) in a tropical habitat. Wildl Res 1997, 24:77-87.
• [26]Choi TY, Lee YS, Park CH: Home-range of wild boar, Sus scrofa living in the Jirisan National Park, Korea. J Ecol Field Biol 2006, 29:253-257. (in Korean with English abstract)
• [27]Han SH, Oh JG, Cho IC, Ko MS, Kim TW, Chang MH, Kim BS, Park SG, Oh HS: A molecular genetic analysis of the introduced wild boar species (Sus scrofa coreanus) on Mount Halla, Jeju Island, Korea. Kor J Env Eco 2011, 5:658-665. (in Korean with English abstract)
• [28]FAO: Swines. In Secondary Guidelines for Development of National Farm Animal Genetic Resources Management Plans. Measurement of Domestic Animal Diversity (MoDAD): Recommended Microsatellite Markers. Rome: FAO; 1998:19-24.
• [29]Kim KS, Stolz U, Miller NJ, Waits ER, Guillemaud T, Sumerford DV, Sappington TW: A core set of microsatellite markers for western corn rootworm (Coleoptera: Chrysomelidae) population genetics studies. Environ Entomol 2008, 37:293-300.
• [30]Park SDE: Trypanotolerance in West African cattle and the population genetic effects of selection. PhD thesis. Ireland: University of Dublin; 2001.
• [31]Hurlbert SH: The nonconcept of species diversity: a critique and alternative parameters. Ecology 1971, 52:577-586.
• [32]Goudet J: FSTAT(version 1.2): a computer program to calculate F-statistics. J Hered 1995, 86:485-486.
• [33]Rice WR: Analyzing tables of statistical tests. Evolution 1989, 43:223-225.
• [34]Wright S: Isolation by distance. Genetics 1943, 28:114-138.
• [35]Peakall R, Smouse PE: GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 2006, 6:288-295.
• [36]Ota T: DISPAN: genetic distance and phylogenetic analysis. University Park, Pennsylvania, USA: Pennsylvania State University; 1993.
• [37]Nei M, Tajima F, Tateno Y: Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 1983, 19:153-170.
• [38]Saitou N, Nei M: The neighbor-joining method: a new method for reconstructing phylogenetic tree. Mol Biol Evol 1987, 4:406-425.
• [39]Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959.