Abstract
Genetic relationships between wild boar populations in the southern regions of Iran still remain unclear. Therefore in the present study our aim was filling this gap and providing preliminary knowledge about the phylogenetic status of Iranian wild boar based on two datasets of the mtDNA control region (the 402-bp and 605-bp segments as the first and second datasets, respectively). Altogether 1063 and 490 sequences were used in the shorter and longer sequences, respectively (29 own samples and 1034 and 461 Genbank sequences from previous studies in the first and second datasets, respectively). Our findings revealed that the wild boars living in Southern Iran belong to the previously described three clades: Asian, Near Eastern 1 (NE1) and Near Eastern 2 (NE2) clades. The NE1 and NE2 clades sympatrically occupy a wide range across the southeast to southwest of Iran, whereas the Asian clade is restricted to a small area in the southeastern part of Iran. Our results propose the existence of a contact zone between the Near Eastern clades and the Asian clade in the studied area. The fixation index (FST) and the analysis of molecular variance (AMOVA) demonstrated significant genetic structure among the identified clades. Some identified haplotypes have a wide distribution, which suggests that they are probably ancestral haplotypes or are likely to be a result of recent population expansion. Overall, current research demonstrates that Iranian wild boars have an important phylogenetic position among the others in the world. In other words, Iran is a very important region for addressing some of the topical questions about phylogenetic relationships among the Eurasian wild boar clades.
Similar content being viewed by others
References
Albarella, U., Dobney, K., Rowley-Conwy, P., 2009. Size and shape of the Eurasian wild boar (Sus scrofa), with a view to the reconstruction of its Holocene history. Environ. Archaeol. 14, 103–136.
Alexandri, P., Triantafyllidis, A., Papakostas, S., Chatzinikos, E., Platis, P., Papageorgiou, N., Larson, G., Abatzopoulos, T.J., Triantaphyllidis, C., 2012. The Balkans and the colonization of Europe: the post-glacial range expansion of the wild boar, Sus scrofa. J. Biogeogr. 39, 713–723.
Allen, M.S., Matisoo-Smith, E., Horsburgh, A., 2001. Pacific ‘Babes’: issues in the origins and dispersal of Pacific pigs and the potential of mitochondrial DNA analysis. Int. J. Osteoarchaeol. 11, 4–13.
Alves, E., Ovilo, C., Rodriguez, M., Silio, L., 2003. Mitochondrial DNA sequence variation and phylogenetic relationships among Iberian pigs and other domestic and wild pig populations. Anim. Genet. 34, 319–324.
Alves, P.C., Pinheiro, Í., Godinho, R., Vicente, J., Gortázar, C., Scandura, M., 2010. Genetic diversity of wild boar populations and domestic pig breeds (Sus scrofa) in South-western Europe. Biol. J. Linn. Soc. 101, 797–822.
Amici, A., Serrani, F., Adriani, S., 2010. Somatic variability in wild boar(Sus scrofa L.) in different areas of Central Italy. Ital. J. Anim. Sci. 9, 39–44.
Ashrafzadeh, M.R., Bordkhani, M., 2012. New morphometric data of wild boar (Sus scrofa Linnaeus, 1758) from the Minoo Island (Iran). Rom. J. Biol. -Zool. 57, 139–153.
Ashrafzadeh, M.R., Kaboli, M., Naghavi, M.R., 2016. Mitochondrial DNA analysis of Iranian brown bears (Ursus arctos) reveals new phylogeographic lineage. Mamm. Biol. 81, 1–9.
Bandelt, H.J., Forster, P., Röhl, A., 1999. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37–48.
Calvignac, S., Hughes, S., Hänni, C., 2009. Genetic diversity of endangered brown bear (Ursus arctos) populations at the crossroads of Europe, Asia and Africa. Divers. Distrib. 15, 742–750.
Clutton-Brock, J., 1987. A Natural History of Domesticated Mammals. Cambridge University Press, Cambridge, UK.
Dan, M., Veličković, N., Obreht, D., Kočiš, T.N., Marković, V., Stevanović, M., Beuković, M., 2013. Mitochondrial DNA control region variability in wild boars from west balkans. Genetika 45, 515–526.
Djamali, M., De Beaulieu, J.L., Miller, N.F., Andrieu-Ponel, V., Ponel, P., Lak, R., Sadeddin, N., Akhani, H., Fazeli, H., 2009. Vegetation history of the SE section of the Zagros Mountains during the last five millennia; a pollen record from the Maharlou Lake, Fars Province, Iran. Veg. Hist. Archaeobot. 18, 123–136.
Excoffier, L., Lischer, H.E., 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and WindowsMol. Ecol. Resour. 10, 564–567.
Fang, M., Berg, F., Ducos, A., Andersson, L., 2006. Mitochondrial haplotypes of European wild boars with 2n = 36 are closely related to those of European domestic pigs with 2n = 38. Anim. Genet. 37, 459–464.
Fonseca, C., 2004. Population Dynamics and Management of Wild Boar (Sus scrofa L.) in Central Portugal and Southeastern Poland. Ph.D. Thesis. University of Aveiro, Aveiro, Portugal.
Gallo Orsi, U., Macchi, E., Perrone, A., Durio, P., 2014. Biometric data and growth rates of a wild boar population living in the Italian Alps. J. Mt. Ecol. 3, 60–63.
Giuffra, E., Kijas, J., Amarger, V., Carlborg, Ö., Jeon, J.T., Andersson, L., 2000. The origin of the domestic pig: independent domestication and subsequent introgression. Genetics 154, 1785–1791.
Groves, C.P., 1983. Pigs East of the Wallace line. J. Soc. Océanistes 39, 105–119.
Herre, W., Röhrs, M., 1977. Zoological considerations on the origins of farming and domestication. In: Reed, C.A. (Ed.), Origins of Agriculture. The Hague, Chicago, pp. 245–279.
Huang, Y.F., Shi, X.W., Zhang, Y.P., 1999. Mitochondrial genetic variation in Chinese pigs and wild boars. Biochem. Genet. 37, 335–343.
Iacolina, L., Scandura, M., Bongi, P., Apollonio, M., 2009. Nonkin associations in wild boar social units. J. Mammal. 90, 666–674.
Karami, M., Mohammadi, H., Cheraghi, S., 2010. Present Distribution, Abundance and Problems of Wild Pig (Sus scrofa) in Iran, Wild Pig Conference, Florida: Science and Management.
Khalilzadeh, P., Rezaei, H.R., Fadakar, D., Serati, M., Aliabadian, M., Haile, J., Goshtasb, H., 2016. Contact zone of Asian and European wild boar at North West of Iran. PLoS One 11, e0159499.
Kijas, J., Andersson, L., 2001. A phylogenetic study of the origin of the domestic pig estimated from the near-complete mtDNA genome. J. Mol. Evol. 52, 302–308.
Kim, K.I., Lee,J.H., Li, K., Zhang, Y.P., Lee, S.S., Gongora, J., Moran, C., 2002. Phylogenetic relationships of Asian and European pig breeds determined by mitochondrial DNA D-loop sequence polymorphism. Anim. Genet. 33, 19–25.
Kusza, S., Podgórski, T., Scandura, M., Borowik, T., Jávor, A., Sidorovich, V.E., Bunevich, A.N., Kolesnikov, M., Jędrzejewska, B., 2014. Contemporary genetic structure, phylogeography and past demographic processes of wild boar Sus scrofa population in Central and Eastern Europe. PLoS One 9, e91401.
Larson, G., Albarella, U., Dobney, K., Rowley-Conwy, P., Schibler, J., Tresset, A., Vigne, J.D., Edwards, C.J., Schlumbaum, A., Dinu, A., 2007. Ancient DNA, pig domestication, and the spread of the Neolithic into Europe. Proc. Natl. Acad. Sci. U. S. A. 104, 15276–15281.
Larson, G., Dobney, K., Albarella, U., Fang, M., Matisoo-Smith, E., Robins, J., Lowden, S., Finlayson, H., Brand, T., Willerslev, E., 2005. Worldwide phylogeography of wild boar reveals multiple centers of pig domestication. Science 307, 1618–1621.
Lattuada, L., Quaglia, F., Iannelli, F., Gissi, C., Mantecca, P., Bacchetta, R., Polli, M., 2009. Mitochondrial DNA sequence variations in some Italian wild boar populations. J. Anim. Breed. Genet. 126, 154–163.
Lemel, J., Truvé, J., Söderberg, B., 2003. Variation in ranging and activity behaviour of European wild boar Sus scrofa in Sweden. Wildl. Biol. 9, 29–36.
Librado, P., Rozas, J., 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.
Luetkemeier, E.S., Sodhi, M., Schook, L.B., Malhi, R.S., 2010. Multiple Asian pig origins revealed through genomic analyses. Mol. Phylogenet. Evol. 54, 680–686.
Maselli, V., Rippa, D., de Luca, A., Larson, G., Wilkens, B., Linderholm, A., Masseti, M., Fulgione, D., 2016. Southern Italian wild boar population, hotspot of genetic diversity. Hystrix Ital. J. Mammal. 27 (2), https://doi.org/10.4404/hystrix-27.2-11489.
Massei, G., Genov, P.V., Staines, B.W., 1996. Diet, food availability and reproduction of wild boar in a Mediterranean coastal area. ActaTheriol. 41, 307–320.
Naderi, G., Kaboli, M., Koren, T., Karami, M., Zupan, S., Rezaei, H.R., Krystufek, B., 2014. Mitochondrial evidence uncovers a refugium forthe fat dormouse (Glis glis Linnaeus, 1766) in Hyrcanian forests of northern Iran. Mamm. Biol. 79, 202–207.
Noroozi, J., Akhani, H., Breckle, S.W., 2008. Biodiversity and phytogeography of the alpine flora of Iran. Biodivers. Conserv. 17, 493–521.
Nowak, R., Paradiso, J., 1999. Walker’s Mammals of the World. The Johns Hopkins University Press, Baltimore and London.
Oliver, W., Leus, K., 2008. Sus scrofa. In: IUCN 2008. IUCN Red List of Threatened Species. Version 2009.1, Available at: https://doi.org/www.iucnredlist.org.
Ottoni, C., Girdland Flink, L., Evin, A., Geörg, C., De Cupere, B., Van Neer, W., Bartosiewicz, L., Linderholm, A., Barnett, R., Peters, J., 2012. Pig domestication and human-mediated dispersal in western Eurasia revealed through ancient DNA and geometric morphometrics. Mol. Biol. Evol. 30, 824–832.
Peterson, A.T., 1992. Philopatry and genetic differentation in the Aphelocomajays (Corvidae). Biol. J. Linn. Soc. 47, 249–260.
Podgórski, T., Lusseau, D., Scandura, M., Sönnichsen, L., Jędrzejewska, B., 2014. Long-lasting, kin-directed female interactions in a spatially structured wild boar social network. PLoS One 9, e99875.
Posada, D., 2008. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25, 1253–1256.
Rajaei, S.H., Rödder, D., Weigand, A.M., Dambach, J., Raupach, M.J., Wägele, J.W., 2013. Quaternary refugia in southwestern Iran: insights from two sympatric moth species (Insecta, Lepidoptera). Org. Divers. Evol. 13, 409–423.
Ronquist, F., Huelsenbeck,J.P., 2003. MrBayes3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
Ruvinsky, A., Rothschild, M.F., 1998. Systematics and evolution of the pig. In: Genet. Pig., pp. 1–16.
Sagheb Talebi, K., Sajedi, T., Pourhashemi, M., 2013. Forests of Iran: A Treasure from the Past, a Hope forthe Future. Springer Science and Business Media, Dordrech, New York.
Scandura, M., Iacolina, L., Crestanello, B., Pecchioli, E., Di Benedetto, M.F., Russo, V., Davoli, R., Apollonio, M., Bertorelle, G., 2008. 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. 17, 1745–1762.
Spencer, P., Hampton, J., Lapidge, S., Mitchell, J., Lee, J., Pluske, J., 2006. assessment of the genetic diversity and structure within and among populations of wild pigs (Sus scrofa) from Australia and Papua New Guinea. J. Genet. 85, 63–66.
Spitz, F., Janeau, G., 1990. Spatial strategies: an attempt to classify daily movements of wild boar. ActaTheriol. 35, 129–149.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729.
Velickovic, N., Djan, M., Ferreira, E., Stergar, M., Obreht, D., Maletic, V., Fonseca, C., 2015. From north to south and back: the role of the Balkans and other southern peninsulas in the recolonization of Europe by wild boar. J. Biogeogr. 42, 716–728.
Velickovic, N., Ferreira, E., Djan, M., Ernst, M., Vidakovic, D.O., Monaco, A., Fonseca, C., 2016. Demographic history, current expansion and future management challenges of wild boar populations in the Balkans and Europe. Heredity 117, 348–357.
Vilaça, S.T., Biosa, D., Zachos, F., Iacolina, L., Kirschning, J., Alves, P.C., Paule, L., Gortazar, C., Mamuris, Z., Jędrzejewska, B., Borowik, T., 2014. Mitochondrial phylogeography of the European wild boar: the effect of climate on genetic diversity and spatial lineage sorting across Europe. J. Biogeogr. 41, 987–998.
Waits, L., Taberlet, P., Swenson, J.E., Sandegren, F., Franzen, R., 2000. Nuclear DNA microsatellite analysis of genetic diversity and gene flow in the Scandinavian brown bear (Ursus arctos). Mol. Ecol. 9, 421–431.
Watanobe, T., Ishiguro, N., Nakano, M., 2003. Phylogeography and population structure of the Japanese wild boar Sus scrofa leucomystax: mitochondrial DNA variation. Zool. Sci. 20, 1477–1489.
Weir, B.S., Cockerham, C.C., 1984. Estimating F-statistics forthe analysis of population structure. Evolution 38, 1358–1370.
West, B.C., Cooper, A.L., Armstrong, J.B., 2009. In: Jack, H. (Ed.), Managing Wild Pigs: A Technical Guide. Berryman Institute, Department ofWildland Resources, Utah State University, Logan, USA.
Wu, G.S., Yao, Y.G., Qu, K.X., Ding, Z.L., Li, H., Palanichamy, M.G., Duan, Z.Y., Li, N., Chen, Y.S., Zhang, Y.P., 2007. Population phylogenomic analysis of mitochondrial DNA in wild boars and domestic pigs revealed multiple domestication events in East Asia. Genome Biol. 8, R245.
Ziaie, H., 2008. A Field Guide to the Mammals of Iran, second ed. Iran Wildlife Center Press, Tehran.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ashrafzadeh, M.R., Rezaei, H.R., Khalilipour, O. et al. Genetic relationships of wild boars highlight the importance of Southern Iran in forming a comprehensive picture of the species’ phylogeography. Mamm Biol 92, 21–29 (2018). https://doi.org/10.1016/j.mambio.2018.04.001
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1016/j.mambio.2018.04.001