Abstract
The widespread occurrence of the wild boar Sus scrofa, its controversial role in natural communities, and its close relationship with humans make this animal an important and convenient subject for studying the history and evolution of natural communities. The territory of Central Asia has been poorly represented in mammalian phylogeographic studies, namely in the case of wild boars and domestic pigs. In this study, we provide new information on wild boar genetic diversity in Central Asia in terms of mitochondrial and Y-chromosome markers and compare the set of haplotypes observed in Uzbekistan and Kazakhstan with those from other parts of the species’ range. The wild boar population in Central Asia is characterized by high uniqueness of mitochondrial and Y-chromosome markers and high haplotype diversity (as compared to other Asian regions). A maternal lineage marker (mitochondrial-DNA control region) clearly places this species in the Asian clade, whereas a paternal lineage markers (AMELY + USP9) positions it closer to wild boars from the western clade. Thus, the molecular genetic data supported the existence of a regionally specific subspecies of the wild boar: S. s. nigripes Blanford, 1875. Median-joining network analysis showed that Central Asia may be a center of dispersal and formation of S. scrofa genetic lineages in North Asia.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated and/or analyzed during the current study are available in the GenBank database, https://www.ncbi.nlm.nih.gov, accession numbers OR239781-.OR239786 Raw data are available upon request.
References
Alexandri P, Triantafyllidis A, Papakostas S et al (2012) The Balkans and the colonization of Europe: The post-glacial range expansion of the wild boar, Sus scrofa. J Biogeogr 39:713–723. https://doi.org/10.1111/j.1365-2699.2011.02636.x
Ashrafzadeh MR, Rezaei HR, Khalilipour O, Kusza S (2018) 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. https://doi.org/10.1016/j.mambio.2018.04.001
Ballari SA, Barrios-García MN (2014) A review of wild boar Sus scrofa diet and factors affecting food selection in native and introduced ranges. Mamm Rev 44:124–134. https://doi.org/10.1111/mam.12015
Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Barrios-Garcia MN, Ballari SA (2012) Impact of wild boar (Sus scrofa) in its introduced and native range: a review. Biol Invasions 14:2283–2300. https://doi.org/10.1007/s10530-012-0229-6
Bykova EA, Esipov AV. (2006) Current condition of game ungulates of Uzbekistan. Selevinia 14:194–197.[In Russian with English summary]
Chindelevitch L, Hayati M, Poon AFY, Colijn C (2021) Network science inspires novel tree shape statistics. PLoS ONE 16:e0259877. https://doi.org/10.1371/journal.pone.0259877
Cho IC, Han SH, Fang M et al (2009) The robust phylogeny of Korean wild boar (Sus scrofa coreanus) using partial D-loop sequence of mtDNA. Mol Cells 28:423–430. https://doi.org/10.1007/s10059-009-0139-3
Choi SK, Kim KS, Ranyuk M et al (2020) Asia-wide phylogeography of wild boar (Sus scrofa) based on mitochondrial DNA and Y-chromosome: revising the migration routes of wild boar in Asia. PLoS ONE 15:1–17. https://doi.org/10.1371/journal.pone.0238049
Csardi G, Nepusz T (2006) The igraph software package for complex network research. Int J Complex Syst 1695:1–9
Danilkin A (2002) Pigs (Suidae). GEOS, Moscow ([In Russian with English summary])
Darriba D, Taboada GL, Doallo R, Posada D (2012) JModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
de Jong JF, Iacolina L, Prins HHT et al (2023) Spatial genetic structure of European wild boar, with inferences on late-Pleistocene and Holocene demographic history. Heredity 130:135–144. https://doi.org/10.1038/s41437-022-00587-1
Forster P, Torroni A, Renfrew C, Röhl A (2001) Phylogenetic star contraction applied to Asian and Papuan mtDNA evolution. Mol Biol Evol 18:1864–1881. https://doi.org/10.1093/oxfordjournals.molbev.a003728
Frantz AC, McDevitt AD, Pope LC et al (2014) Revisiting the phylogeography and demography of European badgers (Meles meles) based on broad sampling, multiple markers and simulations. Heredity 113:443–453. https://doi.org/10.1038/hdy.2014.45
Frantz LAF, Schraiber JG, Madsen O et al (2013) Genome sequencing reveals fine scale diversification and reticulation history during speciation in Sus. Genome Biol. https://doi.org/10.1186/gb-2013-14-9-r107
Fumagalli L, Taberlet P, Favre L, Hausser J (1996) Origin and evolution of homologous repeated sequences in the mitochondrial DNA control region of shrews. Mol Biol Evol 13:31–46. https://doi.org/10.1093/oxfordjournals.molbev.a025568
Genov PV (1999) A review of the cranial characteristics of wild boar (Sus scrofa Linnaeus 1758) with systematic conclusions. Mamm Rev 29:205–238
Ghivizzani SC, Mackay SLD, Madsen CS et al (1993) Transcribed heteroplasmic repeated sequences in the porcine mitochondrial DNA D-loop region. J Mol Evol 37:36–47. https://doi.org/10.1007/BF00170460
Groenen MAM, Archibald AL, Uenishi H et al (2012) Analyses of pig genomes provide insight into porcine demography and evolution. Nature 491:393–398. https://doi.org/10.1038/nature11622
Hasegawa M, Kishino H, Yano TA (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174
Iacolina L, Brajković V, Canu A et al (2016) Novel Y-chromosome short tandem repeats in Sus scrofa and their variation in European wild boar and domestic pig populations. Anim Genet 47:682–690. https://doi.org/10.1111/age.12483
Ishunin GI, Tetyukhin GF (1989) Veroyatniye puti obrazovaniya fauni mlekopitayuschikh na territorii Uzbekistana (Probable Formation Routes of the Mammalian Fauna in the Territory of Uzbekistan). Izdatelstvo “Fan” UzSSR, Tashkent [In Russian]
Kashkarov RD (2002) About mammals fauna (Carnivora and Artiodactyla) of Pskem river basin. Selevinia 10:150–158.[In Russian with English summary]
Keuling O, Podgórski T, Monaco A et al (2018) Eurasian wild boar Sus scrofa (Linnaeus, 1758). In: Meletti M, Meijaard E (eds) Ecology, conservation and management of wild pigs and peccaries. Cambridge University Press, New York, NY., pp 202–233
Knyazev SP, Nikitin SV (2004) Phylogenesis and taxonomic relationships between intraspecies forms of Sus scrofa (Suidae). Zool Zhurnal 83:105–118 ([In Russian with English summary])
Kostyunina O, Traspov A, Economov A et al (2022) Genetic diversity, admixture and analysis of homozygous-by-descent (HBD) segments of Russian wild boar. Biology (basel) 11:203. https://doi.org/10.3390/biology11020203
Kusza S, Podgórski T, Scandura M et al (2014) Contemporary genetic structure, phylogeography and past demographic processes of wild boar Sus scrofa population in Central and Eastern Europe. PLoS ONE 9:e91401. https://doi.org/10.1371/journal.pone.0091401
Larson G, Cucchi T, Fujita M et al (2007) Phylogeny and ancient DNA of Sus provides insights into neolithic expansion in Island Southeast Asia and Oceania. Proc Natl Acad Sci USA 104:4834–4839. https://doi.org/10.1073/pnas.0607753104
Larson G, Dobney K, Albarella U et al (2005) Worldwide phylogeography of wild boar reveals multiple centers of pig domestication. Science 307:1618–1621. https://doi.org/10.1126/science.1106927
Larson G, Liu R, Zhao X et al (2010) Patterns of East Asian pig domestication, migration, and turnover revealed by modern and ancient DNA. Proc Natl Acad Sci USA 107:7686–7691. https://doi.org/10.1073/pnas.0912264107
Lee YS, Markov N, Argunov A et al (2016) Genetic diversity and phylogeography of Siberian roe deer, Capreolus pygargus, in central and peripheral populations. Ecol Evol 6:7286–7297. https://doi.org/10.1002/ece3.2458
Lin CS, Sun YL, Liu CY et al (1999) Complete nucleotide sequence of pig (Sus scrofa) mitochondrial genome and dating evolutionary divergence within Artiodactyla. Gene 236:107–114. https://doi.org/10.1016/S0378-1119(99)00247-4
Marchiori M, Latora V (2000) Harmony in the small-world. Physica A 285:539–546. https://doi.org/10.1016/S0378-4371(00)00311-3
Markov N, Economov A, Hjeljord O et al (2022a) The wild boar Sus scrofa in northern Eurasia: a review of range expansion history, current distribution, factors affecting the northern distributional limit, and management strategies. Mamm Rev 52:519–537. https://doi.org/10.1111/mam.12301
Markov NI, Ranyuk MN, Babaev EA et al (2022) Introduced, mixed, and peripheral: conservation of mitochondrial-DNA lineages in the wild boar (Sus scrofa L.) population in the Urals. Diversity (Basel) 14:916
Niedziałkowska M, Tarnowska E, Ligmanowska J et al (2021) Clear phylogeographic pattern and genetic structure of wild boar Sus scrofa population in Central and Eastern Europe. Sci Rep 11:9680. https://doi.org/10.1038/s41598-021-88991-1
Ottoni C, Flink LG, Evin A et al (2013) Pig domestication and human-mediated dispersal in western eurasia revealed through ancient DNA and geometric morphometrics. Mol Biol Evol 30:824–832. https://doi.org/10.1093/molbev/mss261
Pavlopoulos GA, Secrier M, Moschopoulos CN et al (2011) Using graph theory to analyze biological networks. BioData Min 4:10. https://doi.org/10.1186/1756-0381-4-10
Ramayo Y, Shemereteva IN, Pérez-Enciso M (2011) Mitochondrial DNA diversity in wild boar from the Primorsky Krai Region (East Russia). Anim Genet 42:96–99. https://doi.org/10.1111/j.1365-2052.2010.02074.x
Ramirez O, Ojeda A, Tomas A et al (2009) Integrating Y-Chromosome, mitochondrial, and autosomal data to analyze the origin of pig breeds. Mol Biol Evol 26:2061–2072. https://doi.org/10.1093/molbev/msp118
Randi E, Alves PC, Carranza J et al (2004) Phylogeography of roe deer (Capreolus capreolus) populations: the effects of historical genetic subdivisions and recent nonequilibrium dynamics. Mol Ecol 13:3071–3083. https://doi.org/10.1111/J.1365-294X.2004.02279.X
Ronquist F, Teslenko M, Van der Mark P et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC et al (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248
Tikhonov VN, Knyazev SP (1985) Immunogenetic traits in some forms of wild pigs of Europe, Asia, Africa and America. In: Davletova LV (ed) Morphology and genetics of wild boar. Nauka, Moscow, pp 3–16 ([In Russian])
Tikhonov VN, Troshina AI (1978) Introduction of two chromosomal translocations of Sus scrofa nigripes and Sus scrofa scrofa into the genome of Sus scrofa domestica. Theor Appl Genet 53:261–264. https://doi.org/10.1007/BF00280989
Troshina AI, Tikhonov VN (1985) Cytogenetic peculiarities of some wild pigs of Europe, Asia, Africa and America. In: Davletova LV (ed) Morphology and genetics of wild boar. Nauka, Moscow, pp 17–27 (In Russian)
Veličković N, Djan M, Ferreira E et al (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. https://doi.org/10.1111/jbi.12458
Vilaça ST, Biosa D, Zachos F et al (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. https://doi.org/10.1111/jbi.12268
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. https://doi.org/10.2108/zsj.20.1477
Wu GS, Yao YG, Qu KX et al (2007) Population phylogenomic analysis of mitochondrial DNA in wild boars and domestic pigs revealed multiple domestication events in East Asia. Genome Biol. https://doi.org/10.1186/gb-2007-8-11-r245
Funding
This study was funded by the Russian Foundation for Basic Research, project # 20–04-00234. The authors have no competing interests to declare that are relevant to the contents of this article.
Author information
Authors and Affiliations
Contributions
NM, MR, and VM processed the DNA samples, analyzed the data, and wrote the manuscript. NM, SN, EB, and AE organized the field trips, participated in the sample collection, and participated in draft preparation. All the authors reviewed and approved the final submission.
Corresponding author
Ethics declarations
Ethical approval
None of the animals was killed specifically for the purpose of this study. The wild boar is classified as a game animal in the countries involved in the sampling in this study, and all the wild boar specimens were donated by hunters with a hunting license in each country. The procedures involving the animal specimens were in compliance with the legal system in each country.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling Editor: J. Paul Grobler.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Markov, N.I., Bykova, E.A., Esipov, A.V. et al. Between the east and the west: genetic uniqueness of the Central-Asian wild boar (Sus scrofa) on the basis of maternal and paternal markers. Mamm Biol (2024). https://doi.org/10.1007/s42991-024-00411-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s42991-024-00411-9