Clear phylogeographic pattern and genetic structure of wild boar Sus scrofa population in Central and Eastern Europe
Language English Country England, Great Britain Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
33958636
PubMed Central
PMC8102581
DOI
10.1038/s41598-021-88991-1
PII: 10.1038/s41598-021-88991-1
Knihovny.cz E-resources
- MeSH
- Demography MeSH
- Phylogeography * MeSH
- Genetic Variation MeSH
- Genome, Mitochondrial MeSH
- Sus scrofa classification genetics MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Europe MeSH
The wild boar Sus scrofa is one of the widely spread ungulate species in Europe, yet the origin and genetic structure of the population inhabiting Central and Eastern Europe are not well recognized. We analysed 101 newly obtained sequences of complete mtDNA genomes and 548 D-loop sequences of the species and combined them with previously published data. We identified five phylogenetic clades in Europe with clear phylogeographic pattern. Two of them occurred mainly in western and central part of the continent, while the range of the third clade covered North-Eastern, Central and South-Eastern Europe. The two other clades had rather restricted distribution. In Central Europe, we identified a contact zone of three mtDNA clades. Population genetic structure reflected clear phylogeographic pattern of wild boar in this part of Europe. The contribution of lineages originating from the southern (Dinaric-Balkan) and eastern (northern cost of the Black Sea) areas to the observed phylogeographic pattern of the species in Central and Eastern Europe was larger than those from the regions located in southern France, Iberian, and Italian Peninsulas. The present work was the first mitogenomic analysis conducted in Central and Eastern Europe to study genetic diversity and structure of wild boar population.
Centre for Agrar Genomics and Biotechnology University of Debrecen Debrecen Hungary
Facultatea de Silvicultura Universitatea Stefan Cel Mare Suceava Suceava Romania
Kyiv Zoological Park of National Importance Kyiv Ukraine
Mammal Research Institute Polish Academy of Sciences Białowieża Poland
State National Park Belovezhskaya Pushcha Brest Oblast Kamenec Raion Kamenyuki Belarus
See more in PubMed
Keuling, O. & Leus, K. Sus scrofa. The IUCN Red List of Threatened Species 2019: e.T41775A44141833. 10.2305/IUCN.UK.2019-3.RLTS.T41775A44141833.en. Downloaded on 26 Oct 2020. (2019)
Larson G, et al. Worldwide phylogeography of wild boar reveals multiple centers of pig domestication. Science. 2005;307:1618–1621. doi: 10.1126/science.1106927. PubMed DOI
Choi SK, et al. 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. 2020;15:e0238049. doi: 10.1371/journal.pone.0238049. PubMed DOI PMC
Borowik T, Cornulier T, Jędrzejewska B. Environmental factors shaping ungulate abundances in Poland. Acta Theriol. 2013;58:403–413. doi: 10.1007/s13364-013-0153-x. PubMed DOI PMC
Scandura M, et al. 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. doi: 10.1111/j.1365-294X.2008.03703.x. PubMed DOI
Larson G, et al. 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. doi: 10.1073/pnas.0912264107. PubMed DOI PMC
Iacolina L, et al. Hotspots of recent hybridization between pigs and wild boars in Europe. Sci. Rep. 2018;8:17372. doi: 10.1038/s41598-018-35865-8. PubMed DOI PMC
Jędrzejewska B, Jędrzejewski W, Bunevich AN, Miłkowski L, Krasiński ZA. Factors shaping population densities and increase rates of ungulates in Białowieża Primeval Forest (Poland and Belarus) in the 19th and 20th centuries. Acta Theriol. 1997;42:399–451. doi: 10.4098/AT.arch.97-39. DOI
Apollonio M, Anderson R, Putman R. European Ungulates and Their Management in the 21st Century. Cambridge: Cambridge University Press; 2010.
Okarma H, et al. The roles of predation, snow cover, acorn crop, and man-related factors on ungulate mortality in Białowieża Primeval Forest, Poland. Acta Theriol. 1995;40:197–217. doi: 10.4098/AT.arch.95-20. DOI
Melis C, Szafrańska PA, Jędrzejewska B, Bartoń K. Biogeographical variation in the population density of wild boar (Sus scrofa) in western Eurasia. J. Biogeogr. 2006;33:803–811. doi: 10.1111/j.1365-2699.2006.01434.x. DOI
Dellicour S, et al. Unravelling the dispersal dynamics and ecological drivers of the African swine fever outbreak in Belgium. J. Appl. Ecol. 2020;57:1619–1629. doi: 10.1111/1365-2664.13649. DOI
Wang T, Sun Y, Qiu H-J. African swine fever: An unprecedented disaster and challenge to China. Infect. Dis. Poverty. 2018;7:111. doi: 10.1186/s40249-018-0495-3. PubMed DOI PMC
Schulz K, Conraths FJ, Blome S, Staubach C, Sauter-Louis C. African swine fever: Fast and furious or slow and steady? Viruses. 2019 doi: 10.3390/v11090866. PubMed DOI PMC
Blome S, Franzke K, Beer M. African swine fever: A review of current knowledge. Virus Res. 2020;287:198099. doi: 10.1016/j.virusres.2020.198099. PubMed DOI
Morelle K, et al. Disease-induced mortality outweighs hunting in causing wild boar population crash after african swine fever outbreak. Front. Vet. Sci. 2020 doi: 10.3389/fvets.2020.00378. PubMed DOI PMC
Vicente J, et al. Science-based wildlife disease response. Science. 2019;364:943–944. doi: 10.1126/science.aax4310. PubMed DOI
Schulz K, et al. Epidemiological evaluation of Latvian control measures for African swine fever in wild boar on the basis of surveillance data. Sci. Rep. 2019;9:4189. doi: 10.1038/s41598-019-40962-3. PubMed DOI PMC
Veličković N, et al. Demographic history, current expansion and future management challenges of wild boar populations in the Balkans and Europe. Heredity. 2016;117:348–357. doi: 10.1038/hdy.2016.53. PubMed DOI PMC
Khalilzadeh P, et al. Contact Zone of Asian and European Wild Boar at North West of Iran. PLoS ONE. 2016;11:e0159499. doi: 10.1371/journal.pone.0159499. PubMed DOI PMC
Frantz LAF, et al. Ancient pigs reveal a near-complete genomic turnover following their introduction to Europe. Proc. Natl. Acad. Sci. USA. 2019;116:17231. doi: 10.1073/pnas.1901169116. PubMed DOI PMC
Larson G, et al. Ancient DNA, pig domestication, and the spread of the Neolithic into Europe. Proc. Natl. Acad. Sci. USA. 2007;104:15276. doi: 10.1073/pnas.0703411104. PubMed DOI PMC
Scandura M, Iacolina L, Apollonio M. Genetic diversity in the European wild boar Sus scrofa: Phylogeography, population structure and wild x domestic hybridization. Mamm. Rev. 2011;41:125–137. doi: 10.1111/j.1365-2907.2010.00182.x. DOI
Alexandri P, et al. The Balkans and the colonization of Europe: The post-glacial range expansion of the wild boar, Sus scrofa. J. Biogeogr. 2012;39:713–723. doi: 10.1111/j.1365-2699.2011.02636.x. DOI
Veličković N, et al. 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. 2015;42:716–728. doi: 10.1111/jbi.12458. DOI
Khederzadeh S, et al. Maternal genomic variability of the wild boar (Sus scrofa) reveals the uniqueness of East-Caucasian and Central Italian populations. Ecol. Evol. 2019;9:9467–9478. doi: 10.1002/ece3.5415. PubMed DOI PMC
Kusza S, et al. Contemporary genetic structure, phylogeography and past demographic processes of Wild Boar Sus scrofa Population in Central and Eastern Europe. PLoS ONE. 2014;9:e91401. doi: 10.1371/journal.pone.0091401. PubMed DOI PMC
Tarnowska E, et al. Spatial distribution of the Carpathian and Eastern mtDNA lineages of the bank vole in their contact zone relates to environmental conditions. Biol. J. Linn. Soc. 2016 doi: 10.1111/bij.12764. DOI
Korbut Z, Rusin M, Neumann K, Banaszek A. Filling the gap: the common hamster, Cricetus cricetus, phylogeography: A case study of Ukraine as potential refugial area. Folia Zool. 2019;68:48–58. doi: 10.25225/fozo.068.2019. DOI
Niedziałkowska M. Phylogeography of European moose (Alces alces) based on contemporary mtDNA data and archaeological records. Mamm. Biol. 2017;84:35–43. doi: 10.1016/j.mambio.2017.01.004. DOI
Maselli V, et al. Southern Italian wild boar population, hotspot of genetic diversity. Hystrix. 2016;27:137–144. doi: 10.4404/hystrix-27.2-11489. DOI
Niedziałkowska M, et al. Molecular biogeography of red deer Cervus elaphus from eastern Europe: Insights from mitochondrial DNA sequences. Acta Theriol. 2011;56:1–12. doi: 10.1007/s13364-010-0002-0. PubMed DOI PMC
Niedzialkowska M, et al. Spatial structure in European moose (Alces alces): Genetic data reveal a complex population history. J. Biogeogr. 2014;41:2173–2184. doi: 10.1111/jbi.12362. DOI
Stojak J, Tarnowska E. Polish suture zone as the goblet of truth in post-glacial history of mammals in Europe. Mamm. Res. 2019;64:463–475. doi: 10.1007/s13364-019-00433-6. DOI
Sommer RS, Nadachowski A. Glacial refugia of mammals in Europe: evidence from fossil records. Mamm. Rev. 2006;36:251–265. doi: 10.1111/j.1365-2907.2006.00093.x. DOI
Vilaça ST, et al. 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. doi: 10.1111/jbi.12268. DOI
Markova, A. et al. Evolution of European Ecosystems during Pleistocene–Holocene Transition (24–8 Kyr BP). (2008).
Niedziałkowska M, et al. Winter temperature and forest cover have shaped red deer distribution in Europe and the Ural Mountains since the Late Pleistocene. J. Biogeogr. 2020 doi: 10.1111/jbi.13989. DOI
Hewitt GM. Post-glacial re-colonization of European biota. Biol. J. Lin. Soc. 1999;68:87–112. doi: 10.1006/bijl.1999.0332. DOI
Evin A, et al. Unravelling the complexity of domestication: A case study using morphometrics and ancient DNA analyses of archaeological pigs from Romania. Philos. Trans. R. Soc. B. 2015;370:20130616. doi: 10.1098/rstb.2013.0616. PubMed DOI PMC
Skog A, et al. Phylogeography of red deer (Cervus elaphus) in Europe. J. Biogeogr. 2009;36:66–77. doi: 10.1111/j.1365-2699.2008.01986.x. DOI
Meiri M, et al. Late-glacial recolonization and phylogeography of European red deer (Cervus elaphus L.) Mol. Ecol. 2013;22:4711–4722. doi: 10.1111/mec.12420. PubMed DOI
Doan K, et al. The history of Crimean red deer population and Cervus phylogeography in Eurasia. Zool. J. Linn. Soc. 2018;183:208–225. doi: 10.1093/zoolinnean/zlx065. DOI
Kijas JMH, Andersson L. A phylogenetic study of the origin of the domestic pig estimated from the near-complete mtDNA genome. J. Mol. Evol. 2001;52:302–308. doi: 10.1007/s002390010158. PubMed DOI
Jiang YN, et al. Interpopulation and intrapopulation maternal lineage genetics of the Lanyu pig (Sus scrofa) by analysis of mitochondrial cytochrome b and control region sequences1. J. Anim. Sci. 2008;86:2461–2470. doi: 10.2527/jas.2007-0049. PubMed DOI
Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–1574. doi: 10.1093/bioinformatics/btg180. PubMed DOI
Kumar S, Stecher G, Tamura K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 2016;33:1870–1874. doi: 10.1093/molbev/msw054. PubMed DOI PMC
Li H, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078–2079. doi: 10.1093/bioinformatics/btp352. PubMed DOI PMC
French N, et al. Evolution of Campylobacter species in New Zealand. In: Sheppard SK, Méric G, et al., editors. Campylobacter Ecology and Evolution. Caister Academic Press; 2014. pp. 221–240.
Rozas J, et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 2017;34:3299–3302. doi: 10.1093/molbev/msx248. PubMed DOI
Levins R. Evolution in Changing Environments. Princeton University Press; 1968.
Excoffier L, Lischer HEL. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 2010;10:564–567. doi: 10.1111/j.1755-0998.2010.02847.x. PubMed DOI
Guillot G, Estoup A, Mortier F, Cosson JF. A spatial statistical model for landscape genetics. Genetics. 2005;170:1261–1280. doi: 10.1534/genetics.104.033803. PubMed DOI PMC
Guillot GILL, Mortier FRED, Estoup ARNA. Geneland: A computer package for landscape genetics. Mol. Ecol. Notes. 2005;5:712–715. doi: 10.1111/j.1471-8286.2005.01031.x. DOI
Guillot G. Inference of structure in subdivided populations at low levels of genetic differentiation: The correlated allele frequencies model revisited. Bioinformatics. 2008;24:2222–2228. doi: 10.1093/bioinformatics/btn419. PubMed DOI
Guillot G, Santos F, Estoup A. Analysing georeferenced population genetics data with Geneland: A new algorithm to deal with null alleles and a friendly graphical user interface. Bioinformatics. 2008;24:1406–1407. doi: 10.1093/bioinformatics/btn136. PubMed DOI
Guillot G, Santos F. Using AFLP markers and the Geneland program for the inference of population genetic structure. Mol. Ecol. Resour. 2010;10:1082–1084. doi: 10.1111/j.1755-0998.2010.02864.x. PubMed DOI
Guedj B, Guillot G. Estimating the location and shape of hybrid zones. Mol. Ecol. Resour. 2011;11:1119–1123. doi: 10.1111/j.1755-0998.2011.03045.x. PubMed DOI