Skip to main content
SpringerLink
Log in

Genetic Diversity and Phylogenetic Relationships of Russian Pig Breeds Based on the Analysis of mtDNA D-Loop Polymorphism

  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

A decrease in the level of genetic diversity is one of the main genetic problems in pig breeding worldwide. In Russia, some local breeds are endangered because of their low number. A strong directional selection can lead to a decrease in the diversity in transboundary breeds. In this regard, the aim of our study was to estimate the genetic diversity and to establish phylogenetic relationships in nine pig breeds reared in Russia by the analysis of mtDNA D-loop sequences. In total, 273 nucleotide sequences of mtDNA D-loop were sequenced in pigs of the following breeds: Breit, Kemerovo, Livni, Murom, Urzhum, Mangalitsa, Large White, Landrace, and Duroc. In the entire sample, 84 haplotypes, including 55 in local and 29 in transboundary breeds, and 104 variable sites were identified. Local breeds were characterized by a lower average number of nucleotide differences between the haplotypes than transboundary ones (K = 6.272 and K = 9.934). Of the studied pigs, 78.8% belonged to the haplogroup E; haplogroups D (20.5%) and A (0.7%) were found less frequently. The AMOVA analysis demonstrated that 43.88% of total genetic variability was due to the differences between the studied breeds. The analysis of the median network structure demonstrated that the Kemerovo breed was the most differentiated among local breeds, while the Mangalitsa breed entered the cluster of transboundary breeds owing to its European origin. The results obtained can be useful monitoring the genetic diversity in transboundary breeds, as well as for developing evidence-based programs for local pig breed conservation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

REFERENCES

  1. Song, R., Wang, Yu., Wang, Ya., and Zhao, J., Base editing in pigs for precision breeding, Front. Agr. Sci. Eng., 2020, vol. 7, no. 2, pp. 161—170. https://doi.org/10.15302/J-FASE-2019308

    Article  Google Scholar 

  2. Park, H.-S., Min, B., and Oh, S.-H., Research trends in outdoor pig production—a review, Asian-Australas. J. Anim. Sci., 2017, vol. 30, no. 9, pp. 1207—1214. https://doi.org/10.5713/ajas.17.0330

    Article  PubMed  PubMed Central  Google Scholar 

  3. Thi, L., Huyen, T., Roessler, R., et al., Impact of the Use of Exotic Compared to Local Pig Breeds on Socio-Economic Development and Biodiversity in Vietnam, Stuttgart: Grauer, 2005.

    Google Scholar 

  4. Amills, M., Clop, A., Ramírez, O., and Pérez-Enciso, M., Origin and genetic diversity of pig breeds, Encyclopedia of Life Sciences, Chichester: Wiley, 2010, pp. 1—10. https://doi.org/10.1002/9780470015902.a0022884.

  5. Biscarini, F., Nicolazzi, E.L., Stella, A., et al., Challenges and opportunities in genetic improvement of local livestock breeds, Front. Genet., 2015, vol. 6, no. 33. https://doi.org/10.3389/fgene.2015.00033

  6. Poklukar, K., Čandek-Potokar, M., Batorek Lukač, N., et al., Lipid deposition and metabolism in local and modern pig breeds: a review, Animals, 2020, vol. 10, p. 424. https://doi.org/10.3390/ani10030424

    Article  PubMed Central  Google Scholar 

  7. Ernst, L.K., Dmitriev, N.G., and Paronyan, I.A., Genetic Resources of Farm Animals in Russia and Neighboring Countries, Vserossiiskii Nauchno-Issledovatel’skii Institut Genetiki i Razvedeniya Sel’skokhozyaystvennykh Zhivotnykh, 1994.

    Google Scholar 

  8. Koziner, A.B. and Shtakelberg, E.R., Animal Genetic Resources of the USSR, Rome: FAO and UNEP, 1989.

    Google Scholar 

  9. Traspov, A., Deng, W., Kostyunina, O., et al., Population structure and genome characterization of local pig breeds in Russia, Belorussia, Kazakhstan and Ukraine, Genet. Sel. Evol., 2016, vol. 16. https://doi.org/10.1186/s12711-016-0196-y

  10. FAO. http://www.fao.org/dad-is/data/ru/. Accessed November 2, 2021.

  11. Fang, M. and Andersson, L., Mitochondrial diversity in European and Chinese pigs is consistent with population expansions that occurred prior to domestication, Proc. Biol. Sci., 2006, vol. 273, pp. 1803—1810. https://doi.org/10.1098/rspb.2006.3514

    Article  PubMed  PubMed Central  Google Scholar 

  12. Hammond, K. and Leitch, H.W., Genetic resources and the global programme for their management, in The Genetics of the Pig, Rothschild, M.F. and Ruvinsky, A., Eds., Wallingford: CABI, 1998, pp. 405—425.

    Google Scholar 

  13. Woelders, H., Zuidberg, C.A., and Hiemstra, S.J., Animal genetic resources conservation in the Netherlands and Europe: poultry perspective, Poult. Sci., 2005, vol. 85, pp. 216—222. https://doi.org/10.1093/ps/85.2.216

    Article  Google Scholar 

  14. Zhang, J., Jiao, T., and Zhao, S., Genetic diversity in the mitochondrial DNA D-loop region of global swine (Sus scrofa) populations, Biochem. Biophys. Res. Commun., 2016, vol. 473, pp. 814—820. https://doi.org/10.1016/j.bbrc.2016.03.125

    Article  CAS  PubMed  Google Scholar 

  15. Nguyen, H.D., Bui, T.A., Nguyen, P.T., et al., The complete mitochondrial genome sequence of the indigenous I pig (Sus scrofa) in Vietnam, Asian-Australas. J. Anim. Sci., 2017, vol. 30, no. 7, pp. 930—937. https://doi.org/10.5713/ajas.16.0608

    Article  CAS  PubMed  Google Scholar 

  16. Giuffra, E., Kijas, J.M., Amarger, V., et al., The origin of the domestic pig: independent domestication and subsequent introgression, Genetics, 2000, vol. 154, pp. 1785—1791. https://doi.org/10.1093/genetics/154.4.1785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Larson, G., Dobney, K., Albarella, U., et al., Worldwide phylogeography of wild boar reveals multiple centers of pig domestication, Science, 2005, vol. 307, pp. 1618—1621. https://doi.org/10.1126/science.1106927

    Article  CAS  PubMed  Google Scholar 

  18. Wu, G.S., Yao, Y.G., Qu, K.X., et al., Population phylogenomic analysis of mitochondrial DNA in wild boars and domestic pigs revealed multiple domestication events in East Asia, Genome Biol., 2007, vol. 8, no. 11, p. 245. https://doi.org/10.1186/gb-2007-8-11-r245

    Article  CAS  Google Scholar 

  19. Ge, Q., Gao, C., Cai, Y., et al., Evaluating genetic diversity and identifying priority conservation for seven Tibetan pig populations in China based on the mtDNA D-loop, Asian-Australas. J. Anim. Sci., 2020, vol. 33, no. 12, pp. 1905—1911. https://doi.org/10.5713/ajas.19.0752

    Article  PubMed  PubMed Central  Google Scholar 

  20. Laval, G., Iannuccelli, N., Legault, C., et al., Genetic diversity of eleven European pig breeds, Genet. Sel. Evol., 2000, vol. 32, no. 2, pp. 187—203. https://doi.org/10.1186/1297-9686-32-2-187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Ji, Y.-Q., Wu, D.-D., Wu, G.-S., et al., 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, vol. 6, no. 10, e26416. https://doi.org/10.1371/journal.pone.0026416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Quan, J., Gao, C., Cai, Y., et al., Population genetics assessment model reveals priority protection of genetic resources in native pig breeds in China, Global Ecol. Conserv., 2020, vol. 21. https://doi.org/10.1016/j.gecco.2019.e00829

  23. BLAST. https://blast.ncbi.nlm.nih.gov/Blast.cgi. Accessed March 1, 2021.

  24. Edgar, R.C., MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Res., 2004, vol. 32, pp. 1792—1797. https://doi.org/10.1093/nar/gkh340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Kumar, S., Stecher, G., and Tamura, K., MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets, Mol. Biol. Evol., 2016, vol. 33, no. 7, pp. 1870—1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Castresana, J., Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis, Mol. Biol. Evol., 2000, vol. 17, pp. 540—552. https://doi.org/10.1093/oxfordjournals.molbev.a026334

    Article  CAS  PubMed  Google Scholar 

  27. Peng, M.-S., Fan, L., Shi, N.-N., et al., DomeTree: a canonical toolkit for mitochondrial DNA analyses in domesticated animals, Mol. Ecol. Resour., 2015, vol. 15. https://doi.org/10.1111/1755-0998.12386

  28. Tajima, F., Statistical method for testing the neutral mutation hypothesis by DNA polymorphism, Genetics, 1989, vol. 123, pp. 585—595. https://doi.org/10.1093/genetics/123.3.585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Fu, Y.-X., Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection, Genet. Soc. Am., 1997, vol. 147, pp. 915—925. https://doi.org/10.1093/genetics/147.2.915

    Article  CAS  Google Scholar 

  30. Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J.C., et al., DnaSP 6: DNA sequence polymorphism analysis of large data sets, Mol. Biol. Evol., 2017, vol. 34, pp. 3299—3302. https://doi.org/10.1093/molbev/msx248

    Article  CAS  PubMed  Google Scholar 

  31. Rogers, A.R. and Harpending, H., Population growth makes waves in the distribution of pairwise genetic differences, Mol. Biol. Evol., 1992, vol. 9, pp. 552—569. https://doi.org/10.1093/oxfordjournals.molbev.a040727

    Article  CAS  PubMed  Google Scholar 

  32. Wickham, H., Ggplot2: Elegant Graphics for Data Analysis, New York: Springer-Verlag, 2009.

    Book  Google Scholar 

  33. Excoffier, L. and Lischer, H.E.L., Arlequin Suite ver. 3.5: a new series of programs to perform population genetics analyses under Linux and Windows, Mol. Ecol. Resour., 2010, vol. 10, pp. 564—567. https://doi.org/10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  34. Bandelt, H.J., Forster, P., and Röhl, A., Median-joining networks for inferring intraspecific phylogenies, Mol. Biol. Evol., 1999, vol. 16, pp. 37—48. https://doi.org/10.1093/oxfordjournals.molbev.a026036

    Article  CAS  PubMed  Google Scholar 

  35. Leigh, N., Georgiev, I., Boeker, T., et al., Nuclear star cluster formation in energy—space, Mon. Not. R. Astron. Soc., 2015, vol. 451, no. 1, pp. 859—869. https://doi.org/10.1093/mnras/stv1012

    Article  Google Scholar 

  36. Lanfear, R., Frandsen, P.B., Wright, A.M., et al., PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses, Mol. Biol. Evol., 2017, vol. 34, pp. 772—773. https://doi.org/10.1093/molbev/msw260

    Article  CAS  PubMed  Google Scholar 

  37. Akaike, H., A new look at statistical model identification, IEEE Trans Auto Control, 1974, vol. 19, pp. 716—723. https://doi.org/10.1109/TAC.1974.1100705

    Article  Google Scholar 

  38. Huson, D. and Kloepper, T., Beyond galled trees—decomposition and computation of galled networks, Eleventh Annual International Conference on Research in Computational Molecular Biology, Oakland, CA, 2007. https://doi.org/10.1007/978-3-540-71681-5_15.

  39. Kharzinova, V.R. and Zinovieva, N.A., The pattern of genetic diversity of different breeds of pigs based on microsatellite analysis, Vavilov J. Genet. Breed., 2020, vol. 24, no. 7, pp. 747—754. https://doi.org/10.18699/VJ20.669

    Article  CAS  Google Scholar 

  40. Kharzinova, V.R., Kostyunina, O.V., Karpushkina, T.V., et al., The study of the population structure and genetic diversity of Hungarian Mangalica breed of pigs based on microsatellites analysis, Agrar. Bull. Urale, 2019, vol. 186, no. 7, pp. 77—81. https://doi.org/10.32417/article_5d52b081b3e348.43320197

    Article  Google Scholar 

  41. Balatsky, V.N., Saienko, A.M., Pena, R.N., et al., Genetic diversity of pig breeds on ten production quantitative traits loci, Cytol. Genet., 2015, vol. 49, pp. 299—307. https://doi.org/10.3103/S0095452715050023

    Article  Google Scholar 

  42. Kharzinova, V.R., Kostyunina, O.V., and Zinovieva, N.A., Comparative characterization of the allele pool of local pig breeds based on microsatellite analysis, Pig Breed., 2017, vol. 1, pp. 5—7.

    Google Scholar 

  43. Getmantseva, L., Bakoev, S., Bakoev, N., et al., Mitochondrial DNA diversity in Large White pigs in Russia, Animals, 2020, vol. 10, p. 1365. https://doi.org/10.3390/ani10081365

    Article  PubMed Central  Google Scholar 

  44. Wang, C., Chen, Y., Han, J., et al., Mitochondrial DNA diversity and origin of indigenous pigs in South China and their contribution to western modern pig breeds, J. Integr. Agric., 2019, vol. 18, no. 10, pp. 2338—2350. https://doi.org/10.1016/s2095-3119(19)62731-0

    Article  CAS  Google Scholar 

  45. Ramírez, O., Ojeda, A., Tomàs, A., et al., Integrating Y-chromosome, mitochondrial, and autosomal data to analyze the origin of pig breeds, Mol. Biol. Evol., 2009, vol. 26, no. 9, pp. 2061—2072. https://doi.org/10.1093/molbev/msp118

    Article  CAS  PubMed  Google Scholar 

  46. Ajibike, A.B., Ilori, B.M., Akinola, O., et al., Assessing the genetic diversity of South-western Nigerian indigenous pig (Sus scorfa) using mitochondrial DNA D-loop sequence, Niger. J. Anim. Sci., 2020, vol. 22, pp. 1—9.

    Google Scholar 

  47. Goodall-Copestake, W., Tarling, G., and Murphy, E., On the comparison of population-level estimates of haplotype and nucleotide diversity: a case study using the gene cox1 in animals, Heredity, 2012, vol. 109, pp. 50—56. https://doi.org/10.1038/hdy.2012.12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Nei, M. and Tajima, F., DNA polymorphism detectable by restriction endonucleases, Genetics, 1981, vol. 97, p. 145. https://doi.org/10.1093/genetics/97.1.145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Thompson, J.D., Gibson, T.J., Plewniak, F., et al., The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools, Nucleic Acids Res., 1997, vol. 25, pp. 4876—4882. https://doi.org/10.1093/NAR/25.24.4876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Zhang, J., Yang, B., Wen, X., and Sun, G., Genetic variation and relationships in the mitochondrial DNA D-loop region of Qinghai indigenous and commercial pig breeds, Cell Mol. Biol. Lett., 2018, vol. 3, pp. 23—31. https://doi.org/10.1186/s11658-018-0097-x

    Article  Google Scholar 

  51. Tsai, T.S., Rajasekar, S., and John, J.S.St., The relationship between mitochondrial DNA haplotype and the reproductive capacity of domestic pigs (Sus scrofa domesticus), BMC Genet., 2016, vol. 17, р. 67.https://doi.org/10.1186/s12863-016-0375-4

  52. Collingbourne, S.J., Conservation genetics of traditional and commercial pig breeds, and evaluation of their crossbreeding potential for productivity improvement, PhD Thesis, Univ. Essex, 2019.

  53. Moon, K.-H., Nakanishi, M., Futagami, Y., and Kashiwadani, H., Studies on Cambodian species of Graphidaceae (Ostropales, Ascomycota): II, J. Jpn. Bot., 2015, vol. 90, no. 2, pp. 98—102.

    Google Scholar 

  54. Avise, J.C., Phylogeography: The History and Formation of Species, Cambridge, MA, 2000. https://doi.org/10.5860/choice.37-5647.

  55. Kim, T.H., Kim, K.S., and Choi, B.H., Genetic structure of pig breeds from Korea and China using microsatellite loci analysis, J. Anim. Sci., 2005, vol. 83, pp. 2255—2263. https://doi.org/10.2527/2005.83102255X

    Article  CAS  PubMed  Google Scholar 

  56. Kim, K.S., Yeo, J.S., and Kim, J.W., Assessment of genetic diversity of Korean native pig (Sus scrofa) using AFLP markers, Gen. Genet. Syst., 2002, vol. 77, pp. 361—368. https://doi.org/10.1266/GGS.77.361

    Article  CAS  Google Scholar 

  57. Li, K.Y., Chen, C., Moran, B.F., et al., Analysis of diversity and genetic relationships between four Chinese indigenous pig breeds and one Australian commercial pig breed, Anim. Genet., 2000, vol. 31, pp. 322—325. https://doi.org/10.1046/j.1365-2052.2000.00649.x

    Article  CAS  PubMed  Google Scholar 

  58. Sundari, S., Chanthran, D., Lim, P.-E., et al., Genetic diversity and population structure of Terapon jarbua (Forskål, 1775) (Teleostei, Terapontidae) in Malaysian waters, ZooKeys, 2020, vol. 911, pp. 139—160. https://doi.org/10.3897/zookeys.911.39222

    Article  Google Scholar 

  59. Stajich, J. and Hahn, M.W., Disentangling the effects of demography and selection in human history, Mol. Biol. Evol., 2004, vol. 22, pp. 63—73. https://doi.org/10.1093/MOLBEV/MSH252

    Article  PubMed  Google Scholar 

  60. Alexandrino, J., Arntzen, J.W., and Ferrand, N., Nested clade analysis and the genetic evidence for population expansion in the phylogeography of the golden-striped salamander, Chioglossa lusitanica (Amphibia: Urodela), Heredity, 2002, vol. 88, pp. 66—74. https://doi.org/10.1038/sj.hdy.6800010

    Article  CAS  PubMed  Google Scholar 

  61. Li, D., Wei, H., Zhang, Z., et al., Oriental reed warbler (Acrocephalus orientalis) nest defense behaviour to-wards brood parasites and nest predators, Behaviour, 2015. https://doi.org/10.1163/1568539X-00003295

Download references

ACKNOWLEDGMENTS

During the study, the equipment of the Center for Collective Use Bioresources and Bioengineering of Agricultural Animals of the Ernst Federal Research Center for Animal Husbandry was used.

Funding

The work was financially supported by the Ministry of Science and Higher Education of the Russian Federation, grant no. 075-15-2021-1037 (internal no. 15.BRC.21.0001).

Author information

Authors and Affiliations

  1. Ernst Federal Research Center for Animal Husbandry, 142132, Dubrovitsy, Moscow oblast, Russia

    V. R. Kharzinova, N. A. Akopyan, A. V. Dotsev, T. E. Deniskova, A. A. Sermyagin, T. V. Karpushkina, A. D. Solovieva & N. A. Zinovieva

  2. Department of Animal Breeding and Genetics, University of Veterinary Medicine (VMU), A-1210, Vienna, Austria

    G. Brem

Authors
  1. V. R. Kharzinova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. A. Akopyan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. V. Dotsev
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T. E. Deniskova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. A. Sermyagin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. T. V. Karpushkina
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. A. D. Solovieva
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. G. Brem
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. N. A. Zinovieva
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to V. R. Kharzinova or N. A. Zinovieva.

Ethics declarations

Conflict of interest. The authors declare that they have no conflicts of interest.

Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Translated by A. Barkhash

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kharzinova, V.R., Akopyan, N.A., Dotsev, A.V. et al. Genetic Diversity and Phylogenetic Relationships of Russian Pig Breeds Based on the Analysis of mtDNA D-Loop Polymorphism. Russ J Genet 58, 944–954 (2022). https://doi.org/10.1134/S102279542208004X

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S102279542208004X

Keywords:

Search

Navigation