Comparison of methods for evaluating genetic differentiation of populations by microsatellite markers

Comparative studies of eight methods for evaluation of genetic differences by microsatellite (STR) markers (11 loci) DNA were carried out using the example of seven breed samples (N = 84) of dairy cattle. The range of indicators of genetic diversity of samples was as follows: the number of alleles per locus 3.5-6.2, the number of effective alleles per locus – 2.4-4.3, the Shannon index – 0.95-1.56, the observed and expected heterozygosity – 0.56-0.97 and 0.53-0.75. Evaluation summary of genetic differentiation by group A methods (FST, GST, and GST(NEI)) were 13.4, 10.3, and 11.8% (pperm < 0.001); the differences between the estimates were statistically insignificant. Estimates by group B methods (G'ST(HED), G''ST(HED), DEST) were 36.4, 37.5 and 29.2% (pperm < 0.001); differences between the estimates were also statistically insignificant. Estimates obtained by group B methods were statistically significantly higher than those obtained by group A methods by almost 3 times. Methods of groups A, B, and C (GDN and uGDN) were used to calculate paired genetic distances in the samples. Despite significant dif-ferences in estimates, the Mantel test showed a high degree of correspondence of the genetic distance matrices (RM≥0.97; pperm < 0.001), which was manifested in the projections of genetic relations of breed samples on plane 1 and 2 of the principal coordinates. The first two principal coordinates explained 97-99% of STR variation in the genetic distance matrices. It can be assumed that when assessing the actual differentiation of populations by STR-markers, the methods of group B should be used and among them the statistics of DEST as independent of the level of mean within-subpopulation heterozygosity. In the study of spatial ordination of gene pools of populations, in all probability, it is reasonably to use any method.

1. Galinskaya T. V., Shchepetov D. M., Lysenkov S. N. Predubezhdeniya o mikrosatellitnykh issledovaniyakh i kak im protivostoyat'. [Prejudices against microsatellite studies and the ways to resist them]. Genetika = Russian Journal of Genetics. 2019;55(6):1-16. (In Russ.). DOI: https://doi.org/10.1134/S0016675819060043

2. Zinov'eva N. A., Sermyagin A. A., Dotsev A. V., Boronetskaya O. I., Petrikeeva L. V., Abdel'manova A. S., Brem G. Geneticheskie resursy zhivotnykh: razvitie issledovaniy allelofonda rossiyskikh porod krupnogo rogatogo skota – Miniobzor. [Animal genetic resources: developing the research of allele pool of Russian cattle breeds. Mini review]. Sel'skokhozyaystvennaya biologiya = Agricultural Biology. 2019;54(4):631-641. (In Russ.). DOI: https://doi.org/10.15389/agrobiology.2019.4.631rus

3. Karafet T. M., Zegura S. L., Khammer M. F. Istoricheskoe osvoenie chelovekom novykh territoriy: rol' drevnikh populyatsiy Azii v zaselenii Ameriki. [Historical development of new lands by a man: an ancient link between Asia and America]. Informatsionnyy vestnik VOGiS. 2006;10(1):7-23. (In Russ.). URL: https://elibrary.ru/item.asp?id=9573134

4. Kalinowski S. T. Evolutionary and statistical properties of three genetic distances. Molec. Ecol. 2002;11(8):1263-1273. DOI: https://doi.org/10.1046/j.1365-294X.2002.01520.x

5. Wright S. The genetical structure of populations. Annals of Eugenics. 1951;15(4):323-354. DOI: https://doi.org/10.1111/j.1469-1809.1949.tb02451.x

6. Nei M. Genetic distance between populations. Amer. Natur. 1972;106(949):283-292. URL: https://www.jstor.org/stable/2459777

7. Kuznetsov V. M. F-statistiki Rayta: otsenka i interpretatsiya. [Wright’s F-statistics: estimation and interpre-tation]. Problemy biologii produktivnykh zhivotnykh = Problems of Productive Animal Biology. 2014;4:80-104. (In Russ.). URL: https://elibrary.ru/item.asp?id=22833217

8. Nei M., Chesser R. K. Estimation of fixation indexes and gene diversities. Ann. Hum. Genet. 1983;47(3):253-259. DOI: https://doi.org/10.1111/j.1469-1809.1983.tb00993.x

9. Nei M. Definition and estimation of fixation indices. Evolution. 1986;40(3):643-645. DOI: https://doi.org/10.1111/j.1558-5646.1986.tb00516.x

10. Hedrick P. W. Perspective: Highly variable loci and their interpretation in evolution and conservation. Evolution. 1999;53(2):313-318. DOI: https://doi.org/10.1111/j.1558-5646.1999.tb03767.x

11. Hedrick P. W. A standardized genetic differentiation measure. Evolution. 2005;59(8):1633-1638. URL: https://www.jstor.org/stable/3449070

12. Jost L. GST and its relatives do not measure differentiation. Molec. Ecol. 2008;17(18):4015-4026. DOI: https://doi.org/10.1111/j.1365-294X.2008.03887.x

13. 1Nei M. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics. 1978;89(3):583-590. URL: https://www.genetics.org/content/89/3/583

14. 1Heller R., Siegismund H. R. Relationship between three measures of genetic differentiation GST, DEST and G'ST: how wrong have we been? Molec. Ecol. 2009;18(10):2080-2083. DOI: https://doi.org/10.1111/j.1365-294x.2009.04185.x

15. Volkova V. V., Deniskova T. E., Kostyunina O. V., Amerkhanov Kh. A., Dobrynina T. I., Zinov'eva N. A. Kharakteristika allelofonda lokal'nykh porod krupnogo rogatogo skota Rossii po mikrosatellitnym markeram. [Characteristic of allele pool of local cattle breeds of Russia based on microsatellite markers]. Genetika i razvedenie zhivotnykh = Genetics and breeding animals. 2018;1:3-10. (In Russ.). DOI: https://doi.org/10.31043/2410-2733-2018-1-3-10

16. Sermyagin A. A., Dotsev A. V., Gladyr E. A., Traspov A. A., Deniskova T. E., Kostyunina O. V., Reyer H., Wimmers K., Barbato M., Paronyan I. A., Plemyashov K. V., Sölkner J., Popov R. G., Brem G., Zinovieva N. A. Whole-genome SNP analysis elucidates the genetic structure of Russian cattle and its relationship with Eurasian taurine breeds. Genet. Sel. Evol. 2018;50(37):1-13. DOI: https://doi.org/10.1186/s12711-018-0408-8

17. Yurchenko A., Yudin N., Aitnazarov R., Plyusnina A., Brukhin V., Soloshenko V., Lhasaranov B., Popov R., Paronyan I. A., Plemyashov K. V., Larkin D. M. Genome-wide genotyping uncovers genetic profiles and history of the Russian cattle breeds. Heredity. 2018;120:125-137. DOI: https://doi.org/10.1038/s41437-017-0024-3

18. Yudin N. S., Larkin D. M. Proiskhozhdenie, selektsiya i adaptatsiya rossiyskikh porod krupnogo rogatogo skota po dannym polnogenomnykh issledovaniy.[Whole genome studies of origin, selection and adaptation of the Russian cattle breeds]. Vavilovskiy zhurnal genetiki i selektsii = Vavilov Journal of Genetics and Breeding. 2019;23(5):559-568. (In Russ.). DOI: https://doi.org/10.18699/VJ19.525

19. Volkova V. V., Romanenkova O. S., Deniskova T. E., Mishina A. I., Kostyunina O. V., Zinov'eva N. A. Kharakteristika allelofonda kholmogor-skoy porody krupnogo rogatogo skota s ispol'zovaniem STR-markerov. [Assessment of the allele pool of the Kholmogory cattle breed using STR-markers]. Molochnoe i myasnoe skotovodstvo = Dairy and Beef Cattle Breeding. 2019;(7):3-7. (In Russ.). URL: https://elibrary.ru/item.asp?id=41852279

20. Deniskova T. E., Dotsev A. V., Selionova M. I., Kunz E., Medugorac I., Reyer H., Wimmers K., Barbato M., Traspov A. A., Brem G., Zinovieva N. A. Population structure and genetic diversity of 25 Russian sheep breeds based on whole-genome genotyping. Genet. Sel. Evol. 2018;50(29). DOI: https://doi.org/10.1186/s12711-018-0399-5

21. Deniskova T. E., Kostyunina O. V., Solov'eva A. D., Zinov'eva N. A. Izuchenie geneticheskogo raznoobraziya i differentsiatsii regional'nykh populyatsiy romanovskikh ovets po mikrosatellitnym markeram. [Study of ge-netic diversity and differentiation of regional populations of Romanov sheep using microsatellite markers]. Agrarnaya nauka Evro-Severo-Vostoka = Agricultural Science Euro-North-East. 2018;64(3):75-80. (In Russ.). DOI: https://doi.org/10.30766/2072-9081.2018.64.3.75-80

22. Khrabrova L. A., Blohina N. V., Suleymanov O. I., Rozhdestvenskaya G. A., Pustovoy V. F. Assessment of line differentiation in the Thoroughbred horse breed using DNA microsatellite loci. Vavilovskiy zhurnal genetiki i selektsii = Vavilov Journal of Genetics and Breeding. 2019;23(5):569-574. (In Russ.). DOI: https://doi.org/10.18699/VJ19.526

23. Kharzinova V. R., Kostyunina O. V., Karpushkina T. V., Bykova O. A., Zinov'eva N. A. Izuchenie popu-lyatsionnoy struktury i geneticheskogo raznoobraziya sviney porody vengerskaya mangalitsa na osnove analiza mikrosatellitov. [The study of the population structure and genetic diversity of Hungarian Mangalica breed of pigs based on microsatellites analysis]. Agrarnyy vestnik Urala = Agrarian Bulletin of the Urals. 2019;7(186):77-81. (In Russ.). DOI: https://doi.org/10.32417/article_5d52b081b3e348.43320197

24. Kharzinova V. R., Dotsev A. V., Deniskova T. E., Solovieva A. D., Fedorov V. I., Layshev K. A., Romanenko T. M., Okhlopkov I. M., Wimmers K., Reyer H., Brem G., Zinovieva N. A. Genetic diversity and popu-lation structure of domestic and wild reindeer (Rangifer tarandus L. 1758): A novel approach using BovineHD BeadChip. PLoS ONE. 2018. DOI: https://doi.org/10.1371/journal.pone.0207944

25. Fornara M. S., Kramarenko A. S., Sharov M. A., Zinov'eva N. A. Issledovanie allelofonda i geneticheskoy differentsiatsii dal'nevostochnykh pchel. [Study of allele pool and genetic differentiation of the Far-Eastern honey bees]. Dostizheniya nauki i tekhniki APK = Achievements of Science and Technology of AIC. 2016;30(10):101-104. (In Russ.). URL: https://elibrary.ru/item.asp?id=27175140

26. Peakall R., Smouse P.E. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molec. Ecol. 2006;6(1):288-295. DOI: https://doi.org/10.1111/j.1471-8286.2005.01155.x

27. Peakall R., Smouse P. GenAlEx Tutorial 1: Introduction to population genetic analysis. Australian National University. 2012. 57 p. URL: https://mafiadoc.com/genalex-tutorial-1-introduction-to-population-genetic-_597ef8441723dd6ae3e07272.html

28. Peakall R., Smouse P .E. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics. 2012b;28(19):2537-2539. DOI: https://doi.org/10.1093/bioinformatics/bts460

29. Kuznetsov V. M. Snizhaet li krossbriding geneticheskoe raznoobrazie? ili Razvedenie i sokhranenie porod molochnogo skota v Rossii. [Whether crossbreeding reduces genetic diversity or Breeding and preser-vation of dairy cattle breeds in Russia]. Kirov: NIISKh Severo-Vostoka, 2017. 104 p. URL: http://vm-kuznetsov.ru/files/book/Pap2017_he.pdf

30. Deniskova T. E., Sermyagin A. A., Bagirov V. A., Okhlopkov I. M., Gladyr' E. A., Ivanov R. V., Brem G., Zinov'eva N. A. Sravnitel'noe issledovanie informativnosti STR i SNP markerov dlya vnutrividovoy i mezhvidovoy differentsiatsii roda Ovis. [Comparative analysis of the effectiveness of STR and SNP markers for intraspecific and interspecific differentiation of the genus Ovis]. Genetika = Russian Journal of Genetics. 2016;52(1): 90-96. (In Russ.). DOI: https://doi.org/10.7868/S0016675816010021

31. Hartl D. L., Clark A. G. Principles of Population Genetics. Third Edition. Sunderland, Massachusetts: Sinauer Associates, Inc., 1997. 542 p. URL: https://archive.org/details/B-001-001-062/page/n13

32. Meirmans P. G. Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution. 2006;60(11):2399-2402. DOI: https://doi.org/10.1111/j.0014-3820.2006.tb01874.x

33. Kuznetsov A. V., Tulinova O. V. Kharakteristika porodnykh komponent ayrshirskogo stada PAO «PZ im. V. I. Chapaeva» Krasnodarskogo kraya. [Characteristics of breed component of Ayrshire herd of PC «BP of V. I. Chapaeva» Krasnodar territory]. Genetika i razvedenie zhivotnykh. 2019;2:24-29. (In Russ.). DOI: https://doi.org/10.31043/2410-2733-2019-2-24-29

34. Gautier M., Laloë D., Moazami-Goudarzi K. Insights into the Genetic History of French Cattle from Dense SNP Data on 47 Worldwide Breeds. PLoS ONE. 2010;5(9): e13038. DOI: https://doi.org/10.1371/journal.pone.0013038

35. Plemb Ch. Tipy i porody sel'skokhozyaystvennykh" zhivotnykh". [Types and breeds of farm animals]. S.-Peterburg", 1913. 560 p.

36. Ruzhevskiy A. B., Ruban Yu. D., Berdnik P. P. Porody krupnogo rogatogo skota. [Breeds of cattle]. Moscow: «Kolos», 1980. 246 p.