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Spatial Population Genetic Structuring of the Common Shrew Sorex araneus (Lipotyphla, Mammalia): Variability of Microsatellite Markers

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Abstract

Variability of five microsatellite loci was studied in the common shrew S. araneus belonging to the Moscow chromosomal race. Three local samples (n = 39) from the sites situated at a minimum distance from each other (350–700 m) were examined. The studied samples were characterized by high allelic diversity along with considerable genetic differentiation of the population. Pairwise comparisons revealed statistically significant difference between the samples, with the highest genetic differences observed at a minimum geographic distance. To explain the causes of the population genetic heterogeneity, analysis of the population demographic patterns at the sampling sites and neighboring areas was carried out. The data obtained were consistent with the models of Altukhov’s population system.

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REFERENCES

  1. Bulatova, N.S., Biltueva, L.S., Pavlova, S.V., et al., Chromosomal differentiation in the common shrew and related species, in Shrews, Chromosomes and Speciation, Cambridge: Cambridge Univ. Press, 2019, pp. 134—185. https://doi.org/10.1017/9780511895531.

  2. Fedyk, S., Pavlova, S.V., Chętnicki, W., and Searle, J.B., Chromosomal hybrid zones, in Shrews, Chromosomes and Speciation, Cambridge: Cambridge Univ. Press, 2019, pp. 271—311. https://doi.org/10.1017/9780511895531.

  3. Barton, N.H. and Hewitt, G.M., Hybrid zones and speciation, in Essays in Honour of M. J. D. White: Evolution and Speciation, Cambridge: Cambridge Univ. Press, 1981, pp. 109—145.

    Google Scholar 

  4. Barton, N.H. and Hewitt, G.M., Analysis of hybrid zones, Annu. Rev. Ecol. Syst., 1985, vol. 16, pp. 113—148.

    Google Scholar 

  5. Feder, J.L., Egan, S.P., and Nosil, P., The genomics of speciation-with-gene-flow, Trends Genet., 2012, vol. 28, pp. 342—350.

    CAS  PubMed  Google Scholar 

  6. Hewitt, G.M., Hybrid zones—natural laboratories for evolutionary studies, TREE, 1988, vol. 3, pp. 158—165. https://doi.org/10.1016/0169-5347(88)90033-X

    Article  CAS  PubMed  Google Scholar 

  7. Bulatova, N.S., Jones, R.M., White, T.A., et al., Natural hybridization between extremely divergent chromosomal races of the common shrew (Sorex araneus, Soricidae, Soricomorpha): hybrid zone in European Russia, Evol. Biol., 2011, vol. 24, pp. 573—586.

    CAS  Google Scholar 

  8. Andersson, A.C., Alström-Rapaport, C., and Fredga, K., Lack of mitochondrial DNA divergence between chromosome races of the common shrew, Sorex araneus, in Sweden: implications for interpreting chromosomal evolution and colonization history, Mol. Ecol., 2005, vol. 14, pp. 2703—2716.

    CAS  PubMed  Google Scholar 

  9. Raspopova, A.A. and Shchipanov, N.A., Variability of a cytochrome b region in different chromosome races and populations of the common shrew Sorex araneus L., 1758, Russ. J. Genet., 2011, vol. 47, no. 4, pp. 462—470. https://doi.org/10.1134/S1022795411030148

    Article  CAS  Google Scholar 

  10. Lundqvist, A.C., Alström-Rapaport, C., and Tegelström, H., Fennoscandian phylogeography of the common shrew Sorex araneus: post-glacial recolonisation combining information from chromosomal variation with mitochondrial DNA data, Acta Theriol., 2011, vol. 56, pp. 103—116.

    Google Scholar 

  11. Thaw, S., White, T.A., Bannikova, A.A., and Searle, J.B., Phylogeography, in Shrews, Chromosomes and Speciation, Cambridge: Cambridge Univ. Press, 2019, pp. 113—133. https://doi.org/10.1017/9780511895531.

  12. Ratkiewicz, M., Fedyk, S., Banaszek, A., et al., The evolutionary history of the two karyotypic groups of the common shrew, Sorex araneus, in Poland, Heredity, 2002, vol. 88, pp. 235—242.

    CAS  PubMed  Google Scholar 

  13. Andersson, A.C., Narain, Y., Tegelström, H., and Fredga, K., No apparent reduction of gene flow in a hybrid zone between the West and North European karyotypic groups of the common shrew, Sorex araneus,Mol. Ecol., 2004, vol. 13, pp. 1205—1215.

    CAS  PubMed  Google Scholar 

  14. White, T.A. and Searle, J.B., Mandible asymmetry and genetic diversity in island populations of the common shrew, Sorex araneus,Evol. Biol., 2008, vol. 21, pp. 636—641. https://doi.org/10.1111/j.1420-9101.2007.01481.x

    Article  CAS  Google Scholar 

  15. Horn, A., Basset, P., Yannic, G., et al., Chromosomal rearrangements do not seem to affect the gene flow in hybrid zones between karyotypic races of the common shrew (Sorex araneus), Evolution, 2012, vol. 66, pp. 882—889. https://doi.org/10.1111/j.1558-5646.2011.01478.x

    Article  PubMed  Google Scholar 

  16. Yannic, G., Basset, P., Horn, A., and Hausser, J., Gene flow between chromosomal races and species, Shrews, Chromosomes and Speciation, Cambridge: Cambridge Univ. Press, 2019, pp. 313—335. https://doi.org/10.1017/9780511895531.

  17. Wyttenbach, A., Goudet, J., Cornuet, J.M., and Hausser, J., Microsatellite variation reveals low genetic subdivision in a chromosome race of Sorex araneus (Mammalia, Insectivora), J. Hered., 1999, vol. 90, pp. 323—327.

    Google Scholar 

  18. Jadwiszczak, K.A., Ratkiewicz, M., and Banaszek, A., Analysis of molecular differentiation in a hybrid zone between chromosomally distinct races of the common shrew Sorex araneus (Insectivora: Soricidae) suggests their common ancestry, Biol. J. Linn. Soc., 2006, vol. 89, no. 1, pp. 79—90.

    Google Scholar 

  19. Wyttenbach, A. and Hausser, J., Microsatellites in Sorex araneus (Insectivora): highly polymorphic markers for population genetic studies within and between chromosomal races, Hereditas, 1996, vol. 125, pp. 177—181.

    Google Scholar 

  20. Wyttenbach, A., Narain, Y., and Fredga, K., Genetic structuring and gene flow in a hybrid zone between two chromosome races of the common shrew (Sorex araneus, Insectivora) revealed by microsatellites, Heredity, 1999, vol. 82, pp. 79—88.

    Google Scholar 

  21. Grigoryeva, O.O., Shestak, A.G., Potapov, S.G., et al., The microsatellite polymorphism and gene flow in the contact zone of four common shrew (Sorex araneus L., Mammalia) chromosome races, Biol. Bull. (Moscow), 2011, vol. 38, no. 5, pp. 425–433. https://doi.org/10.1134/S1062359011050062

  22. Narain, Y. and Fredga, K., Spermatogenesis in common shrews, Sorex araneus, from a hybrid zone with extensive Robertsonian polymorphism, Cytogenet. Cell Genet., 1998, vol. 80, pp. 158—164.

    CAS  PubMed  Google Scholar 

  23. Shchipanov, N.A. and Pavlova, S.V., Multilevel subdivision in the group of species “araneus” of the genus Sorex: 1. Chromosomal differentiation, Zool. Zh., 2016, vol. 95, no. 2, pp. 216—233. https://doi.org/10.7868/S0044513416020148

    Article  Google Scholar 

  24. Shchipanov, N.A. and Pavlova, S.V., Role of population structuring in the formation of karyotypic diversity of the common shrew Sorex araneus (Lipotyphla, Mammalia), Russ. J. Ecol., 2019, no. 2, pp. 101—111.

  25. Altukhov, Yu.P. and Rychkov, Yu.G., Population systems and their structural components: genetic stability and variation, Zh. Obshch. Biol., 1970, vol. 31, no. 5, pp. 507—525.

    PubMed  Google Scholar 

  26. Altukhov, Yu.P., Geneticheskie protsessy v populyatsiyakh (Genetic Processes in Populations), Moscow: Nauka, 1983.

  27. Altukhov, Yu.P., Geneticheskie protsessy v populyatsiyakh (Genetic Processes in Populations), Moscow: Akademkniga, 2003, 3rd ed.

  28. Bulatova, N.Sh. and Pavlova, S.V., The chromosome race in the epicenter of hybrid zones, Inf. Vestn. Vavilovskogo O-vaGenet. Sel., 2011, vol. 11, no. 2, pp. 432—435.

    Google Scholar 

  29. Shchipanov, N.A., Kalinin, A.A., Oleinichenko, V.Yu., et al., The method of studying the use of space by red-toothed shrews, Zool. Zh., 2000, vol. 79, no. 3, pp. 362—371.

    Google Scholar 

  30. Shchipanov, N.A., Labeling on live trap lines for monitoring small mammals: a method for calculating population density and non-resident indices, Zool. Zh., 2020 (in press).

  31. Arrigi, F.E., Bergendahl, G., and Mandel, M., Isolation and characterization of DNA from fixed cells and tissues, Exp. Cell. Res., 1968, no. 50, pp. 47—53.

  32. Sambrook, J., Fritsch, E.F., and Maniatis, T., Molecular Cloning: A Laboratory Manual, New York: Cold Spring Harbor Lab., 1989.

    Google Scholar 

  33. Basset, P., Yannic, G., Yang, F.T., et al., Chromosome localization of microsatellite markers in the shrews of the Sorex araneus group, Chromosome Res., 2006, vol. 14, pp. 253—262.

    CAS  PubMed  Google Scholar 

  34. Stenseth, N.C. and Framstad, E., Reproductive effort and optimal reproductive rates in small rodents, Oikos, 1980, vol. 34, no. 1, pp. 23—34.

    Google Scholar 

  35. Henttonen, H., McGuire, A.D., and Hansson, L., Comparisons of amplitudes and frequencies (spectral analyses) of density variations in long-term data sets of Clethrionomys species, Ann. Zool. Fenn., 1985, vol. 22, no. 3, pp. 221—227.

    Google Scholar 

  36. Stenseth, N.C., Bjørnstad, O.N., and Saitoh, T., Seasonal forcing on the dynamics of Clethrionomys rufocanus: modeling geographic gradients in population dynamics, Popul. Ecol., 1998, vol. 40, no. 1, pp. 85—95.

    Google Scholar 

  37. Bjørnstad, O.N., Stenseth, N.C., Saitoh, T., and Lingjære, O.C., Mapping the regional transitions to cyclicity in Clethrionomys rufocanus: spectral densities and functional data analysis, Popul. Ecol., 1998, vol. 40, no. 1, pp. 77—84.

    Google Scholar 

  38. Saitoh, T., Stenseth, N.C., and Bjørnstad, O.N., The population dynamics of the vole Clethrionomys rufocanus in Hokkaido, Japan, Popul. Ecol., 1998, vol. 40, no. 1, pp. 61—76.

    Google Scholar 

  39. Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., and Shipley, P., Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data, Mol. Ecol. Notes, 2004, vol. 4, pp. 535—538.

    CAS  Google Scholar 

  40. Garza, J.C. and Williamson, E.G., Detection of reduction in population size using data from microsatellite loci, Mol. Ecol., 2010, vol. 10, pp. 305—318.

    Google Scholar 

  41. Excoffier, L., Laval, G., and Schneider, S., Arlequin ver. 3.0: an integrated software package for population genetics data analysis, Evol. Bioinf. Online, 2005, vol. 1, pp. 47—50. https://doi.org/10.1177/117693430500100003

    Article  CAS  Google Scholar 

  42. Nei, M., F-statistics and analysis of gene diversity in subdivided populations, Ann. Hum. Genet., 1977, vol. 41, pp. 225—233.

    CAS  PubMed  Google Scholar 

  43. Slatkin, M.A., Measure of population subdivision based on microsatellite allele frequencies, Genetics, 1995, vol. 139, pp. 457—462.

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Goudet, J., Raymond, M., Demeeus, T., and Rousset, F., Testing differentiation in diploid populations, Genetics, 1996, vol. 144, pp. 1933—1940.

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Goudet, J., Fstat (ver. 2.9.4), a program to estimate and test population genetics parameters, 2003. http://www2.unil.ch/popgen/softwares/fstat.htm.

  46. Kimura, M. and Ohta, T., Stepwise mutation model and distribution of allelic frequencies in a finite population, Proc. Natl. Acad. Sci. U.S.A., 1978, vol. 75, pp. 2868—2872.

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Selander, R.K., Behavior and genetic variation in natural populations, Am. Zool., 1970, vol. 10, pp. 53—66.

    CAS  PubMed  Google Scholar 

  48. Shchipanov, N.A., Zima, J., and Churchfield, S., Introducing the common shrew chromosomal hybrid zones, in Shrews, Chromosomes and Speciation, Cambridge: Cambridge Univ. Press, 2019, pp. 19—64. https://doi.org/10.1017/9780511895531.

  49. Hanski, I., Peltonen, A., and Kaski, L., Natal dispersal and social dominance in the common shrew Sorex araneus,Oikos, 1991, vol. 62, pp. 48—58.

    Google Scholar 

  50. Kalinin, A.A. and Kupriyanova, I.F., Techniques of the small mammals counting during migration through the water barriers, Zool. Zh., 2015, vol. 94, no. 2, pp. 365—369.

    Google Scholar 

  51. Shchipanov, N.A. and Pavlova, S.V., Density-dependent processes determine the distribution of chromosomal races of the common shrew Sorex araneus (Lipotyphla, Mammalia), Mammal Res., 2017, vol. 62, no. 3, pp. 267—282. https://doi.org/10.1007/s13364-017-0314-4

    Article  Google Scholar 

  52. Tegelström, H. and Hansson, L., Evidence of long-distant dispersal in the common shrew (Sorex araneus), Z. Saugetierk., 1987, vol. 52, pp. 52—54.

    Google Scholar 

  53. Shchipanov, N.A., Kuptsov, A.V., Kalinin, A.A., and Oleinichenko, V.Yu., Cones and live-traps catch different shrews (Insectivora, Soricidae), Zool. Zh., 2003, vol. 83, no. 10, pp. 1258—1265.

    Google Scholar 

  54. Shchipanov, N.A., Kuptsov, A.V., Demidova, T.B., et al., Non-residency and resettlement of the common shrew (Sorex araneus, Insectivora), Zool. Zh., 2008, vol. 87, no. 3, pp. 331—343.

    Google Scholar 

  55. Altukhov, Yu.P. and Pobedonostseva, E.Yu., Biological features of experimental population system of Drosophila melanogaster,Zh. Obshch. Biol., 1979, vol. 40, no. 6, pp. 916—923.

    Google Scholar 

  56. Altukhov, Yu.P. and Pobedonostseva, E.Yu., Genetic process in experimental population system of Drosophila melanogaster,Zh. Obshch. Biol., 1979, vol. 40, no. 3, pp. 368—367.

    Google Scholar 

  57. Rychlik, L., Evolution of social systems in shrews, in Evolution of Shrews, Białowieża: Mammal Research Institute, 1998, pp. 347—406.

    Google Scholar 

  58. Oleinichenko, V.Yu., Yearling behavior of common (Sorex araneus), masked (Sorex caecutiens), and pygmy (Sorex minutus) shrews on acquired land and alien territories, Zool. Zh., 2007, vol. 86, no. 10, pp. 1259—1271.

    Google Scholar 

  59. Churchfield, S., The Natural History of Shrews, London: Christopher Helm, 1990.

    Google Scholar 

  60. Shillito, J.F., Field observation on the growth, reproduction and activity of a woodland population of the common shrew Sorex araneus L., Proc. Zool. Soc. London, 1963, vol. 140, pp. 99—113. https://doi.org/10.1111/j.1469-7998.1963.tb01856.x

    Article  Google Scholar 

  61. Shillito, J.F., Observations on the range and movements of a woodland population of the common shrew Sorex araneus L., Proc. R. Soc. London, 1963, vol. 140, pp. 533—546.

    Google Scholar 

  62. Shchipanov, N.A., Kalinin, A.A., Demidova, T.B., et al., Population ecology of red-toothed shrews, Sorex araneus, S. caecutiens, S. minutus, and S. isodon, in Central Russia, in Advances in the Biology of Shrews II, New York: International Society of Shrew Biologists, 2005, pp. 201—216.

    Google Scholar 

  63. Kalinin, A.A., Demidova, T.B., Oleinichenko, V.Yu., and Shchipanov, N.A., Seasonal dynamics in numbers of red-toothed shrews (Insectivora, Soricidae), Zool. Zh., 2008, vol. 87, pp. 218—225.

    Google Scholar 

  64. Crowcroft, W.P., The Life of the Shrew, London: Max Reinhardt, 1957.

    Google Scholar 

  65. Buckner, C.H., Some aspects of the population ecology of the common shrew, S. araneus, near Oxford, England, J. Mamm., 1969, vol. 50, pp. 326–332.

  66. Pernetta, J.C., Population ecology of British shrews in grassland, Acta Theriol., 1977, vol. 22, pp. 279—296.

    Google Scholar 

  67. Churchfield, S., Population dynamics and seasonal fluctuations in numbers of the common shrew in Britain, Acta Theriol., 1980, vol. 25, pp. 451—459.

    Google Scholar 

  68. Hanski, I., Metapopulation Ecology, New York: Oxford Univ. Press, 1999.

    Google Scholar 

  69. Shchipanov, N.A., Understanding the boundaries between chromosome races of common shrews in terms of restricted movement by individual shrews, Russ. J. Theriol., 2007, vol. 6, pp. 117—122.

    Google Scholar 

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ACKNOWLEDGMENTS

We thank Dr. Olga Grigorieva (Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow) for consultations in analyzing the microsatellite diversity.

Funding

This study was supported by the Russian Foundation for Basic Research (grant no. 19-04-00985) (S.P.) and the Program of the Presidium of the Russian Academy of Sciences “Biodiversity and Biological Resources of Russia” (Program 41) (S.P.). Part of the study was carried out within the framework of the state contract with Penza State University in the field of scientific activity for 2017–2019 (project 6.7197.2017/BCh) (S.T.).

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  1. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 119071, Moscow, Russia

    N. A. Shchipanov, A. V. Artamonov & S. V. Pavlova

  2. Penza State University, 440026, Penza, Russia

    S. V. Titov

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  1. N. A. Shchipanov
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  2. A. V. Artamonov
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  3. S. V. Titov
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  4. S. V. Pavlova
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Correspondence to S. V. Pavlova.

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Shchipanov, N.A., Artamonov, A.V., Titov, S.V. et al. Spatial Population Genetic Structuring of the Common Shrew Sorex araneus (Lipotyphla, Mammalia): Variability of Microsatellite Markers. Russ J Genet 56, 942–951 (2020). https://doi.org/10.1134/S102279542008013X

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