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Channelized Karyotype Evolution of the Common Shrew Sorex araneus (Mammalia)

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Abstract—

A model of the channelized evolution of the S. araneus L. karyotype in the processes of replacement of ten pairs of acrocentric chromosomes by five pairs of metacentric chromosomes has been proposed. The channelized evolution of the karyotype arises due to the inability of Rb-fusions with incomplete (monobrachial) homology to spread in the same population. Therefore, an Rb-fusion, due to some random event first appearing in a population, largely determines the further evolution of the karyotype of that population. After the third replacement of acrocentric chromosomes by metacentric chromosomes, the replacement of the remaining 6 pairs of acrocentrics allows the formation of no more than three karyotypes with five diagnostic metacentrics, which can be predicted, regardless of which rearrangements result in metacentric chromosomes (Rb-fusion or WART). The channelized karyotypic evolution greatly increases the likelihood of parallel karyotype formation, in cases where evolution begins with identical metacentrics in geographically distant populations. An example of parallel evolution that began with the gk metacentric is the identical karyotypes of the new Mogilev race from Belarus and the Tomsk race from Western Siberia. The evolution of Eastern European chromosomal races shows hybrid fusion processes between the karyotypes of the East European karyotypic group (EEKG) and the West European karyotypic group (WEKG).

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REFERENCES

  1. 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.

    Article  CAS  PubMed  Google Scholar 

  2. Baker, R.J. and Bickham, J.W., Karyotypic evolution in bats: Evidence of extensive and conservative chromosomal evolution in closely related taxa, Syst. Zool., 1980, vol. 29, no. 1, pp. 239–254.

    Article  Google Scholar 

  3. Baker, R.J. and Bickham, J.W., Speciation by monobrachial centric fusions, Proc. Natl. Acad. Sci. U. S. A., 1986, vol. 83, pp. 8245–8248.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Berg, L.S., Nomogenesis, or evolution determined by law, in Teorii evolyutsii (Theories of Evolution), Petrograd: Academia, 1922, Ch. 5, pp. 82–94.

  5. Berg, R.L., Genetika i evolyutsiya. Izbrannye Trudy (Genetics and Evolution. Selected Works), Novosibirsk: Nauka, 1993.

  6. Bickham, J.W. and Baker, R.J., Canalization model of chromosomal evolution, Bull. Carnegie Mus. Nat. Hist., 1979, vol. 13, pp. 70–84.

    Google Scholar 

  7. Biltueva, L.S., Perelman, P.L., Polyakov, A.V., et al., Comparative chromosome analysis in three Sorex species: S. raddei, S. minutus and S. caecutiens, Acta Theriol., 2000, vol. 45, suppl. 1, pp. 119–130.

    Article  Google Scholar 

  8. Borisov, Yu.M., Cherepanova, E.V., and Orlov, V.N., A wide hybrid zone of chromosome races of the common shrew, Sorex araneus Linnaeus, 1758 (Mammalia), between the Dnieper and Berezina Rivers (Belarus), Comp. Cytogenet., 2010, vol. 3, no. 2, pp. 195–201.

    Google Scholar 

  9. Borisov, Yu.M., Kryshchuk, I.A., Cherepanova, E.V., et al., Chromosomal polymorphism of populations of the common shrew, Sorex araneus L. in Belarus, Acta Theriol., 2014, vol. 59, no. 2, pp. 243–249.

    Article  Google Scholar 

  10. Borisov, Yu.M., Gaiduchenko, H.S., Cherepanova, E.V., et al., The clinal variation of metacentric frequency in the populations of the common shrew, Sorex araneus L., in the Dnieper and Pripyat interfluve, Mammal Res., 2016, vol. 61, pp. 269–277.

    Article  Google Scholar 

  11. Borisov, Y.M., Kryshchuk, I.A., Gaiduchenko, H.S., et al., Karyotypic differentiation of populations of the common shrew Sorex araneus L. (Mammalia) in Belarus, Comp. Cytogenet., 2017, vol. 11, no. 2, pp. 359–373.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Brünner, H., Turni, H., and Kapischke, H.-J., New Sorex araneus karyotypes from Germany and the postglacial recolonization of central Europe, Acta Theriol., 2002, vol. 47, no. 3, pp. 277–293.

    Article  Google Scholar 

  13. Bulatova, N., Searle, J.B., Bystrakova, N., et al., The diversity of chromosome races in Sorex araneus from European Russia, Acta Theriol., 2000, vol. 45, suppl. 1, pp. 33–46.

    Article  Google Scholar 

  14. Bulatova, N.S., Biltueva, L.S., and Pavlova, S.V., Chromosomal differentiation in the common shrew and related species, in Shrews, Chromosomes and Speciation, Searle, J., Polly, P., and Zima, J., Eds., Cambridge Studies in Morphology and Molecules: New Paradigms in Evolutionary Bio, Cambridge: Cambridge Univ. Press, 2019, pp. 134–184.

    Google Scholar 

  15. Capanna, E., Robertsonian numerical variation in animal speciation: Mus musculus an emblematic model, in Mechanism of Speciation, Barigozzi, C., Ed., New York: Alan Liss, 1982, pp. 155–177.

  16. Capanna, E. and Castiglia, R., Chromosomes and speciation in Mus musculus domesticus, Cytogenet. Genome Res., 2004, vol. 105, pp. 375–384.

    Article  CAS  PubMed  Google Scholar 

  17. Capanna, E., Civitelli, M.V., and Cristaldi, M., Chromosomal rearrangement, reproductive isolation and speciation in mammals. The case of Mus musculus, Boll. Zool., 1977, vol. 44, pp. 213–246.

    Article  Google Scholar 

  18. Cucchi, T., Vigne, J.D., and Auffray, J.-C., First occurrence of the house mouse (Mus musculus domesticus Schwarz et Schwarz, 1943) in the western Mediterranean: A zooarchaeological revision of sub-fossil house mouse occurrences, Biol. J. Linn. Soc., 2005, vol. 84, pp. 429–445.

    Article  Google Scholar 

  19. Cytotaxonomy and Vertebrate Evolution, Chiarelli, A.B. and Capanna, E., Eds., London: Academic, 1973.

    Google Scholar 

  20. Darwin, C.R., On the Origin of Species by Means of Natural Selection, London: Murray, 1859.

    Google Scholar 

  21. Fedyk, S., Banaszek, A., Chętnicki, W., et al., Reassessment of the range of the Drnholec race: Studies on meiosis in Sorex araneus hybrids, Acta Theriol., 2000, vol. 45, suppl. 1, pp. 59–67.

    Article  Google Scholar 

  22. Fedyk, S., Pavlova, S.V., Chętnicki, W., and Searle, J.B., Chromosomal Hybrid Zones, in Shrews, Chromosomes and Speciation, Searle, J., Polly, P., and Zima, J., Eds., Cambridge Studies in Morphology and Molecules: New Paradigms in Evolutionary Bio, Cambridge: Cambridge Univ. Press, 2019, pp. 271–312.

    Google Scholar 

  23. Ford, C.E. and Hamerton, J.L., A colchicine hypotonic citrate, squash sequence for mammalian chromosomes, Stain Technol., 1956, vol. 31, pp. 247–251.

    Article  CAS  PubMed  Google Scholar 

  24. Fredga, K. and Nawrin, J., Karyotype variability in Sorex araneus L. (Insectivora, Mammalia), Chromosomes Today, 1977, vol. 6, pp. 153–161.

    Google Scholar 

  25. Fredga, K., The chromosome races of Sorex araneus in Scandinavia, Hereditas, 1996, vol. 125, pp. 123–135.

    Article  Google Scholar 

  26. Fredga, K., Reconstruction of the postglacial colonization of Sorex araneus into northern Scandinavia based on karyotype studies, and the subdivision of the Abisko race into three, Russ. J. Theriol., 2007, vol. 6, pp. 85–96.

    Article  Google Scholar 

  27. Garagna, S., Page, J., and Fernandez-Donoso, R., The robertsonian phenomenon in the house mouse: Mutation, meiosis and speciation, Chromosoma, 2014, vol. 123, pp. 529–544.

    Article  PubMed  Google Scholar 

  28. Hausser, J., Fedyk, S., Fredga, K., et al., Definition and nomenclature of chromosome races of Sorex araneus, Folia Zool., 1994, vol. 43, suppl. 1, pp. 1–9.

    Google Scholar 

  29. 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.

    Article  PubMed  Google Scholar 

  30. Hsu, T.C. and Benirschke, K., An Atlas of Mammalian Chromosomes, Berlin: Springer, 1967–1977, vols. 1–10.

  31. Huxley, J.S., Evolutionary process and taxonomy, with special reference to grades, Uppsala Univ. Arsskr., 1958, no. 6, pp. 21–39.

  32. Ivanitskaya, E.Yu., Chromosome numbers and brief morphological characteristics of mammalian karyotypes, in Comparative Cytogenetics and Karyosystematics of Mammals, Orlov, V.N. and Bulatova, N.Sh., Eds., Moscow: Nauka, 1983, pp. 171–403.

    Google Scholar 

  33. Král, B. and Radjabli, S.I., Banding patterns and Robertsonian fusion in the western Siberian population of Sorex araneus (Insectivora, Soricidae), Zool. Listy, 1974, vol. 23, pp. 217–227.

    Google Scholar 

  34. Kryshchuk, I.A., Orlov, V.N., Cherepanova, E.V., and Borisov, Yu.M., Unusual chromosomal polymorphism of the common shrew, Sorex araneus L., in southern Belarus, Comp. Cytogenet., 2021, vol. 15, no. 2, pp. 159–169.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Mackiewicz, P., Moska, M., Wierzbicki, H., et al., Evolutionary history and phylogeographic relationships of shrews from Sorex araneus group, PLoS One, 2017, vol. 12, p. e0179760.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Markova, A.K. and Puzachenko, A.Yu., Mammal assemblages during the Last Glacial Maximum (Last Glacial Maximum—LGM) (<=24–>=17 kyr BP), in Evolyutsiya ekosistem Evropy pri perekhode ot pleistotsena k golotsenu (24–8 tys. l. n.) (Evolution of European Ecosystems during Pleistocene—Holocene Transition) (24–8 kyr BP), Markova A.K. and van Kolfschoten, T., Eds., Moscow: KMK, 2008.

  37. Meyn, S.P. and Tweedie, R.L., Markov Chains and Stochastic Stability, London: Springer, 1993, 2nd ed.

    Book  Google Scholar 

  38. Mishta, A.V., Searle, J.B., and Wójcik, J.M., Karyotypic variation of the common shrew Sorex araneus in Belarus, Estonia, Latvia, Lithuania and Ukraine, Acta Theriol., 2000, vol. 45, suppl. 1, pp. 47–58.

    Article  Google Scholar 

  39. Orlov, V.N., Kariosistematika mlekopitayushchikh (Karyosystematics of Mammals), Moscow: Nauka, 1974.

  40. Orlov, V.N., Kozlovskii, A.I., Balakirev, A.E., and Bori-sov, Yu.M., Endemic chromosome races of the common shrew Sorex araneus L. (Insectivora, Mammalia) and the possible preservation of refugia in the Late Valdai glaciation area, Dokl. Biol. Sci., 2007a, vol. 416, pp. 396–399.

    Article  CAS  PubMed  Google Scholar 

  41. Orlov, V.N., Kozlovsky, A.I., Okulova, N.M., and Balakirev, A.E., Postglacial recolonisation of European Russia by the common shrew Sorex araneus, Russ. J. Theriol., 2007b, vol. 6, no. 1, pp. 97–104.

    Article  Google Scholar 

  42. Orlov, V.N., Kozlovskii, A.I., Balakirev, A.E., and Borisov, Yu.M., Fixation of metacentric chromosomes in Eastern Europe populations of the common shrew Sorex Araneus L., Russ. J. Genet., 2008, vol. 44, no. 5, pp. 501–512.

    Article  CAS  Google Scholar 

  43. Orlov, V.N., Cherepanova, E.V., Krivonogov, D.M., et al., Zonal and refugial stages of species evolution by the example of the common shrew, Sorex araneus L. (Soricidae, Soricomorpha), Biol. Bull. Rev., 2017, vol. 7, no. 6, pp. 478–492.

    Article  Google Scholar 

  44. Pavlova, S.V., Borisov, S.A., Timoshenko, A.F., and Sheftel, B.I., “European” race-specific metacentrics in East Siberian common shrews (Sorex araneus): A description of two new chromosomal races, Irkutsk and Zima, Comp. Cytogenet., 2017, vol. 11, pp. 797–806.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Petit, J.R., Jouzel, J., Raunaud, D., et al., Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica, Nature, 1999, vol. 399, pp. 429–436.

    Article  CAS  Google Scholar 

  46. Polyakov, A.V., Volobouev, V.T., Borodin, P.M., and Searle, J.B., Karyotypic races of the common shrew (Sorex araneus) with exceptionally large ranges: The Novosibirsk and Tomsk races of Siberia, Hereditas, 1996, vol. 125, pp. 109–115.

    Article  Google Scholar 

  47. Polyakov, A. V., Panov, V.V., Ladygina, T.Yu., et al., Chromosomal evolution of the common shrew Sorex araneus L. from the Southern Urals and Siberia in the postglacial period, Russ. J. Genet., 2001, vol. 37, no. 4, pp. 351–357.

    Article  CAS  Google Scholar 

  48. 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.

    Article  CAS  PubMed  Google Scholar 

  49. Seabright, M., A rapid banding technique for human chromosomes, Lancet, 1971, vol. 11, pp. 971–972.

    Article  Google Scholar 

  50. Searle, J.B., Three new karyotypic races of the common shrew Sorex araneus (Mammalia: Insectivora) and a phylogeny, Syst. Zool., 1984, vol. 33, pp. 184–194.

    Article  Google Scholar 

  51. Searle, J.B., Karyotypic variation and evolution in the common shrew, in Kew Chromosome Conference III, Brandham, P.E., Ed., London: HMSO, 1988, pp. 97–107.

  52. Searle, J.B. and Wójcik, J.M., Chromosomal evolution: The case of Sorex Araneus, in Evolution of Shrews, Wójcik, J.M., Wolsan, M., and Bialowieza, M., Eds., Warsaw: Mammal Res. Inst., 1998, pp. 219–268.

    Google Scholar 

  53. Searle, J.B., Fedyk, S., Fredga, K., et al., Nomenclature for the chromosomes of the common shrew (Sorex araneus), Comp. Cytogenet., 2010, vol. 4, pp. 87–96.

    Article  Google Scholar 

  54. 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, pp. 267–282.

    Article  Google Scholar 

  55. Shmal’gauzen, I.I., Problemy darvinizma (Problems of Darwinism), Leningrad: Nauka, 1969.

  56. Shrews, Chromosomes and Speciation, Searle, J., Polly, P., and Zima, J., Eds., Cambridge Studies in Morphology and Molecules: New Paradigms in Evolutionary Bio, Cambridge: Cambridge Univ. Press, 2019.

    Google Scholar 

  57. Vavilov, N.I., The law of homologous series of variability, Doklady na III Vseros. selektsionnom s”ezde v g. Saratove 4 iyunya 1920 (Proc. III All-Russian Breeding Congress in Saratov on June 4, 1920), 1920.

  58. Volobouev, V. and Catzeflis, F., Mechanism of chromosomal evolution in three European species of the Sorex Araneus-arcticus group (Insectivora: Soricidae), Z. Zool. Syst. Evolutionsforsch., 1989, vol. 27, pp. 252–262.

    Article  Google Scholar 

  59. Volobouev, V.T., Phylogenetic relationships of the Sorex araneus-arcticus species complex (Insectivora, Soricidae) based on high-resolution chromosome analysis, J. Hered., 1989, vol. 80, pp. 284–290.

    Article  Google Scholar 

  60. Vorontsov, N.N., Significance of the study of chromosome sets for the mammals taxonomy, Byull. Mosk. O-va Ispyt. Prir., Otd. Biol., 1958, vol. 63, no. 2, pp. 5–86.

    Google Scholar 

  61. White, M.J.D., Chain processes in chromosomal speciation, Syst. Zool., 1978, no. 3, pp. 285–298.

  62. White, T.A., Bordewich, M., and Searle, J.B., A network approach to study karyotypic evolution: The chromosomal races of the common shrew (Sorex araneus) and house mouse (Mus musculus) as model systems, Syst. Biol., 2010, pp. 262–276.

  63. White, T.A., Wójcik, J.M., and Searle, J.B., Phylogenetic relationships of chromosomal races, in Shrews, Chromosomes and Speciation, Searle, J., Polly, P., and Zima, J., Eds., Cambridge Studies in Morphology and Molecules: New Paradigms in Evolutionary Bio, Cambridge: Cambridge Univ. Press, 2019, Ch. 6, pp. 186–216.

    Google Scholar 

  64. Wójcik, J.M. and Searle, J.B., The chromosome complement of Sorex granarius—The ancestral karyotype of the common shrew (Sorex araneus)?, Heredity, 1988, vol. 61, pp. 225–229.

    Article  PubMed  Google Scholar 

  65. Wójcik, J.M., Chromosome races of the common shrew Sorex araneus in Poland: A model of karyotype evolution, Acta Theriol., 1993, vol. 38, pp. 315–338.

    Article  Google Scholar 

  66. Wójcik, J.M., Ratkiewicz, M., and Searle, J.B., Evolution of the common shrew, Sorex araneus: Chromosomal and molecular aspects, Acta Theriol., 2002, vol. 47, suppl. 1., pp. 139–167.

    Article  Google Scholar 

  67. Zhdanova, N.S., Rogozina, Y.I., Minina, Y.M., et al., Telomeric DNA allocation in chromosomes of common shrew (Sorex araneus, Eulipotyphla), Cell Tissue Biol., 2009, vol. 3, no. 4, pp. 323–329.

    Article  Google Scholar 

  68. Zima, J. and Kral, B., Karyotypes of european mammals I–III, Acta Sci. Nat. Brno, 1984, vol. 18, nos. 7–9.

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ACKNOWLEDGMENTS

The authors thank Elena Sergeevna Gaiduchenko, Senior Researcher, Scientific and Practical Center for Bioresources, National Academy of Sciences of Belarus (Minsk) for her assistance in collection of the specimens on the territory of Belarus (Mogilev oblast).

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

    V. N. Orlov, E. V. Cherepanova & Yu. M. Borisov

  2. Scientific and Practical Center for Bioresources, National Academy of Sciences of Belarus, Minsk, Republic of Belarus

    I. A. Kryshchuk

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  1. V. N. Orlov
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Statement on the welfare of animals. The guidelines for the care and use of animals and pentobarbital euthanasia, approved by the Committee for the Care and Use of Animals of the Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, were followed.

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Orlov, V.N., Kryshchuk, I.A., Cherepanova, E.V. et al. Channelized Karyotype Evolution of the Common Shrew Sorex araneus (Mammalia). Biol Bull Rev 13, 124–139 (2023). https://doi.org/10.1134/S2079086423020056

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