Structure of the hybrid zone between allied species of the common vole, Microtus arvalis and M. obscurus: Influence of genetic factors and landscape-geographic conditions

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Patterns of introgression of several genetic markers across the hybrid zone between allied species of the common vole Microtus arvalis s. str. и M. obscurus were studied in four its sections: in northwest Nizhny Novgorod region, east Vladimir and southwest of Nizhny Novgorod regions, south Lipetsk region, and northwest Voronezh region. Analysis of the clinal variability for three molecular-genetic markers (cytb, tp53, SMCY11) and for karyotypes showed a structural similarity between the “Vladimir – Nizhny Novgorod”, “Nizhny Novgorod”, and “Voronezh” sections. The maximal width was shown for the cytb cline, the minimal width – for the SMCY11 cline; the tp53 cline and chromosomal cline occupy intermediate position for this parameter. Furthermore, in these transects the centre of the cline for the cytb is shifted southeastward (into the distribution range of M. obscurus) from the centres of three other clines. The revealed asymmetric introgression of mitochondrial genome from M. arvalis to M. obscurus may be explained by the fact that the hybrid zone was formed as a result of invasion of M. obscurus into the range of M. arvalis. The “Lipetsk” transect differs from three above-mentioned transects by very narrow clines with nearly coinciding centres. Such characteristics of the “Lipetsk” transect are obviously caused by localization of the hybrid zone in this section along river Voronezh. The obtained results led us to suppose that the structure of the studied hybrid zone is determined mainly by coinciding (or non-coinciding) of its centre with local physical barriers.

Full Text

Restricted Access

About the authors

L. A. Lavrenchenko

Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences

Author for correspondence.
Email: llavrenchenko@gmail.com
Russian Federation, Moscow, 119071

A. R. Gromov

Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences

Email: llavrenchenko@gmail.com
Russian Federation, Moscow, 119071

A. A. Martynov

Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences

Email: llavrenchenko@gmail.com
Russian Federation, Moscow, 119071

D. S. Kostin

Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences

Email: llavrenchenko@gmail.com
Russian Federation, Moscow, 119071

V. A. Komarova

Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences

Email: llavrenchenko@gmail.com
Russian Federation, Moscow, 119071

D. M. Krivonogov

Lobachevsky State University of Nizhny Novgorod (Arzamas Branch)

Email: llavrenchenko@gmail.com
Russian Federation, Arzamas, 607220

E. V. Cherepanova

Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences

Email: llavrenchenko@gmail.com
Russian Federation, Moscow, 119071

References

  1. Hewitt G.M. Hybrid Zones – Natural laboratories for evolutionary studies // Trends Ecol. Evol. 1988. V. 3. P. 158–167.
  2. Булатова Н.Ш., Голенищев Ф.Н., Ковальская Ю.М. и др. Цитогенетическое изучение парапатрической зоны контакта двух 46-хромосомных форм обыкновенной полевки в Европейской России // Генетика. 2010. Т. 46. № 4. С. 502–508. https://doi.org/10.1134/S1022795410040095
  3. Баскевич М.И., Окулова Н.М., Потапов С.Г. и др. Новые данные о распространении видов-двойников и гибридизации 46-хромосомных форм Microtus arvalis sensu lato (Rodentia, Arvicolinae) в Центральном Черноземье // Зоол. журн. 2012. Т. 91. № 8. С. 994–1005.
  4. Баскевич М.И., Миронова Т.А., Черепанова Е.В., Кривоногов Д.М. Новые данные по хромосомной изменчивости видов-двойников и гибридизации 46-хромосомных форм Microtus arvalis sensu lato (Rodentia, Arvicolinae) в Верхнем Поволжье // Зоол. журн. 2016. Т. 95. № 9. С. 1096–1107. https://doi.org/10.1134/S1062359016110042
  5. Stojak J., McDevitt A.D., Herman J.S. et al. Between the Balkans and the Baltic: Phylogeography of a common vole mitochondrial DNA lineage limited to central Europe // PLoS One. 2016. V. 11. № 12. https://doi.org/10.1371/journal.pone.0168621
  6. Tougard C., Montuire S., Volobouev V. et al. Exploring phylogeography and species limits in the Altai vole (Rodentia: Cricetidae) // Biol. J. Linnean Society. 2013. V. 108. № 2. P. 434–452. https://doi.org/10.1111/j.1095-8312.2012.02034.x
  7. Сибиряков П.А., Товпинец Н.Н., Дупал Т.А. и др. Филогеография обыкновенной полевки Microtus arvalis (Rodentia, Arvicolinae) формы obscurus: новые данные по изменчивости митохондриальной ДНК // Генетика. 2018. Т. 54. № 10. С. 1162–1176. https://doi.org/10.1134/S1022795418100137
  8. Голенищев Ф.Н., Мейер М.Н., Булатова Н.Ш. Гибридная зона между двумя кариоморфами Microtus arvalis (Rodentia, Arvicolidae) // Тр. Зоол. ин-та РАН. 2001. Т. 289. С. 89–94.
  9. Лавренченко Л.А., Потапов С.Г., Булатова Н.Ш., Голенищев Ф.Н. Изучение естественной гибридизации двух форм обыкновенной полевки (Microtus arvalis) молекулярно-генетическими и цитогенетическими методами // Докл. РАН. 2009. Т. 426. № 1. С. 135–138.
  10. Lavrenchenko L.A., Gromov A.R., Martynov A.A. et al. Genetic, chromosomal and phenotypic variation across a hybrid zone between two common vole species (Microtus arvalis and M. obscurus) // Hystrix. 2023. V. 34. № 1. P. 24–32. https://doi.org/10.4404/hystrix-00588-2022
  11. Малыгин В.М. Сравнительный морфологический анализ кариотипов двух географических форм 46-хромосомной обыкновенной полевки (Microtus arvalis) // Зоол. журн. 1974. Т. 53. № 5. С. 769–777.
  12. Král B., L’apunova E.A. Karyotypes of 46-chromosome Microtus arvalis (Microtinae, Rodentia) // Zool. Listy. 1975. V. 24. P. 1–11.
  13. Воронцов Н.Н., Ляпунова Е.А., Белянин А.Н. и др. Сравнительно-генетические методы диагностики и оценки степени дивергенции видов-двойников Microtus arvalis и Microtus epiroticus // Зоол. журн. 1984. Т. 63. № 10. С. 1555–1565.
  14. Мейер М.Н., Голенищев Ф.Н., Раджабли С.И., Саблина О.В. Серые полевки (подрод Microtus Schrank) фауны России и сопредельных территорий. СПб.: Зоол. ин-т РАН, 1996. 320 с.
  15. Раджабли С.И., Графодатский А.С. Эволюция кариотипов млекопитающих (структурные перестройки хромосом и гетерохроматин) // Цитогенетика гибридов, мутации и эволюция кариотипа. Новосибирск: Наука, 1977. С. 231–248.
  16. Козловский А.И., Булатова Н.Ш., Новиков А.Д. Двойной эффект инверсии в кариотипе обыкновенной полевки // Докл. АН СССР. 1988. T. 298. № 4. С. 994–997.
  17. Fink S., Excoffier L., Heckel G. Mitochondrial gene diversity in the common vole Microtus arvalis shaped by historical divergence and local adaptations // Mol. Ecol. 2004. V. 13. № 11. P. 3501–3514. https://doi.org/10.1111/j.1365-294X.2004.02351.x
  18. Булатова Н.Ш., Потапов С.Г., Лавренченко Л.А. Геномная и хромосомная политипия в исследовании маркеров митохондриальной и ядерной ДНК у обыкновенных полевок (группа Microtus arvalis) // Генетика. 2010. Т. 46. № 5. С. 668–676 https://doi.org/10.1134/S1022795410050121
  19. Ford C.E., Hamerton J.L. A colchicine, hypotonic citrate, squash sequence for mammalian chromosomes // Stain Technol. 1956. V. 31. № 6. P. 247–251. https://doi.org/10.3109/10520295609113814
  20. The R Project for Statistical Computing. URL https://www.r-project.org.
  21. Derryberry E.P., Derryberry G.E., Maley J.M., Brumfield R.T. HZAR: Hybrid zone analysis using an R software package // Mol. Ecol. Resources. 2014. V. 14. № 3. P. 652–663. https://doi.org/10.1111/1755-0998.12209
  22. Георгиевский А.Б. К истории закона Харди–Вейнберга // Историко-биологические исследования. 2011. Т. 3. № 1. C. 63–75.
  23. Nance V., Vanlerberghe F., Nielsen J.T. et al. Chromosomal introgression in house mice from the hybrid zone between M. m. domesticus and M. m. musculus in Denmark // Biol. J. Linnean Society. 1990. V. 41. № 1-3. P. 215–227. https://doi.org/10.1111/j.1095-8312.1990.tb00831.x
  24. Fel-Clair F., Lenormand T., Catalan J. et al. Genomic incompatibilities in the hybrid zone between house mice in Denmark: Evidence from steep and non-coincident chromosomal clines for Robertsonian fusions // Genet. Res. Camb. 1996. V. 67. № 2. P. 123–134. https://doi.org/10.1017/S0016672300033589
  25. Petit R.J., Excoffier L. Gene flow and species delimitation // Trends Ecol. Evol. 2009. V. 24. P. 386–393. https://doi.org/10.1016/j.tree.2009.02.011
  26. Gauffre B., Petit E., Brodier S. et al. Sex-biased dispersal patterns depend on the spatial scale in a social rodent // Proc R. Soc. B. 2009. V. 276. P. 3487–3494. https://doi.org/10.1098/rspb.2009.0881
  27. Beysard M., Krebs-Wheaton R.K., Heckel G. Tracing reinforcement through asymmetrical partner preference in the European common vole Microtus arvalis // BMC Evol. Biol. 2015. V. 15. P. 170–181. https://doi.org/10.1186/s12862-015-0455-5
  28. Vanlerberghe F., Dod B., Boursot P. et al. Absence of Y-chromosome introgression across the hybrid zone between Mus musculus domesticus and Mus musculus musculus // Genet. Res. 1986. V. 48. P. 191–197.
  29. Haldane J.B.S. Sex ratio and unisexual sterility in hybrid animals // J. Genetics. 1922. V. 12. № 2. P. 101–109.
  30. Currat M., Ruedi M., Petit R.J., Excoffier L. The hidden side of invasions: massive introgression by local genes // Evolution. 2008. V. 62. № 8. P. 1908–1920. https://doi.org/10.1111/j.1558-5646.2008.00413.x
  31. Excoffier L., Foll M., Petit R.J. Genetic consequences of range expansions // Ann. Rev. Ecol. Evol. Syst. 2009. V. 40. P. 481–501. https://doi.org/10.1146/annurev.ecolsys.39.110707.173414
  32. Mastrantonio V., Porretta D., Urbanelli S. et al. Dynamics of mtDNA introgression during species range expansion: insights from an experimental longitudinal study // Sci. Rep. 2016. V. 6. P. 303–355. https://doi.org/10.1038/srep30355
  33. Toews D.P.L., Brelsford A. The biogeography of mitochondrial and nuclear discordance in animals // Mol. Ecol. 2012. V. 21. № 16. P. 3907–3930. https://doi.org/10.1111/j.1365-294X.2012.05664.x
  34. Drovetski S.V., Semenov G., Red’kin Y.A. et al. Effects of asymmetric nuclear introgression, introgressive mitochondrial sweep, and purifying selection on phylogenetic reconstruction and divergence estimates in the Pacific clade of Locustella warblers // PLoS One. 2015. V. 10. № 4. https://doi.org/10.1371/journal.pone.0122590
  35. Levanen R., Kunnasranta M., Pohjoismaki J. Mitochondrial DNA introgression at the northern edge of the brown hare (Lepus europaeus) range // Ann. Zool. Fenn. 2018. V. 55. P. 15–24. https://doi.org/10.5735/086.055.0103
  36. Kinoshita G., Nunome M., Kryukov A.P. et al. Contrasting phylogeographic histories between the continent and islands of East Asia: Massive mitochondrial introgression and long-term isolation of hares (Lagomorpha: Lepus) // Mol. Phylogenet. and Evol. 2019. V. 136. P. 65–75. https://doi.org/10.1016/j.ympev.2019.04.003
  37. Саблина С.А., Белозерцева И.В. Поведение самцов обыкновенной полевки (Microtus arvalis) хромосомных форм arvalis и obscurus в тестах предпочтения ольфакторных сигналов и открытое поле // Зоол. журн. 2012. Т. 91. № 2. С. 208–218.
  38. Саблина С.А., Тихонова Е.П., Белозерцева И.В. Поведение самцов обыкновенной полевки (Microtus arvalis Pallas, 1779) хромосомных форм “arvalis” и “obscurus” в тесте “перегородка” // Тр. Зоол. ин-та РАН. 2017. Т. 321. № 2. С. 218–227. https://doi.org/10.31610/trudyzin/2017.321.2.218
  39. Hewitt G.M. The subdivision of species by hybrid zones // Speciation and Its Consequences. / Eds Otte D., Endler J, Sunderland, Massachusetts: Sinauer Associates, 1989. С. 85–110.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. The hybridization zone between 46-chromosomal species of the common vole (Microtus arvalis S. str. and M. obscurus) and the transects considered through this zone. Solid curved lines show the traced position of the GZ, the dotted line shows the intended position of the GZ. The straight segments show the transects: 1 – “Nizhny Novgorod”, 2 – “Vladimirsko-Nizhny Novgorod", 3 – “Lipetsk” and 4 – “Voronezh".

Download (66KB)
Indexing metadata
3. Fig. 2. Transects (shown in straight lines) through the hybrid zone between Microtus arvalis S. str. and M. obscurus: a – “Nizhny Novgorod”, b – “Vladimirsko-Nizhny Novgorod", c – “Lipetsk", d – “Voronezh". The numbering of the capture sites corresponds to that in the additional materials. The height of the relief is shown in gradient color: black is the lowest, light gray is the highest.

Download (114KB)
Indexing metadata
4. Fig. 3. Wedges of four genetic traits diagnostic for Microtus arvalis S. str. and M. obscurus, identified on four transects under consideration through the hybridization zone between these species. Different shades of gray indicate 95% confidence intervals (2LL low-high) for each wedge. cytb is a mitochondrial gene, tp53 is a nuclear gene, SMCY11 is a marker of the Y chromosome, chromosomes are a “hybrid” chromosome index. ARV – M. arvalis s. str., OBS – M. obscurus.

Download (79KB)
Indexing metadata
5. Additional table
Download (133KB)
Indexing metadata

Copyright (c) 2024 Russian Academy of Sciences