Weak Population Genetic Structure of the Eurasian Crane  Grus grus  L.

E. A. Mudrik; Мудрик Е. А.; E. I. Ilyashenko; Ильяшенко Е. И.; V. Yu. Ilyashenko; Ильяшенко В. Ю.; P. A. Kazimirov; Казимиров П. А.; A. V. Shatokhina; Шатохина А. В.; T. А. Kashentseva; Кашенцева Т. А.; K. D. Kondrakova; Кондракова К. Д.; K. A. Postelnykh; Постельных К. А.; Yu. M. Markin; Маркин Ю. М.; D. V. Politov; Политов Д. В.

doi:10.31857/S0016675823120068

Weak Population Genetic Structure of the Eurasian Crane Grus grus L.

Authors: Mudrik E.A.¹, Ilyashenko E.I.¹^,2, Ilyashenko V.Y.², Kazimirov P.A.¹, Shatokhina A.V.¹, Kashentseva T.А.³, Kondrakova K.D.¹^,2, Postelnykh K.A.³, Markin Y.M.³, Politov D.V.¹
Affiliations:
1. Vavilov Institute of General Genetics Russian Academy of Sciences
2. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences
3. Oka State Nature Biosphere Reserve
Issue: Vol 59, No 12 (2023)
Pages: 1407-1418
Section: ГЕНЕТИКА ЖИВОТНЫХ
URL: https://journals.rcsi.science/0016-6758/article/view/233640
DOI: https://doi.org/10.31857/S0016675823120068
EDN: https://elibrary.ru/QDIEVG
ID: 233640

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Abstract
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Abstract

The article presents an extended (as compared with our previous studies) analysis of the population genetic structure of a migratory wide-range bird species with a high abundance, the Eurasian Crane Grus grus L. Using seven highly polymorphic microsatellite loci, high and very similar values of genetic diversity parameters were obtained in the samples of both the western (G. g. grus) and eastern (G. g. lilfordi) subspecies. Coefficients of genetic differentiation between these subspecies (F_ST = 0.008, G_ST = 0.002) were also found to be low. According to AMOVA, 99% of genetic variation of G. grus is attributed to individual levels. Using the Bayesian clustering algorithm implemented in STRUCTURE software, no clear population-genetic structuring of the species was revealed. However, visualization of spatial patterns of genetic variability in Geneland showed the presence of a cluster of “pure” subspecies G. g. grus and G. g. lilfordi surrounding a cluster of individuals from the zone of intergradation of these subspecies. This result, along with the observed very low F_ST values, may indicate subtle genetic differences between cranes from the studied area, possibly having a mutational nature. The lower allelic richness and lack of private alleles in the eastern subspecies suggest that G. g. lilfordi is relatively evolutionary young and suggest its recent origin from some eastern marginal populations of the nominative western subspecies.

Keywords

Gruidae, genetic variability, genetic differentiation, microsatellite loci, Russia.

References

Prange H., Ilyashenko E.I. Eurasian crane // Crane Conservation Strategy. Baraboo, Wisconsin, USA: Int. Crane Foundation, 2019. P. 397–423.
Bird Life International. 2016. Grus grus. The IUCN Red List of Threatened Species 2016. https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T2-2692146A86219168.en
Ильяшенко В.Ю. О систематике серого журавля // Журавли Евразии (биология, распространение, миграция, управление). 2011. Вып. 4. С. 93–103.
Ильяшенко В.Ю., Белялов О.В. Новый подвид серого журавля Grus grus korelovi ssp. n. (Aves: Gruidae) из Центрального и Восточного Тянь-Шаня // Русс. орнитол. журн. 2011. Т. 20. № 687. С. 1803–1811.
Ильяшенко В.Ю., Касабян М.Г., Маркин Ю.М. Морфологическая изменчивость серого журавля – Grus grus (Linnaeus, 1758) (Aves: Gruidae) // Журавли Евразии (биология, распространение, миграции). 2008. Вып. 3. С. 50–82.
Crane conservation strategy / Eds Mirande C.M., Harris J.T. Baraboo, Wisconsin, USA: Int. Crane Foundation, 2019. 454 p.
Ilyashenko E., Markin Y. Changing of the Eurasian crane staging areas distribution in the European part of Russia from 1982 to 2007 // Proc. of the Cranes, Agriculture, and Climate Change Workshop (Muraviovka Park. Russia, 28 May–3 June, 2010). 2012. P. 88–99.
Пранге Х. Распространение и миграции серого журавля на западноевропейском пролетном пути // Журавли Евразии (биология, распространение, разведение). М.–Н. Цасучей: Изд-во “Белый ветер”. 2015. Вып. 5. С. 287‒312.
Ильяшенко Е.И. Оценка численности журавлей (Gruiformes, Gruidae) Северной Евразии в начале 21 века // Зоол. журнал. 2016. Т. 95. № 8. P. 976–980. https://doi.org/10.7868/S0044513416080043
Hasegawa O., Ishibashi Y., Abe S. Isolation and characterization of microsatellite loci in the red-crowned crane Grus japonensis // Mol. Ecol. 2000. V. 9. № 10. P. 1677–1678.
Jones K.L., Henkel J.R., Howard J.J. et al. Isolation and characterization of 14 polymorphic microsatellite DNA loci for the endangered whooping crane (Grus americana) and their applicability to other crane species // Conserv. Gen. Res. 2010. V. 2. № 1. P. 251–254. https://doi.org/10.1007/s12686-010-9196-3
Meares K., Dawson D., Horsburgh G. et al. Characterisation of 14 blue crane Grus paradisea (Gruidae, AVES) microsatellite loci for use in detecting illegal trade // Conserv. Genet. 2008. V. 9. P. 1363–1367. https://doi.org/10.1007/s10592-007-9490-0
Мудрик Е.А., Кашенцева Т.А., Редчук П.С., Политов Д.В. Данные по микросателлитной изменчивости подтверждают низкую генетическую дифференциацию западного и восточного подвидов серого журавля (Grus grus L.) // Мол. биология. 2015. Т. 49. № 2. С. 297–304. https://doi.org/10.7868/S002689841502010X
Ильяшенко Е.И., Ильяшенко В.Ю., Викельски М., Цао Л. Предварительные результаты слежения за серыми журавлями, помеченными в европейской части России и Западной Сибири в 2019–2021 гг. // Инф. бюлл. РГЖЕ. 2022. № 16. С. 157–169.
Zhang L., Zhang Z., Shen F. et al. Identification and characterization of polymorphic microsatellite loci in the red-crowned crane // Genet. Mol. Res. 2015. V. 14. № 4. P. 15169–15176. https://doi.org/10.4238/2015.November.25.5
Krajewski C., Sipiorski J.T., Anderson F.E. Complete mitochondrial genome sequences and the phylogeny of cranes (Gruiformes: Gruidae) // Auk. 2010. V. 127. № 2. P. 440–452. https://doi.org/10.1525/auk.2009.09045
Lazar I., Jr., Lazar I., Sr. GelAnalyzer 19.1. www.gelanalyzer.com
Van Oosterhout C., Hutchinson W.F., Wills D.P., Shipley P. MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data // Mol. Ecol. Notes. 2004. V. 4. № 3. P. 535–538. https://doi.org/10.1111/J.1471-8286.2004.00684.X
Peakall R., Smouse P.E. GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research – an update // Bioinformatics. 2012. № 28. P. 2537–2539. https://doi.org/10.1093/bioinformatics/bts460
Pritchard J.K., Stephens M., Donnelly P. Inference of population structure using multilocus genotype data // Genetics. 2000. V. 155. № 2. P. 945–959. https://doi.org/10.3410/f.1015548.197423
Guillot G., Estoup A., Mortier F., Cosson J.F. A spatial statistical model for landscape genetics // Genetics. 2005. V. 170. № 3. P. 1261–1280. 10.1534/genetics.104.033803' target='_blank'>http://doi.org/doi: 10.1534/genetics.104.033803
Guillot G., Mortier F., Estoup A. Geneland: A program for landscape genetics // Mol. Ecol. Notes. 2005. V. 5. № 3. P. 712–715. 10.1111/j.1471-8286.2005.01031.x' target='_blank'>http://doi.org/doi: 10.1111/j.1471-8286.2005.01031.x
Guillot G. Inference of structure in subdivided populations at low levels of genetic differentiation. The correlated allele frequencies model revisited // Bioinformatics. 2008. V. 24. P. 2222–2228. https://doi.org/10.1093/bioinformatics/btn419
Guillot G., Renaud S., Ledevin R. et al. Unifying model for the analysis of phenotypic, genetic and geographic data // System. Biol. 2012. V. 61. № 6. P. 897–911. https://doi.org/10.1093/sysbio/sys038
Guillot G., Santos F. A computer program to simulate multilocus genotype data with spatially auto-correlated allele frequencies // Mol. Ecol. Res. 2009. V. 9. № 4. P. 1112–1120.
Guillot G., Santos F. Using AFLP markers and the Geneland program for the inference of population genetic structure // Mol. Ecol. Res. 2010. V. 10. № 6. P. 1082–1084. https://doi.org/10.1111/j.1755-0998.2010.02864.x
Guillot G., Santos F., Estoup A. Analysing georeferenced population genetics data with Geneland: A new algorithm to deal with null alleles and a friendly graphical user interface // Bioinformatics. 2008. V. 24. № 11. P. 1406–1414. https://doi.org/10.1093/bioinformatics/btn136
Guillot G., Santos F., Estoup A. Population genetics analysis using R and the Geneland program. Lyngby, Denmark: Technical University of Denmark, 2011.
Evanno G., Regnaut S., Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study // Mol. Ecol. 2005. V. 14. № 8. P. 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Kopelman N.M., Mayzel J., Jakobsson M. et al. Clumpak: A program for identifying clustering modes and packaging population structure inferences across K // Mol. Ecol. Res. 2015. V. 15. № 5. P. 1179–1191. https://doi.org/10.1111/1755-0998.12387
Anselin L., Syabri I., Kho Y. GeoDa: An introduction to spatial data analysis // Handbook of Applied Spatial Analysis: Software Tools, Methods and Applications. Berlin, Heidelberg: Springer, 2010. P. 73–89. https://doi.org/10.1007/978-3-642-03647-7_5
Schnute J.T., Boers N., Haigh R. et al. PBS mapping: Mapping Fisheries Data and Spatial Analysis Tools // Fisheries and Oceans Canada. 2022. https://github.com/pbs-software/pbs-mapping
R CoreTeam. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria: 2021. https://www.R-project.org
Мевес В. Постоянство использования гнездовых участков журавлями в округе Мекленбург-Западная Померания (Северо-Восточная Германия) // Журавли Евразии: биология, охрана, управление. М., Цасучей: Изд-во “Белый ветер”, 2015. Вып. 5. С. 68–76.
Кондракова К.Д., Маркин Ю.М., Постельных К.А. и др. Перемещения неполовозрелых серых журавлей в центре европейской части России // Орнитология. 2021. Т. 45. С. 75–80.
Sviridova T.V., Grinchenko O.S., Wikelski M., Ilyashenko E.I. Geographical connectivity, migration routes, and wintering grounds of the common crane in the Northern Moscow Region // Arid Ecosystems. 2023. V. 13. № 2. P. 196–207. https://doi.org/10.1134/S2079096123020142
Hayes M.A. Dispersal and Population Genetic Structure in Two Flyways of Sandhill Cranes (Grus canadensis). Madison, Wisconsin (US): The University of Wisconsin-Madison. 2015. 277 p.
Nesbitt S.A., Schwikert S.T., Folk M.J. Natal dispersal in Florida sandhill cranes // J. Wildl. Manage. 2002. P. 349–352.
Haase M., Höltje H., Blahy B. et al. Shallow genetic population structure in an expanding migratory bird with high breeding site fidelity, the western eurasian crane Grus grus grus // J. Ornithol. 2019. V. 160. P. 965–972. https://doi.org/10.1007/s10336-019-01688-1
Mudrik E.A., Ilyashenko E.I., Goroshko O.A. et al. The demoiselle crane (Anthropoides virgo) population genetic structure in Russia // Vavilov J. Genetics and Breeding. 2018. V. 22. № 5. P. 586–592. https://doi.org/10.18699/VJ18.398
Мудрик Е.А., Горошко О.А., Сурмач С.Г. и др. Однородность генофонда западной и восточной популяций даурского журавля Antigone vipio на разных пролетных путях // Генетика. 2022. Т. 58. № 5. С. 570–580. https://doi.org/10.31857/S001667582205006X
Мудрик Е.А., Политов Д.В. Молекулярно-генетические подходы в изучении и сохранении популяционных генофондов журавлей (Gruidea, Aves) // Усп. соврем. биологии. 2022. Т. 142. № 5. P. 477–486. https://doi.org/10.31857/S004213242205009X
Parau L.G., Wink M. Common patterns in the molecular phylogeography of western palearctic birds: A comprehensive review // J. Ornithol. 2021. V. 162. P. 937–959. https://doi.org/10.1007/s10336-021-01893-x
Haase M., Ilyashenko V. A glimpse on mitochondrial differentiation among four currently recognized subspecies of the common crane Grus grus // Ardeola. 2012. V. 59. № 1. P. 131–136. https://doi.org/10.13157/arla.59.1.2012.131