The genetic structure of populations of specially protected mollusk Cepaea vindobonensis (Mollusca, Gastropoda, Pulmonata) in a north-eastern part of the modern area

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Background. The population structure of relict and protected species Cepaea vindobonensis Fer. (Mollusca, Gastropoda, Pulmonata) in a north-eastern part of the modern area has been studied. State population gene pools (11 populations) for environmental activities need to be assessed. 

Materials and Methods. Using allozymes (esterases) and DNA markers (RAPD, ISSR) analysis was performed. The methods polyacrylamide gel electrophoresis and the DNA in the agarose gel were used. 

Results. The populations with a low level of heterozygosity and high heterozygosity were identified. Group located in the east, did not differ in allelic diversity of the western groups. The average expected heterozygosity for allozyme He = 0,217 ± 0,080 and DNA markers He = 0,164 ± 0,024. However, the population of the Austrian snail in the study area is strongly separated from each other (Fst = 0,231, Gst = 0,265, Фst = 0,261-0,263, Nm = 0,630-0,832). The effective population size (Ne), calculated on the basis of the inbreeding coefficient, was level 0,868 ± 0,028 of the total population. The effective population size, calculated on the basis of the linear regression equation between genetic and geographic distance (Ne = 0,36-2,6) and calculated by a factor of subdivision of populations (Ne = 6,3 ± 0,1), in comparison with the effective size of the populations of common species of terrestrial mollusks was the same. 

Conclusion. Thus, on the basis of these data, in general, we can say, the Austrian population snails have a higher potential for life. However, the reduction of allelic diversity, the increase in the coefficient of inbreeding in some groups and a high level of isolation of populations of C. vindobonensis in the north-eastern part of the range is a concern and requires an adjustment in respect of environmental protection measures of this species.

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About the authors

Eduard A. Snegin

Belgorod national research university

Author for correspondence.

Russian Federation Dr. Biol. Sci., senior lecturer, Head of the Laboratory of Population Genetics and Genetoxicology

Elena A Snegina

Belgorod national research university


Russian Federation Researcher of the Laboratory of Population Genetics and Genetoxicology


  1. Литература
  2. Шилейко А.А. Наземные моллюски надсемейства Helicoidea. Фауна СССР. Моллюски. — Л.: Наука, 1978. — Т. 3. — Вып. 6. — 384 с. [Shileiko AA. Terrestrial mollusks superfamily Helicidae. Fauna of the USSR. Shellfish. Leningrad: Nauka; 1978;3(6):384. (In Russ).]
  3. Снегин Э.А. Использование видов наземных моллюсков в качестве индикаторов реликтовых ценозов // Вестник Житомирского педагогического университета. — 2002. — Вып. 10. — С. 128–129. [Snegin EA. The use of species of terrestrial molluscs as a relic cenoses indicators. Vestnik Zhitomirskogo pedagogicheskogo universiteta. 2002;10:128-129. (In Russ).]
  4. Красная книга Белгородской области. Редкие и исчезающие растения, грибы, лишайники и животные. — Белгород, 2004. — 532 с. [The Red Book of the Belgorod region. Rare and endangered plants, fungi, lichens and animals. Belgorod; 2004. 532 p. (In Russ).]
  5. Rotarides M. Über die Bändervariationen von Cepaea vindobonensis Fér Zool Anz. 1926;67(½):28-44.
  6. Jones JS. Environmental selection in the snail Cepaea vindpbonensis in the Lika area of Yugoslavia. Heredity. 1974;32(2):165-170. doi: 10.1038/hdy.1974.20.
  7. Jones JS. The genetic structure of some steppe populations of the snail Cepaea vindobonensis. Genetica. 1975;45:217-225. doi: 10.1007/BF01517198.
  8. Sacchi CF. Population ecology of Cepaea nemoralis and C. vindobonensis along the north Adriatic coasts of Italy. Malacologia. 1984;25(2):315-323.
  9. Хлус Л.М., Хлус К.М. Конхиологичнi особливости буковиньских популяцiй Cepaea vindobonensis Fer. (Geophyla, Helicidae) // Матерiали конф. «Гори I люди (у контекстi сталого развитку)». — Рахiв, 2002. — Т. 2. — С. 522–526. [Khlus LM, Khlus KM. Konkhiologichni osoblivosti bukovin’skikh populyatsii Cepaea vindobonensis Fer. (Geophyla, Helicidae). Materiali konf. “Gori I lyudi (u konteksti stalogo razvitku)” (conference proceedings). Rakhiv; 2002;2:522-526. (In Ukrainian).]
  10. Honek A. Shell-band color polymorphism in Cepaea vindobonensis at the northern limit of its range. Malacologia. 2003;25:133-140.
  11. Сверлова Н.В., Кирпан С.П. Фенетична структура популяцій Cepaea vindobonensis (Gastropoda, Pulmonata, Helicidae) на заході України // Наук. зап. Держ. природозн. музею. — Львів, 2004. — Т. 19. — С. 107–114. [Sverlova NV, Kirpan SP. Phenetic Structure of Populations of Cepaea vindobonensis (Gastopoda, Pulmonata; Helicidae) in Western Ukraine. Naukovi Zapiski DPM. 2004;19:107-114. (In Ukrainian).]
  12. Гураль-Сверлова Н.В., Мартынов В.В. Конхологические особенности популяций Cepaea vindobonensis на территории Донецкой области // Проблемы экологии и охраны природы техногенного региона. — Донецк: Изд-во Донецкого национального ун-та, 2007. — Вып. 7. — С. 85–91. [Gural’-Sverlova NV, Martynov VV. Conchological particular populations of Cepaea vindobonensis on the territory of Donetsk region. In: Problems of Ecology and Nature Protection technogenic region. Donetsk: Publishing House of the Donetsk National University Press; 2007;7:85-91. (In Russ).]
  13. Крамаренко С.С., Хохуткин И.М., Гребенников М.Е. Особенности фенетической структуры наземного моллюска Cepaea vindobonensis в урбанизированных и природных популяциях // Экология. — 2007. — № 1. — С. 42–48. [Kramarenko SS, Khokhutkin IM, Grebennikov ME. Specific Features of Phenetic Structure of the Terrestrial Snail Cepaea vindobonensis (Pulmonata; Helicidae) in Urbanized and Natural Populations. Russian J of Ecology. 2007;38(1):39-45. (In Russ).] doi: 10.1134/S1067413607010079.
  14. Ożgo М, Komorowska А. Shell banding polymorphism in Cepaea vindobonensis in relation to habitat in southeastern Poland. Malacologia. 2009;51(1):81-88. doi: 10.4002/040.051.0105.
  15. Крамаренко С.С. Анализ генетической структуры популяций наземного моллюска Cepaea vindobonensis (Gastropoda, Pulmonata, Helicidae) с использованием RAPD-маркера // Вестник зоологии. — 2009. — Т. 43. — № 5. — С. 449–455. [Kramarenko SS. Analysis of the genetic structure of terrestrial mollusk populations of Cepaea vindobonensis (Gastropoda, Pulmonata, Helicidae) using RAPD-marker. Vestnik zoologii. 2009;43(5):449-455. (In Russ).]
  16. Снегин Э.А. Оценка жизнеспособности популяций особо охраняемого вида Cepaea vindobonensis (Mollusca, Gastropoda, Pulmonata) в условиях юга лесостепи Среднерусской возвышенности // Вестник КрасГАУ. — 2011. — № 11. — С. 142–148. [Snegin EA. Vitality estimation of the Cepaea vindobonensis (Mollusca, Gastropoda, Pulmonata) especially protected species populations in the conditions of the Central Russian Upland forest-steppe south. Vestnik KrasGAU. 2011a;(11):142-148. (In Russ).]
  17. Neiber MT, Hausdorf B. Molecular phylogeny reveals the polyphyly of the snail genus Cepaea (Gastropoda: Helicidae). Mol Phyl and Evol. 2015;93:143-149. doi: 10.1016/j.ympev.2015.07.022.
  18. Neiber MT, Sagorny C, Hausdorf B. Increasing the number of molecular markers resolves the phylogenetic relationship of ‘Cepaea’ vindobonensis (Pfeiffer 1828) with Caucasotachea Boettger 1909 (Gastropoda: Pulmonata: Helicidae). J Zool Syst Evol Res. 2016;54(1):40-45. doi: 10.1111/jzs.12116.
  19. Welsh J, McClelland M. Fingerprinting genomes using CR with arbitrary primers. Nucleic Acids Res. 1990;18(22):7213-7219. doi: 1093/nar/18.24.7213.
  20. Zietkiewicz E, Rafalski A, Labuda D. Genome fingerprinting by simple sequence repeat (SSR) — anchored polymerase chain reaction amplification. Genomics. 1994;20(2):176-181. doi: 10.1006/geno.1994.1151.
  21. Peakall R, Smouse PE. GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes. 2006;(6):288-295.
  22. Yeh FC, Yang R, Boyle TJ, et al. POPGENE32, Microsoft Window-based Freeware for Population Genetic Analysis, Version 1.32; Molecular Biology and Biotechnology Centre, University of Alberta: Edmonton, Canada. 2000.
  23. Tamura K, Stecher G, Peterson D, et al. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Phyl and Evol. 2013;30:2725-2729. doi: 10.1093/molbev/mst197.
  24. Chao A. Species richness estimation. In: Balakrishnan N., Read C.B., Vidakovic B., editors. Encyclopedia of Statistical Science. New York: Wiley; 2005. P. 7907-7916.
  25. Burnham KP, Overton WS. Estimation of the size of a closed population when capture probabilities vary among animals. Biometrika. 1978;(65):625-633. doi: 10.1093/biomet/65.3.625.
  26. Chao А, Shen T-J. 2009. SPADE.
  27. Right S. The genetical structure of populations. Ann Eugenics. 1951;(15):323-354.
  28. Nei M. Molecular population genetics and evolution. Amsterdam; 1975. 278 p.
  29. Excoffier L, Smouse PE, Quattro JM. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics. 1992;(131):479-491.
  30. Ли Ч. Введение в популяционную генетику. — М.: Мир, 1978. — 560 с. [Li C. First course in population genetics. The Boxwood Press. Pacific Grove. California. 1976. 631 p.]
  31. Slatkin M. Isolation by distance in equilibrium and non-equilibrium populations. Evolution. 1993;47(1):
  32. -279. doi: 10.2307/2410134.
  33. Wright S. Random drift and shifting balance theory of evolution. Mathematical Topics in Population Genetics. Berlin: Springer Verlag; 1970. P. 1-31. doi: 10.1007/978-3-642-46244-3_1.
  34. Динамика популяционных генофондов при антропогенных воздействиях / Под ред. Ю. П. Алтухова. — М.: Наука, 2004. — 619 с. [The dynamics of population gene pools under anthropogenic influences. Ed Yu.P. Altukhov. Moscow: Nauka; 2004. P. 619. (In Russ).]
  35. Nei M. Genetic distance between populations. Am Nat. 1972;106(949):283-292. doi: 10.1086/282771.
  36. Майр Э. Зоологический вид и эволюция. — М.: Мир, 1968. — 398 c. [Mayr E. Animal species and evolution. London: Oxford University Press; 1965. 797 p.]
  37. Hanski I. Metapopulation Ecology. Oxford: Oxford University Press; 1999. 328 p.
  38. Crow JF, Morton NE. Measurement of gene frequency drift in small population. Evolution. 1955;9:202-214. doi: 10.2307/2405589.
  39. Crow JF, Kimura M. An introdution to population genetics theory. N.Y.: Harpers and Row; 1970. 591 p.
  40. Снегин Э.А. Генетическая структура популяций модельных видов наземных моллюсков в условиях урбанизированного ландшафта на примере Сhondrula tridens Müll. (Gastropoda, Pulmonata) // Экологическая генетика. — 2011. — Т. IX. — № 2. — С. 54–64. [Snegin EA. The genetic structure of model species populations of terrestrial mollusks in conditions of urbanized landscape using the example of Chondrula tridens Müll (Gastropoda, Pulmonata). Russian J of Genetics: Applied Research. 2012;9(2):160-170.] doi: 10.1134/S2079059712020128.
  41. Снегин Э.А. Пространственные и временные аспекты эколого-генетической структуры популяций беспозвоночных животных (на примере наземных моллюсков и насекомых юга Среднерусской возвышенности): Дис. … д-ра биол. наук. — Белгород: НИУ БелГУ, 2012. — 394 с. [Snegin EA. Spatial and temporal aspects of the ecological and genetic structure of populations of invertebrates (for example, terrestrial mollusks and insects of Southern Central Russian Upland. [dissertation]. Belgorod: BSU; 2012. P. 394 (In Russ).]
  42. Снегин Э.А., Сычев А.А. Оценка жизнеспособности популяций особо охраняемого вида Helicopsis striata Müller (Mollusca, Gastropoda, Pulmonata) в условиях юга Среднерусской возвышенности // Теоретическая и прикладная экология. — 2011. — № 2. — С. 84–93. [Snegin EA, Sichev AA. Assessment of the viability of populations of specially protected species Helicopsis striata Müller (Mollusca, Gastropoda, Pulmonata) in the conditions of the Southern Upland. Teoreticheskaya i prikladnaya ekologiya. 2011;(2):84-93. (In Russ).]
  43. Снегин Э.А., Артемчук О.Ю. Морфогенетический анализ популяций Helix pomatia L. (Pulmonata, Helicidae) юго-восточной и восточной части современного ареала // Экологическая генетика. — 2014. — Т. XII. — № 4. — С. 25–37. [Snegin EA, Artemchuk OYu. Morphogenetic analysis of Helix pomatia L. (Pulmonata, Helicidae) populations from south-eastern and eastern parts of the modern area. Russian J of Genetics: Applied Research. 2016;6(2):152-162.] doi: 10.1134/S207905971602012X.
  44. Снегин Э.А. Оценка состояния популяционных генофондов наземных моллюсков в условиях влияния горнообогатительных комбинатов на примере Bradybaena fruticum Müll. (Gastropoda, Pulmonata) // Экологическая генетика. — 2010. — Т. VIII. — № 2. — С. 45–55. [Snegin EA. Assessment of the state of population gene pools of terrestrial mollusks in conditions of influence of ore dressing combines from the example of Bradybaena fruticum Müll. (Gastropoda, Pullmonata). Russian J of Genetics: Applied Research. 2011;1(5):379-389.] doi: 10.1134/S2079059711050133.
  45. Снегин Э.А. Анализ генетической изменчивости популяций наземного моллюска Сhondrula tridens Müll. (Gastropoda, Pulmonata) с использованием RAPD- и ISSR-маркеров // Экологическая генетика. — 2013. — T. XI. — № 3. — С. 37–47. [Snegin EA. Analysis of genetic variability in populations of a terrestrial snail Chondrula tridens Müll. (Gastropoda, Pulmonata), based on the RAPD and ISSR markers. Russian J of Genetics: Applied Research. 2014;4(5):444-454.] doi: 10.1134/S207905971405013X.
  46. Снегин Э.А. Оценка состояния популяционных генофондов особо охраняемого вида Helicopsis striata (Mollusca, Gastropoda, Pulmonata) на основе ДНК-маркеров // Экологическая генетика. — 2015. — Т. XIII. — № 3 — С. 28–39. [Snegin EA. Assessment of the state population gene pool of specially protected species Helicopsis striata (Mollusca, Gastropoda, Pulmonata) using DNA-markers.Ecologicheskaya Genetika. 2015;13(3):28-39. (In Russ).].

Supplementary files

Supplementary Files Action
The collection points of the C. vindobonensis

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Fig. 2. RAPD- and ISSR-DNA patterns of the C. vindobonensis

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Fig. 3. The dendrogram of genetic distances by Nei [33] (UPGMA) between populations of the C. vindobonensis at allozyme loci (a) and DNA markers (b)

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Fig. 4. The linear regression logarithm of gene flow Nm between the populations pairs C. vindobonensis on logarithm geographic distance Dg between them (a — for Allozymes, b — for DNA markers)

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Fig. 5. The ratio of expected (Не) and observed heterozygosity (Но) in the populations of C. vindobonensis

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