Assessment of the state of population gene pools of the slightly mobile animal species on the example of the land snail Bradybaena fruticum Müll. (Gastropoda, Pulmonata) based on the DNA markers

Cover Page

Cite item

Full Text

Abstract

Using the polymorphic DNA markers (RAPD and ISSR), the genetic structure was examined and the viability of 26 populations of the terrestrial gastropod Bradybaena (Fruticicola) fruticum Müll., most of which lives in the south of the Central Russian Upland, was estimated. Samples from Romania, the Urals and Vyatka regions for comparison were taken. In total, 1153 individuals were examined. The level of expected heterozygosity averaged He = 0.208 ± 0.028, the Shannon index Ish = 0.320 ± 0.039. The lowered level of variability, both actual and theoretically expected (estimated by the methods of Chao1-bc and 1st order jackknife) in groups of anthropogenically disturbed biotopes inhabiting the zones of industrial enterprises is noted. The indices of the genetic disunity of the populations were Fst = 0.298, Gst = 0.254, and the level of the gene flow Nm = 0.708. The cluster analysis and the Mantel correlation coefficient Rm = –0.024 showed the absence of a reliable relationship between the geographic and genetic distance between populations, which indicates the violation of the isolation model by distance and confirms the thesis advanced earlier that the urbanized forest-steppe landscape disrupts the natural migration processes, leads to the strong isolation and of the genetic drift in populations of snails. At the same time, the observed phenomenon of increasing the degree of subdivision of populations against the background of a decrease in the allelic diversity noted by us in many groups of bush snail can be regarded as the shift of genetic equilibrium toward increasing interpopopulation diversity (according to Wright's model). The calculation of the effective population size with the help of the Slatkin model turned out to be the lowest of the background mollusks in the study area (Ne = 0.39-0.83). However, the level of the effective population size calculated with the subdivision index (Fst and Gst) was equal to 6.2 and 7.3, respectively, which is comparable with other species of mollusks.

About the authors

Eduard A. Snegin

Belgorod State National Research University

Author for correspondence.
Email: snegin@bsu.edu.ru

Dr. Biol. Sci., the senior lecturer, the director of the research center of genomic selection

Russian Federation, 85, Pobeda street, Belgorod, 308015

Elena A. Snegina

Belgorod State National Research University

Email: snegina@bsu.edu.ru

Researcher of the research center of genomic selection

Russian Federation, 85, Pobeda street, Belgorod, 308015

References

  1. Ланде Р., Бэрроуклаф Д. Эффективная численность популяций, генетическая изменчивость и их использование для управления популяциями // Жизнеспособность популяций: Природоохранные аспекты. – М.: Мир, 1989. – С. 117–157. [Lande R, Barroclough D. Effective Population Number, Genetic Variability and Their Use for Population Management. In Viability of Populations: Environmental Aspects. Moscow: Mir; 1989. P. 117-157. (In Russ.)]
  2. Кантор Ю.И., Сысоев А.В. Каталог моллюсков России и сопредельных стран. – М.: Т-во научных изданий КМК, 2005. – 627 с. [Cantor YI, Sysoev AV. Mollusks catalog of Russia and neighboring countries. Moscow: The Association of Scientific Publications KMK; 2005. 627 p. (In Russ.)]
  3. Зейферт Д.В., Хохуткин И.М. Экология кустарниковой улитки Fruticicola fruticum. – М.: Т-во научных изданий КМК, 2010. – 92 с. [Seifert DV, Khokhutkin IM. Ecology of the bush snail Fruticicola fruticum. Moscow: The Association of Scientific Publications KMK; 2010. 92 p. (In Russ.)]
  4. 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. Vol. 3. Issue 6. P. 384. (In Russ.)]
  5. Удалой А.В. К вопросу о распространении кустарниковой улитки Fruticicola fruticum (Müller, 1774) на юге Западной Сибири / Материалы 4-й международной науч.-практ. конференции «Сохранение разнообразия животных и охотничье хозяйство России». – М., 2011. – С. 104–106. [Udaloy AV. On the distribution of the bush snail Fruticicola fruticum (Müller, 1774) in the south of Western Siberia. (Proceedings of the 4th international scientific-practical conference.) “Conservation of animal diversity and hunting in Russia”. Moscow; 2011. P. 104-106. (In Russ.)]
  6. Снегин Э.А. Структура расселенности Bradybaena fruticum (Mollusca, Gastropoda, Pulmonata) в условиях юга лесостепной зоны Русской равнины: автореф. дис. … канд. биол. наук. – М., 1999. [Snegin EA. Structure of the settlement of Bradybaena fruticum (Mollusca, Gastropoda, Pulmonata) in the conditions of the south of the forest-steppe zone of the Russian Plain. [dissertation] Moscow; 1999. (In Russ.)]
  7. Хохуткин И.М. Структура изменчивости видов на примере наземных моллюсков. – Екатеринбург: УрО РАН, 1997. – 175 с. [Khokhutkin IM. Species Variability Structure as Exemplified by Terrestrial Snails: UrB RAS; 1997. 175 p. (In Russ.)]
  8. Матёкин П.В., Макеева В.М. Полиморфная система эстераз и пространственная структура вида у кустарниковой улитки (Bradybaena fruticum Müll.) // Журнал общей биологии. – 1977. – Т. 38. – № 6. – С. 908–913. [Matekin PV, Makeeva VM. Polymorphic Esterase System and the Spatial Structure of the Species in the bush snail (Bradybaena fruticum Müll.). Zh Obshch Biol. 1977;38(6):908-913. (In Russ.)]
  9. Макеева В.М., Белоконь М.М., Малюченко О.П. Оценка состояния генофонда природных популяций беспозвоночных животных в условиях фрагментарного ландшафта Москвы и Подмосковья (на примере кустарниковой улитки Bradybaena fruticum (Müll) // Генетика. – 2005. – Т. 41. – № 11. – С. 1495–1510. [Makeeva VM, Belokon MM, Malyuchenko OP. Estimating the Gene Pool Condition in Natural Populations of Invertebrates in the Fragmented Landscape of Moscow and Moscow Region with Special Reference to Bush Snail Bradybaena fruticum Müll. Russian Journal of Genetics. 2005;41(11):1230-1244. (In Russ., Eng.)]
  10. Falniowski A, Szarowska M, Witkowska-Pelc E. Intra- and interpopulation genetic differentiation and gene flow in a group of isolated populations of Bradybaena fruticum (Müller, 1774) in South Poland. Journal of Zoological Systematics and Evolutionary Research. 2004;42(1):70-80.
  11. Welsh J, McClelland M. Fingerprinting genomes using CR with arbitrary primers. Nucleic Acids Res. 1990;18(22):7213-7219. doi: 10.1093/nar/18.24.7213.
  12. 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.
  13. Снегин Э.А. Эколого-генетические аспекты расселения Bradybaena fruticum (Mollusca, Gastropoda, Pullmonata) в элементах лесостепного ландшафта // Экология. – 2005. – № 1. – С. 39–47. (Snegin EA. Ecological and Genetic Characteristics of the Distribution of Bradybaena fruticum (Mollusca, Gastropoda, Pullmonata) in a Forest-Steppe Landscape. Russian Journal of Ecology. 2005;36(1):33-40. (In Russ., Eng.)]
  14. Снегин Э.А. Оценка состояния популяционных генофондов наземных моллюсков в условиях влияния горно-обогатительных 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. (In Russ., Eng.)]. doi: 10.1134/S2079059711050133.
  15. Снегин Э.А. Временная динамика частот полиморфных признаков раковины в популяциях Bradybaena fruticum Müll (Gastropoda, Pulmonata) на юге Среднерусской возвышенности // Научные ведомости БелГУ. – Серия «Естественные науки». – 2013. – № 10(153). – Вып. 20. – С. 87–91. [Snegin EA. Temporal dynamics of frequencies of polymorphic features of the shell in the populations of Bradybaena fruticum Müll (Gastropoda, Pulmonata) in the south of the Central Russian Upland. Scientific Bulletins of BelSU. Ser. of Natural Sciences. 2013;10(153)(20):87-91. (In Russ.)]
  16. Снегин Э.А. Анализ генетической изменчивости популяций наземного моллюска Bradybaena fruticum Müll. с использованием RAPD и ISSR маркеров // Научные ведомости БелГУ. – Сер. «Естественные науки». – 2011. – № 15 (110). – Вып. 16. – С. 37–43. [Snegin EA. Analysis of the genetic variability of populations of terrestrial mollusk Bradybaena fruticum Müll. Using RAPD and ISSR markers. Scientific Bulletins of BelSU. Ser. Natural Sciences. 2011;15(110)(16):37-43. (In Russ.)]
  17. Baur B, Klemm M. Absence of isozyme variation in geographically isolated populations of the land snail Chondrina clienta. Heredity. 1989;63(2):239-244. doi: 10.1038/hdy.1989.97.
  18. Шмальгаузен И.И. Факторы эволюции. Теория стабилизирующего отбора. – М.: Наука, 1968. – 451 c. [Shmalgauzen II. Factors of evolution. The theory of stabilizing selection. Moscow: Science; 1968. 451 p. (In Russ.)]
  19. Frankel OH, Soule ME. Conservation and Evolution. Cambridge: Cambridge University Press; 1981.
  20. Nevo E. Genetic variation in natural population: patterns and theory. Theor Pop Biol. 1978;13:121-177. doi: 10.1016/0040-5809(78)90039-4.
  21. Левонтин Р. Генетические основы эволюции. – М.: Мир, 1978. – 351 с. [Lewontin RC. The genetic basis of evolutionary change. New York: Columbia University Press; 1974. (In Russ., Eng.)]
  22. Майр Э. Зоологический вид и эволюция. – М.: Мир, 1968. – 398 c. [Mayr E. Animal species and evolution. London: Oxford University Press; 1965. 797 p. (In Russ., Engl.)]
  23. Haikola S, Fortelius W, O’Hara RB, et al. Inbreeding depression and the maintenance of genetic load in Melitaea cinxia metapopulation. Conservation Genetics. 2001;2:325-335. doi: 10.1023/A:1012538329691.
  24. Tomimatsu H, Ohara M. Effects of forest fragmentation on seed predation of the understory herb Trillium comschatcense. Conserv Biol. 2002;16:1277-1285. doi: 10.1046/j.1523-1739.2002.00412.x.
  25. Хански И. Ускользающий мир: Экологические последствия утраты местообитаний. – М.: Т-во научных изданий КМК, 2010. – 340 с. [Hanski I. The shrinking world: Ecological consequences of habitat loss. International Ecology Institute, Oldendorf/Luhe, Germany; 2005. 307 p. (In Russ., Engl.)]
  26. Hanski I. Metapopulation dynamics. Nature. 1998;396:41-49. doi: 10.1038/23876.
  27. Hanski I. Metapopulation Ecology. Oxford: Oxford University Press; 1999.
  28. Heino M, Hanski I. Evolution of migration rate in a spatially realistic metapopulation model. Am Nat. 2001;157:495-511. doi: 10.1086/319927.
  29. Струнников В.А. Возникновение компенсаторного комплекса генов одна из причин гетерозиса // Журнал общей биологии. – 1974. – Т. 35. – С. 666–677. [Strunnikov VA. The origin of the compensatory complex of genes is one of the causes of heterosis. Zhurnal obshhej biologii. 1974;35:666-677. (In Russ.)]
  30. Ray C. Maintaining genetics diversity despite local extinctions: effects of population scale. Biol Conserv. 2001;100:3-14. doi: 10.1016/S0006-3207(00)00202-0.
  31. Wright S. Random drift and shifting balance theory of evolution. Mathematical Topics in Population Genetics. Berlin: Springer Verlag; 1970. P. 1-31.
  32. 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.
  33. Peakall R, Smouse PE. GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes. 2006;6:288-295. doi: 10.1111/j.1471-8286.2005.01155.x.
  34. Mantel N. The detection of disease clustering and a generalized regression approach. Cancer Research. 1967;27:209-220.
  35. Diniz-Filho JAF, Soares TN, Lima JS, et al. Mantel test in population genetics. Genetics and Molecular Biology. 2013;36(4):475-485. doi.org/10.1590/S1415-47572013000400002
  36. Nei M. Molecular population genetics and evolution. Amsterdam; 1975.
  37. Yeh FC, Yang R, Boyle TJ, Ye Z, Xiyan JM. POPGENE32, Microsoft Window-based Freeware for Population Genetic Analysis, Version 1.32; Molecular Biology and Biotechnology Centre, University of Alberta: Edmonton, Canada. 2000. http://www.ualberta.ca/~fyeh/popgene_download.html. (cited 12.04.2008).
  38. Nei M, Li WH. Mathematical model for studying genetic variation in terms restriction endonucleases. Proceedings the National Academy Sciences. USA. 1979;76:5269-5273. doi: 10.1073/pnas.76.10.5269.
  39. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution. 1987;4(4):406-425.
  40. Van de Peer Y, De Wachter Y. TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Computer Applications in the Biosciences. 1994;10(5):69-70. doi: 10.1093/bioinformatics/10.5.569
  41. 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 by Yu.P. Altukhov. Moscow: Nauka; 2004. 619 p. (In Russ.)]
  42. 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. 394 p. (In Russ.)]
  43. Chao A, Species richness estimation. In: Balakrishnan N, Read CB, Vidakovic B, editors. Encyclopaedia of Statistical Science. New York: Wiley; 2005. P. 7907-7916.
  44. 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
  45. Chao А, Shen TJ. 2009. SPADE. http: //chao.stat.nthu.edu.tw. (cited 12.03.2015).
  46. Slatkin M. Isolation by distance in equilibrium and non-equilibrium populations. Evolution. 1993;47(1):294-79. doi: 10.1111/j.1558-5646.1993.tb01215.x.
  47. Wright S. The genetical structure of populations. Ann Eugenics. 1951;15:323-354. doi: 10.1111/j.1469-1809.1949.tb02451.x.
  48. Снегин Э.А. Временная динамика генетической структуры и эффективная численность популяций Bradybaena fruticum Müll. (Mollusca, Gastropoda, Pullmonata) в условиях юга Среднерусской возвышенности // Экология. – 2015. – № 3. – C. 198–205. doi: 10.7868/S0367059715020110. [Snegin EA. Temporal dynamics of the genetic structure and effective size of Bradybaena fruticum Müll. (Mollusca, Gastropoda, Pulmonata) populations in the south of the Central Russian Upland. Russian Journal of Ecology. 2015;46(3):260-266. (In Russ., Engl.)]. doi: 10.1134/S1067413615020113.
  49. 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 Journal of Genetics: Applied Research. 2014;4(5):444-454. (In Russ., Engl.)]. doi: 10.1134/S207905971405013X.
  50. 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. Estimating the State of Population Gene Pools of the Specially Protected Helicopsis striata (Mollusca, Gastropoda, Pulmonata) Species Based on DNA Markers. Russian Journal of Genetics: Applied Research. 2017;7(2):135-144. (In Russ., Engl.)]. doi: 10.1134/S2079059717020113.
  51. Снегин Э.А., Снегина Е.А. Генетическая структура популяций особо охраняемого моллюска Cepaea vindobonensis (Mollusca, Gastropoda, Pulmonata) в условиях северо-восточной части современного ареала // Экологическая генетика. – 2016. – Т. XIV. – № 3. – С. 13–27. [Snegin EA, Snegina EA. Genetic structure of the populations of the specially protected mollusk Cepaea vindobonensis (Mollusca, Gastropoda, Pulmonata) in the north-eastern part of the present range. Ecologicheskaia genetica. 2016;14(3):13-27. (In Russ.)]. doi: 10.17816/ecogen14313-27.
  52. Снегин Э.А., Артемчук О.Ю. Генетическая структура популяций Helix pomatia L. (Mollusca, Pulmonata) юго-восточной и восточной части ареала // Генетика. –2017. – Т. 53. – № 3. – С. 334–344. doi: 10.7868/S0016675817030122. [Snegin EA, Artemchuk OYu. Population Genetic Structure of Helix pomatia L. (Mollusca, Pulmonata) from the Southeastern and Eastern Parts of the Range. Russian Journal of Genetics. 2017;53(3):348-357. (In Russ., Engl.)]. doi: 10.1134/S1022795417030127.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. Collection points Br. fruticum (description of items in table 1)

Download (772KB)
Indexing metadata
3. Fig. 2. Indicators of expected heterozygosity (He) in populations Br. fruticum at various loci

Download (54KB)
Indexing metadata
4. Fig. 3. Debetz polygons, constructed from the q-allele aggregate frequencies of the 44 loci

Download (195KB)
Indexing metadata
5. Fig. 4. Dendrogram of genetic distances, constructed by the neighbor-joining method (NJ) between populations Br. fruticum by DNA-loci

Download (85KB)
Indexing metadata
6. Fig. 5. Dependence of the level of gene flow Nm between pairs of populations of Br. fruticum on the geographical distance between them Dg (km)

Download (20KB)
Indexing metadata

Copyright (c) 2017 Snegin E.A., Snegina E.A.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
 


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies