Article

Article name LONG-TERM DYNAMICS OF MORPHOGENETIC INDICATORS OF THE TERRESTRIAL MOLLUSK CEPAEA VINDOBONENSIS (GASTROPODA, PULMONATA, HELICIDAE) IN THE BEKARYUKOVSKY BOR NATURAL MONUMENT, RUSSIA
Authors

Eduard A. Snegin, PhD, Director of the Research Center for Genomic Selection of the Belgorod State National Research University (430005, Russia, Belgorod Region, Belgorod, Pobedy Street, 85); iD ORCID: https://orcid.org/0000-0002-7574-6910; e-mail: snegin@bsu.edu.ru
Aleksandra Yu. Tishchenko, Junior Researcher of the Research Center for Genomic Selection of the Belgorod State National Research University (430005, Russia, Belgorod Region, Belgorod, Pobedy Street, 85); iD ORCID: https://orcid.org/0000-0003-1838-7816; e-mail: tishchenko_ayu@bsu.edu.ru

Reference to article

Snegin E.A., Tishchenko А.Yu. 2021. Long-term dynamics of morphogenetic indicators of the terrestrial mollusk Cepaea vindobonensis (Gastropoda, Pulmonata, Helicidae) in the Bekaryukovsky Bor Natural Monument, Russia. Nature Conservation Research 6(3): 58–72. https://dx.doi.org/10.24189/ncr.2021.038

Section Research articles
DOI https://dx.doi.org/10.24189/ncr.2021.038
Abstract

Cepaea vindobonensis (Gastropoda, Pulmonata, Helicidae) is a terrestrial mollusk, protected in the Belgorod Region (European Russia). In the Bekaryukovsky Bor Natural Monument, its peripheral population is known considering to be one of the most abundant in the north-eastern part of its range. In this paper, changes in the morphogenetic structure of C. vindobonensis population and its relationships with microclimatic environmental factors were analysed for the last 20 years. The results of the Kruskal-Wallis test of conchiometric features showed statistically significant (p < 0.05) differences between the studied years for all measurements. We found a statistically significant correlation between the parameters of the adult shell and some climatic characteristics, including both the average values for a four-year period and values recorded during the shell formation at the juvenile life cycle stage. This correlation apparently indicates the epigenetic nature of this population adaptation to the environment. The calculation of the average number of phenotypes (identified according to Zhivotovsky) showed the lowest level in 2020 (µ = 1.44 ± 0.20), and the highest level in 2002 (µ = 2.19 ± 0.21). To determine the population vitality degree, we analysed the genetic structure of the C. vindobonensis population on the basis of esterase izozyme loci. The highest changes in allele frequencies were observed in EST8 locus, where there was a statistically significant (p < 0.05) decrease in the EST8-2 allele frequency in 2006–2011, while being absent in the population in 2012–2020. At the same time, in 2020 the studied population became monomorphic for the EST8-3 allele. It is assumed that the transition to the homozygous state in this locus was caused not only by the genetically automatic process, but also by changes in habitats. In addition, there was a considerable lack of heterozygotes (inbreeding coefficient F = 0.517 ± 0.395) in 2020. The effective population size (Ne), calculated using the temporal method, was equal to 13.52. The forecast of the lifetime of the С. vindobonensis population based on genetic data demonstrated the value of about 100 years. The obtained results show a low vitality degree of the studied peripheral C. vindobonensis population. This may lead to its further extinction, especially in the case of changes in environmental parameters. However, the maintaining of nature conservation measures in the study area may allow avoiding this event.

Keywords

conchiometric features, effective population size, genetic structure, peripheral population, population dynamics

Artice information

Received: 15.03.2021. Revised: 08.06.2021. Accepted: 16.06.2021.

The full text of the article
References

Arnaud-Haond S., Teixeira S., Massa S.I., Billot C., Saenger P., Coupland G., Serrão E.A. 2006. Genetic structure at range edge: low diversity and high inbreeding in Southeast Asian mangrove (Avicennia marina) populations. Molecular Ecology 15(12): 3515–3525. DOI: 10.1111/j.1365-294X.2006.02997.x
Barrett R.D., Schluter D. 2008. Adaptation from standing genetic variation. Trends in Ecology and Evolution 23(1): 38–44. DOI: 10.1016/j.tree.2007.09.008
Bengtson S.A., Nilsson A., Nordström S., Rundgren S. 1979. Selection for adult shell size in natural populations of the landsnail Cepaea hortensis (Müll.). Annales Zoologici Fennici 16(3): 187–194.
Berry A.J. 1963. Growth and variation of the shell in certain Malayan limestone hill snails. Journal of Molluscan Studies 35(5): 203–206. DOI: 10.1093/oxfordjournals.mollus.a064919
Buria H., Stahel W. 1983. Altitudinal variation in Arianta arbustorum (Mollusca, Pulmonata) in the Swiss Alps. Genetica 62(2): 95–108. DOI: 10.1007/BF00116631
Cain A.J., Cook L.M. 1989. Persistence and extinction in some Cepaea populations. Biological Journal of the Linnean Society 38(2): 183–190. DOI: 10.1111/j.1095-8312.1989.tb01573.x
Cameron R.A.D. 1992. Change and stability in Cepaea populations over 25 years: a case of climatic selection. Proceedings of the Royal Society B: Biological Sciences 248(1322): 181–187. DOI: 10.1098/rspb.1992.0060
Cameron R.A.D., Pokryszko B.M. 2008. Variation in Cepaea populations over 42 years: climate fluctuations destroy a topographical relationship of morph-frequencies. Biological Journal of the Linnean Society 95(1): 53–61. DOI: 10.1111/j.1095-8312.2008.01042.x
Carr P.D., Ollis D.L. 2009. Alpha/beta hydrolase fold: an update. Protein and Peptide Letters 16(10): 1137–1148. DOI: 10.2174/092986609789071298
Crow J.F., Kimura M. 1970. An introduction to population genetics theory. New York: Harpers and Row. 591 p.
Diver C. 1939. Aspects of the study of variation in snails. Journal of Conchology 21(4–5): 91–141.
Eckert C.G., Samis K.E., Lougheed S.C. 2008. Genetic variation across species' geographical ranges: the central-marginal hypothesis and beyond. Molecular Ecology 17(5): 1170–1188. DOI: 10.1111/j.1365-294X.2007.03659.x
Gaal Ö., Medgyesi G.A., Vereczkey L. 1980. Electrophoresis in the separation of biological macromolecules. Chichester, UK: John Wiley & Sons; Budapest: Akademiai Kiado. 422 p.
Goodfriend G.A. 1986. Variation in Land-snail Shell form and Size and its Causes: a Review. Systematic Biology 35(2): 204–223. DOI: 10.1093/sysbio/35.2.204.
Gural-Sverlova N.V. 2013. Dependence of size, form and color of shells in populations of Cepaea vindobonensis (Gastropoda, Pulmonata, Helicidae) from various regions of Ukraine. Scientific Bulletin of Natural Sciences 19: 75–82. [In Russian]
Gural-Sverlova N.V., Martynov V.V. 2007. Conchological peculiarities of Cepaea vindobonensis populations on the territory of the Donetsk region. Problems of Ecology and Nature Protection of Technogenic Region 7: 85–91. [In Russian]
Gural-Sverlova N.V., Gural R.I. 2021. Shell banding and colour polymorphism of introduced snail Cepaea hortensis (Gastropoda, Pulmonata, Helicidae) from some parts of Eastern Europe. Ruthenica 31(2): 59–76.
Harmon J.P., Moran N.A., Ives A.R. 2009. Species response to environmental change: impacts of food web interactions and evolution. Science 323(5919): 1347–1350. DOI: 10.1126/science.1167396
Hoffmann A.A., Sgrò C.M. 2011. Climate change and evolutionary adaptation. Nature 470(7335): 479–485. DOI: 10.1038/nature09670
Ivanter E.V. 2017. Revising the ecological concept of peripheral populations. Russian Journal of Ecology 48(1): 81–85. DOI: 10.1134/S1067413617010076
Johnson M.S. 2011. Thirty-four years of climatic selection in the land snail Theba pisana. Heredity 106(5): 741–748. DOI: 10.1038/hdy.2010.114
Kajtoch Ł., Davison A., Grindon A., Deli T., Sramkó G., Gwardjan M., Kramarenko S., Mierzwa-Szymkowiak D., Ruta R., Ścibior R., Tóth J.P., Wade C., Kolasa M., Egorov R.V., Fehér Z. 2017. Reconstructed historical distribution and phylogeography unravels non-steppic origin of Caucasotachea vindobonensis (Gastropoda: Helicidae). Organisms Diversity and Evolution 17(3): 679–692. DOI: 10.1007/s13127-017-0337-3
Khlus L.M. 2004. Morphometric structure of natural populations of Cepaea vindobonensis Fer. on the territory of Ukraine. Scientific Herald of Chernivtsi University 223: 83–88. [In Ukrainian]
Kramarenko S.S. 2016. Patterns of spatio-temporal variation in land snails: a multi-scale approach. Folia Malacologica 24(3): 112–177. DOI: 10.12657/folmal.024.008
Kramarenko S.S., Khokhutkin I.M., Grebennikov M.E. 2007. Specific features of phenetic structure of the terrestrial snail Cepaea vindobonensis (Pulmonata; Helicidae) in urbanized and natural populations. Russian Journal of Ecology 38(1): 39–45. DOI: 10.1134/S1067413607010079
Krimbas C.B., Tsakas S. 1971. The genetics of Dacus oleae. V. Changes of esterase polymorphism in a natural population following insecticide control-selection or drift? Evolution 25(3): 454–460. DOI: 10.1111/j.1558-5646.1971.tb01904.x
Lakin G.F. 1990. Biometry. Moscow: Vysshaya Shkola. 350 p. [In Russian]
Lang A. 1906. Über die Mendelschen Gesetze, Art- und Varietätenbildung, Mutation und Variation, insbesondere bei unsern Hain- und Garetnschnecken. In: Verhandlungen der Schweizerischen Naturforschenden Gesellschaft in Luzern. Luzern. P. 209–254.
Makeeva V.M., Belokon M.M., Malyuchenko O.P. 2005. 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 41(11): 1230–1244. DOI: 10.1007/s11177-005-0224-4
Mayr E. 1965. Animal Species and Evolution. London: Oxford University Press. 797 p.
Milkov F.N. 1950. Forest-steppe of the Russian plain: experience of landscape characteristics. Moscow: AS USSR. 292 p. [In Russian]
Murray J., Clarke B. 1978. Change of gene frequency in Cepaea nemoralis over fifty years. Malacologia 17: 317–330.
Nei M., Tajima F. 1981. Genetic drift and estimation of effective population size. Genetics 98(3): 625–640.
Ożgo M., Komorowska A. 2009. Shell banding polymorphism in Cepaea vindobonensis in relation to habitat in Southeastern Poland. Malacologia 51(1): 81–88. DOI: 10.4002/040.051.0105
Ożgo M., Schilthuizen M. 2012. Evolutionary change in Cepaea nemoralis shell colour over 43 years. Global Change Biology 18(1): 74–81. DOI: 10.1111/j.1365-2486.2011.02514.x
Parmar T.K., Rawtani D., Agrawal Y.K. 2016. Bioindicators: the natural indicator of environmental pollution. Frontiers in Life Science 9(2): 110–118. DOI: 10.1080/21553769.2016.1162753
Peakall R., Smouse P.E. 2006. GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6(1): 288–295. DOI: 10.1111/j.1471-8286.2005.01155.x
Peake J.F. 1973. Species isolation in sympatric populations of the genus Diplommatina (Gastropoda, Prosobranchia, Cyclophoridae, Diplommatininae). Malacologia 14: 303–312.
Pettitt C. 1977. An investigation of variation in shell form in Discula (Hystricella) turricula (Love, 1831) (Pulmonata; Helicacea). Journal of Conchology 29: 147–150.
Pokryszko B.M., Maltz T.K., Cameron R.A. 2004. Cepaea vindobonensis (Férussac, 1821) in the Pieniny Mts. Folia Malacologica 12(3): 153–156. DOI: 10.12657/folmal.012.013
Provan J., Maggs C.A. 2011. Unique genetic variation at a species' rear edge is under threat from global climate change. Proceedings of the Royal Society B: Biological Sciences 279(1726): 39–47. DOI: 10.1098/rspb.2011.0536
Red Data Book of Russian Federation (plants and fungi). Moscow: KMK Scientific Press Ltd., 2008. 855 p. [In Russian]
Red Data Book of the Belgorod Region. Rare and endangered plants, fungi, lichens and animals. Belgorod: Belgorod State University, 2019. 668 p. [In Russian]
Rensch B. 1932. Uber die Abhingigkeit der Grosse, des relativen Gewichtes und der Oberflachen struktur der Landschneckenschalen von Umwelts-faktoren (Okologische Molluskenstudien I.) Zeitschrift für Morphologie und Ökologie der Tiere 25: 757–807.
Richardson B.J., Baverstock P.R., Adams M. 2012. Allozyme electrophoresis: a handbook for animal systematics and population studies. Sydney and London: Academic Press. 410 p.
Rosin Z.M., Kwieciński Z., Lesicki A., Skórka P., Kobak J., Szymańska A., Osiejuk T.S., Kałuski T., Jaskulska M., Tryjanowski P. 2018. Shell colour, temperature, (micro)habitat structure and predator pressure affect the behaviour of Cepaea nemoralis. Science of Nature 105 (5–6): 35. DOI: 10.1007/s00114-018-1560-2
Shileyko A.A. 1978 Terrestrial mollusks of the superfamily Helicoidea. Fauna of the USSR. Vol. 3(6). Leningrad: Nauka. 384 p. [In Russian]
Siepielski A.M., DiBattista J.D., Carlson S.M. 2009. It's about time: the temporal dynamics of phenotypic selection in the wild. Ecology Letters 12(11): 1261–1276. DOI: 10.1111/j.1461-0248.2009.01381.x
Sinyavskaya A.S. 2009. The phenetic structure of Cepaea nemoralis in the evolving range. In: Conference «Research Work of Students». Brest: Brest State University. P. 24–26. [In Russian]
Snegin E.A. 2011. Assessment of the state of population gene pools of terrestrial mollusks in conditions of influence of ore dressing combines from the example Bradybaena fruticum Müll. (Gastropoda, Pullmonata). Russian Journal of Genetics: Applied Research 1(5): 379–389. DOI: 10.1134/s2079059711050133
Snegin E.A. 2012. 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 Journal of Genetics: Applied Research 2(2): 160–170. DOI: 10.1134/S2079059712020128
Snegin E.A. 2012. Spatial and temporal aspects of the ecological and genetic structure of invertebrate populations (on the example of terrestrial mollusks and insects in the south of the Central Russian Upland). Dr.Sc. Thesis. Belgorod. 394 p. [In Russian]
Snegin E.A., Snegina E.A. 2018. Genetic Structure of Populations of Specially Protected Mollusk Cepaea vindobonensis (Mollusca, Gastropoda, Pulmonata) in the Northeastern Part of the Modern-Day Range. Russian Journal of Genetics: Applied Research 8(2): 159–171. DOI: 10.1134/S2079059718020090
Soulé M.E. 1980. Thresholds for Survival: Maintaining Fitness and Evolutionary Potential. In: M.E. Soulé, B.M. Wilcox (Eds.): Conservation Biology: An Evolutionary-Ecological Perspective. Sunderland: Sinauer. P. 151–170.
Staikou A.E. 1998. Aspects of life cycle, population dynamics, growth and secondary production of the pulmonate snail Cepaea vindobonensis (Férussac, 1821) in northern Greece. Journal of Molluscan Studies 64(3): 297–308. DOI: 10.1093/mollus/64.3.297
Staikou A.E. 1999. Shell temperature, activity and resistance to desiccation in the polymorphic land snail Cepaea vindobonensis. Journal of Molluscan Studies 65(2): 171–184. DOI: 10.1093/mollus/65.2.171
Sverlova N. 2004. Landschnecken-Farbpolymorphismus aus physikalischen Gründen (Gastropoda: Pulmonata: Stylommatophora). Malakologische Abhandlungen Museum für Tierkunde Dresden 22: 131–145.
Sverlova N.V. 2007. Peculiarities of polymorphism structure of introduced populations of Cepaea nemoralis. In: Falzfein Readings. Kherson: PP Vyshemirsky. P. 287–292. [In Russian]
Thomas C.D., Bodsworth E.J., Wilson R.J., Simmons A.D., Davies Z.G., Musche M., Conradt L. 2001. Ecological and evolutionary processes at expanding range margins. Nature 411(6837): 577–581. DOI: 10.1038/35079066
Tillier S. 1981. Clines, convergence and character displacement in New Caledonian diplommatinids (land prosobranchs). Malacologia 21(1–2): 177–208.
Vychalkovskaya N.V. 2012. Some distribution peculiarities of the dimensional and age related classes frequencies in Brephulopsis cylindrica populations. Scientific Issues of Ternopil Volodymyr Hnatiuk National Pedagogical University. Series: Biology 2(51): 52–53. [In Russian]
Wall S., Carter M.A., Clarke B. 1980. Temporal changes of gene frequencies in Cepaea hortensis. Biological Journal of the Linnean Society 14(3–4): 303–317. DOI: 10.1111/j.1095-8312.1980.tb00111.x
Wolda H. 1969. Genetics of polymorphism in the land snail, Cepaea nemoralis. Genetica 40(1): 475–502. DOI: 10.1007/BF01787373
Zhivotovskii L.A. 1991. Population biometry. Moscow: Nauka. 271 p. [In Russian]