Polymorphism of the Introduced Snail Cepaea nemoralis (Gastropoda, Helicidae) from two Distant Parts of Eastern Europe: Accidental Similarity or Regularity?
Abstract
The shell coloration of Cepaea nemoralis from Western Ukraine (Ivano-Frankivsk, Lviv, and Ternopil regions) and from the Moscow region of Russia was analyzed, in total, almost 6 thousand specimens from 32 sites. In the samples from the Moscow region, on average, there were half as many yellow shells and four times as many pink mid-banded shells. There were no other statistically significant differences. As in other areas of Eastern Europe, yellow unbanded and brown shells were often absent or represented by few individuals in both compared areas, and brown banded shells were completely (Western Ukraine) or almost completely (Moscow region) absent, which may be related to the founder effect. Analysis of the literature data showed that in the introduced populations of C. nemoralis from Europe and USA, a distinct predominance of one or two of the 4 light phenotypes (yellow unbanded, yellow mid-banded, pink unbanded, and pink mid-banded) is often observed. The total frequency of these phenotypes in introduced populations is often higher than its average values calculated for different parts of the natural range. A possible relationship between the observed pattern and climatic selection is discussed.
References
Alexander, R. C. 1952. Introduced species of land snails in New Jersey. The Nautilus, 65 (4), 132-135.
Alexandrov, D. A., Sergievsky, S. O. 1980. Genetic structure of peripheral populations of land mollusc Cepaea hortensis (Müll.). Doklady Akademii nauk SSSR, 225 (1), 206-208.
Arnason, E., Grant, P.R. 1976. Climatic selection in Cepaea hortensis at the northern limit of its range in Iceland. Evolution, 30, 499-508.
https://doi.org/10.1111/j.1558-5646.1976.tb00928.x
Arnold, R. W. 1968. Studies on Cepaea. VII. Climatic selection in Cepaea nemoralis (L.) in the Pyrenees. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 253 (789), 549-593.
https://doi.org/10.1098/rstb.1968.0011
Arnold, R. W. 1970. A comparison of populations of the polymorphic land snail Cepaea nemoralis (L.) living in a lowland district in France with those in a similar district in England. Genetics, 64, 589-604.
https://doi.org/10.1093/genetics/64.3-4.589
Arnold, R. W. 1971. Cepaea nemoralis on the East Sussex South Downs, and the nature of area effects. Heredity, 26, 277-298.
https://doi.org/10.1038/hdy.1971.33
Bąkowski, J. 1880. Mięczaki zebrane w r. 1879 w okolicy Rzeszowa. Sprawozdanie Komisyi Fizyjograficznéj, 14 (2), 254-257.
Bengtson, S.A., Nilsson, A., Nordström, S., Rundgren, S. 1979. Distribution patterns of morph frequencies in the snail Cepaea hortensis in Iceland. Holarctic Ecology, 2, 144-149.
https://doi.org/10.1111/j.1600-0587.1979.tb00694.x
Brussard, P. F. 1975. Geographic variation in North American colonies of Cepaea nemoralis. Evolution, 29 (3), 402-410.
https://doi.org/10.1111/j.1558-5646.1975.tb00830.x
Cain, A. J. 1968. Studies of Cepaea. V. Sand-dune populations of Cepaea nemoralis (L.). Philosophical Transactions of the Royal Society of London. Series B, 253, 499-517.
https://doi.org/10.1098/rstb.1968.0009
Cain, A. J., Currey, J. D. 1963. Area effects in Cepaea. Philosophical Transactions of the Royal Society of London. Series B, 246 (726), 1-81.
https://doi.org/10.1098/rstb.1963.0001
Cain, A. J., Sheppard, P. M. 1954. Natural selection in Cepaea. Genetics, 39, 89-116.
https://doi.org/10.1093/genetics/39.1.89
Cameron, R.A.D. 2001. Cepaea nemoralis in a hostile environment: continuity, colonizations and morph-frequencies over time. Biological Journal of the Linnean Society, 74, 255-264.
https://doi.org/10.1111/j.1095-8312.2001.tb01390.x
Cameron, R.A.D., Dillon, P.J. 1984. Habitat stability, population histories and patterns of variation in Cepaea. Malacologia, 25 (2), 271-290.
Cameron, R.A.D., Pannett, D.J. 1985. Interaction between area effects and variation with habitat in Cepaea. Biological Journal of the Linnean Society, 24, 365-379.
https://doi.org/10.1111/j.1095-8312.1985.tb00382.x
Carter, M. A. 1968. Studies on Cepaea. II. Area effects and visual selection in Cepaea nemoralis (L.) and Cepaea hortensis. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 253 (789), 397-446.
https://doi.org/10.1098/rstb.1968.0006
Clarke, B., Diver, C., Murray, J. 1968. Studies of Cepaea. VI. The spatial and temporal distribution of phenotypes in a colony of Cepaea nemoralis (L.). Philosophical Transactions of the Royal Society of London. Series B, 253, 519-548.
https://doi.org/10.1098/rstb.1968.0010
Clarke, B., Murray, J. 1962. Changes of gene-frequency in Cepaea nemoralis (L.). Heredity, 17 (4), 445-465.
https://doi.org/10.1038/hdy.1962.47
Clench, W. J. 1930. Additional notes on the colony of Helix nemoralis at Marion, Mass. The Nautilus, 44, 13-14.
Cowie, R. H., Jones, J.S. 1998. Gene frequency changes in Cepaea snails on the Marlborough Downs over 25 years. Biological Journal of the Linnean Society, 65, 233-255.
https://doi.org/10.1006/bijl.1998.0250
Egorov, R. 2018. On the distribution of introduced species of the genus Cepaea Held, 1838 (Gastropoda: Pulmonata: Helicidae) in European Russia. Nachrichtenblatt der Ersten Vorarlberger Malakologischen Gesellschaft, 25, 79-102.
Gural-Sverlova, N. V., Egorov, R. V. 2021. Shell colour and banding polymorphism in Cepaea nemoralis (Gastropoda, Pulmonata, Helicidae) from the Moscow region. Ruthenica, Russian Malacological Journal, 31 (1), 27-38.
https://doi.org/10.35885/ruthenica.2021.31(1).4
Gural-Sverlova, N. V., Gural, R. I. 2018. Long-term dynamic of phenetic structure in colonies of the introduced species, Cepaea hortensis (Gastropoda, Pulmonata, Helicidae). Zoologicheskij Zhurnal, 97 (7), 751-761 [In Russian].
Gural-Sverlova, N. V., Gural, R. I., Savchuk, S. P. 2020. New records of Cepaea nemoralis (Gastropoda, Pulmonata, Helicidae) and phenotypic composition of its colonies in Western Ukraine. Ruthenica, Russian Malacological Journal, 30 (2), 75-86 [In Russian].
https://doi.org/10.35885/ruthenica.2021.30(2).1
Honěk, A. 1995. Distribution and shell colour and banding polymorphism of the Cepaea species in Bohemia. Acta Societatis Zoologicae Bohemicae, 59, 63-77.
Honěk, A., Martinkova, Z. 2003. Persistence and shell band morph frequencies in urban populations of Cepaea. In: BCPC Symposium Proceedings, 80. Slugs & Snails: Agricultural, Veterinary & Environmental Perspectives, 165-170.
Howe, J. L. 1898. Variation in the shell of Helix nemoralis in the Lexington, Va., colony. The American Naturalist, 32 (384), 913-920.
https://doi.org/10.1086/277067
Johnson, C. W. 1927. Further notes on the colony of Helix nemoralis in Massachusetts. The Nautilus, 41, 47-49.
Jones, J.S., Leith, B.H., Rawlings, P. 1977. Polymorphism in Cepaea - a problem with too many solution? Annual Review of Ecology and Systematics, 8, 109-143.
https://doi.org/10.1146/annurev.es.08.110177.000545
Kolesnik, V. G., Kruglova, O. Yu. 2016. Phenotypic variability in the populations of Cepaea nemoralis Linnaeus, 1758 (Gastropoda, Pulmonata, Helicidae) from Minsk city and Minsk region. In: Actual problems of ecology. Grodno State University, Grodno, 102-103 [In Russian].
Lamotte, M. 1951. Recherches sur la structure génétique des populations naturelles de Cepaea nemoralis (L.). Bulletin biologique de la France et de la Belgique: Supplément, 35, 1-239.
Lamotte, M. 1959. Polymorphism of natural populations of Cepaea nemoralis. In: Cold Spring Harbor Symposia on Quantitative Biology, 24, 65-86.
https://doi.org/10.1101/SQB.1959.024.01.009
Landman, M. A. 1956. Statistics on a colony of Cepaea nemoralis. The Nautilus, 69 (3), 104-106.
Łomnicki, M. 1899. Helix nemoralis L. Kosmos, 23, 382.
Mazon, L. I., Martinez de Pancorbo, M.A., Vicario, A., Aguirre, A.I., Estomba, A., Lostao, C.M. 1989. Selection in sympatric populations of Cepaea. Genetics Selection Evolution, 21, 269-281.
https://doi.org/10.1186/1297-9686-21-3-269
McConnell, D. 1936. Notes on Helix nemoralis at Lexington, Virginia. The Nautilus, 50 (1), 15-16.
Mukhanov, A. V., Lisitsyn, P. A. 2018. New data on distribution of two alien species of the land snail of the family Helicidae in European Russia. Russian Journal of Biological Invasions, 9 (1), 57-62.
https://doi.org/10.1134/S2075111718010125
Murray, J. 1966. Cepaea nemoralis in the isles of Scilly. Proceedings of the Malacological Society London, 37, 167-181.
Murray, J. 1975. The genetics of the Mollusca. In: King, R. C., ed. Handbook of genetics, 3. Plenum Press, New York: 3-31.
https://doi.org/10.1007/978-1-4615-7145-2_1
Murray, J., Clarke, B. 1978. Changes of gene frequency in Cepaea nemoralis over fifty years. Malacologia, 17 (2), 317-330.
Örstan, A., Cameron, R. A. D. 2015. Cepaea nemoralis in Burlington, New Jersey, USA: its possible origin and state 157 years after its introduction. Journal of Conchology, 42 (2), 193-198.
Ostrovsky, A. M., Prokofieva, K. V. 2017. The phenotypic structure of introduced populations of Cepaea nemoralis (Linnaeus, 1758) (Gastropoda, Pulmonata, Helicidae) in urban environments. In: Actual issues of modern malacology. Publishing House Belgorod, Belgorod, 85-89 [In Russian].
Ożgo, M. 2005. Cepaea nemoralis (L.) in southeastern Poland: association of morph frequencies with habitat. Journal of Molluscan Studies, 71, 93-103.
https://doi.org/10.1093/mollus/eyi012
Pokryszko, B. M., Cameron, R. A. D., Horsák, M. 2012. Variation in the shell colour and banding polymorphism of Cepaea nemoralis (L.) in rural areas around Wrocław. Folia Malacologica, 20 (2), 87-98.
https://doi.org/10.2478/v10125-012-0012-4
Ramos, M. A. 1984. Polymorphism of Cepaea nemoralis (Gastropoda, Helicidae) in the Spanish Occidental Pyrenees. Malacologia, 25 (2), 325-341.
https://doi.org/10.1111/j.1095-8312.1985.tb00392.x
Ramos, M. A. 1985. Shell polymorphism in a southern peripheral population of Cepaea nemoralis (L.) (Pulmonata, Helicidae) in Spain. Biological Journal of the Linnean Society, 25, 197-208.
https://doi.org/10.1111/j.1095-8312.1985.tb00392.x
Richards, A. V., Murray, J. 1975. The relation of phenotype to habitat in an introduced colony of Cepaea nemoralis. Heredity, 35, 128-131.
https://doi.org/10.1038/hdy.1975.13
Richards, P. M., Liu, M. M., Lowe, N., Davey, J. W., Blaxter, M. L., Davison, A. 2013. RAD-Seq derived markers flank the shell colour and banding loci of the Cepaea nemoralis supergene. Molecular Ecology, 22, 3077-3089.
https://doi.org/10.1111/mec.12262
Rost, H. 1952. Studies on Cepaea hortensis (Müll.) in Northern Norway. Astarte, 2, 1-10.
Sacchi, C. F. 1984. Population ecology of Cepaea nemoralis and C. vindobonensis along the north Adriatic coast of Italy. Malacologia, 25 (2), 315-323.
Schilder, F.A., Schilder, M. 1957. Die Bänderschnecken. Eine Studie zur Evolution der Tiere. Schluß: Die Bänderschnecken Europas. Gustav Fischer Verlag, Jena, 93-206.
Sverlova, N. 2002. Einschleppung und Polymorphismus der Cepaea-Arten am Beispiel von Lwow in der Westukraine (Gastropoda: Pulmonata: Helicidae). Malakologische Abhandlungen aus dem Staatlichen Museum für Tierkunde Dresden, 20 (2), 267-274.
Sverlova, N. 2004 a. Landschnecken-Farbpolymorphismus aus physikalischen Gründen (Gastropoda: Pulmonata: Stylommatophora). Malakologische Abhandlungen aus dem Staatlichen Museum für Tierkunde Dresden, 22, 131-145.
Sverlova, N. 2004 b. Zur Auswertung der Diversitaet und Struktur des Polymorphismus bei den Bänderschnecken Cepaea hortensis (Muller, 1774) und C.nemoralis (Linne 1758) am Beispiel isolierter Populationen. Mitteilungen aus dem Museum für Naturkunde in Berlin. Zoologische Reihe, 80 (2), 159-180.
https://doi.org/10.1002/mmnz.4850800203
Sverlova, N. V. 2007. Peculiarities of polymorphism structure of introduced populations of Cepaea nemoralis. In: Faltsfeinivski chytannia. PP Vyshemyrskyi, Kherson, 287-292 [In Russian]
Valovirta, I., Halkka, O. 1976. Colour polymorphism in northern peripheral populations of Cepaea hortensis. Hereditas, 83, 123-126.
https://doi.org/10.1111/j.1601-5223.1976.tb01576.x
Wolda, H. 1969 a. Fine distribution of morph frequencies in the snail, Cepaea nemoralis near Groningen. Journal of Animal Ecology, 38 (2), 305-327.
Wolda, H. 1969 b. Stability of a steep cline in morph frequencies of the snail Cepaea nemoralis (L.). Journal of Animal Ecology, 38 (3), 623-635.