Abstract
Allozyme variation was determined in two land snail species (Cepaea nemoralis and Succinea putris) from four localities in northern Belgium. In each locality we selected a polluted and a nearby, less-polluted, reference plot. We examined whether (i) genetic variability differed between the polluted and reference plots, (ii) populations from polluted plots experienced recent bottlenecks, and (iii) certain allele or genotype frequencies were associated with the pollution. Our results suggest that (i) about 13% of the genetic differentiation in C. nemoralis and 5% in S. putris was due to differences among polluted and reference plots, (ii) polluted and reference plots had comparable levels of genetic variation, but in C. nemoralis observed heterozygosities were higher in polluted plots, (iii) most plots showed significant evidence for recent bottlenecks, irrespective of the degree of pollution, so that bottlenecks seem poor indicators of pollution-induced stress in land snails, and (iv) mutagenic or pollution-induced modifications did not seem to account for new allozyme variants in polluted sites. The observed patterns of genetic variation may be explained by the action of genetic drift, pollution-mediated selection, restricted gene flow, or a combination of these processes.
Similar content being viewed by others
References
J.-F. Arnaud L. Madec A. Bellido A. Guiller (1999) ArticleTitleMicrospatial genetic structure in the land snail Helix aspersa (Gastropoda: Helicidae) Heredity 83 110–119 Occurrence Handle10469198 Occurrence Handle10.1038/sj.hdy.6885650
T. Backeljau S.Z. Ahmadyar M. Selens J. Rompaey ParticleVan W. Verheyen (1987) ArticleTitleComparative electrophoretic analyses of three European Carinarion species (Mollusca, Pulmonata, Arionidae) Zool. Scr. 16 209–222 Occurrence Handle10.1111/j.1463-6409.1987.tb00068.x
T. Backeljau K. Breugelmans H. Leirs T. Rodriguez D. Sherbakov T. Sitnikova J.-M. Timmermans J.L. Goethem ParticleVan E. Verheyen (1994) ArticleTitleApplication of isoelectric focusing in molluscan systematics The Nautilus 2 IssueIDsuppl. 156–167
C.J. Bayne (1974) ArticleTitlePhysiology of the pulmonate reproductive tract: location of spermatozoa in isolated, self-fertilizing succinid snails The Veliger 16 169–175
N.M. Belfiore S.L. Anderson (2001) ArticleTitleEffects of contaminants on genetic patterns in aquatic organisms: a review Mutat. Res. Rev. Mutat. Res. 489 97–122 Occurrence Handle1:CAS:528:DC%2BD3MXovF2htbs%3D
M.J. Benton S.I. Guttman (1992a) ArticleTitleAllozyme genotype and differential resistance to mercury pollution in the caddisfly, Nectopsyche albida. I. Single locus genotypes Can. J. Fish. Aquat. Sci. 49 142–146 Occurrence Handle10.1139/f92-016
M.J. Benton S.I. Guttman (1992b) ArticleTitleAllozyme genotype and differential resistance to mercury pollution in the caddisfly, Nectopsyche albida. II. Multilocus genotypes Can. J. Fish. Aquat. Sci. 49 147–149
M.J. Benton M.L. Malott J. Trybula D.M. Dean S.I. Guttman (2002) ArticleTitleGenetic effects of mercury contamination on aquatic snail populations: allozyme genotypes and DNA strand breakage Environ. Toxicol. Chem. 21 584–589 Occurrence Handle11878471 Occurrence Handle1:CAS:528:DC%2BD38XhvVehs7s%3D Occurrence Handle10.1897/1551-5028(2002)021<0584:GEOMCO>2.0.CO;2
J.W. Bickham M.J. Smolen (1994) ArticleTitleSomatic and heritable effects of environmental genotoxins and the emergence of evolutionary toxicology Environ. Health Persp. 102 IssueIDsuppl. 12 25–28
J.W. Bickham S. Sandhu P.D.N. Hebert L. Chikhi R. Athwal (2000) ArticleTitleEffects of chemical contaminants on genetic diversity in natural populations: implications for biomonitoring and ecotoxicology Mutat. Res. 463 33–51 Occurrence Handle10838208 Occurrence Handle1:CAS:528:DC%2BD3cXjs1Cntbo%3D Occurrence Handle10.1016/S1383-5742(00)00004-1
Burdon, R.H., 1999. Genes and the environment. Taylor & Francis
N.L. Chagnon S.I. Guttman (1989a) ArticleTitleDifferential survivorship of allozyme genotypes in mosquitofish populations exposed to copper or cadmium Environ. Toxicol. Chem. 8 319–326 Occurrence Handle1:CAS:528:DyaL1MXitVOgtbw%3D
N.L. Chagnon S.I. Guttman (1989b) ArticleTitleBiochemical analysis of allozyme copper and cadmium tolerance in fish using starch gel electrophoresis Environ. Toxicol. Chem. 8 1141–1147 Occurrence Handle1:CAS:528:DyaK3cXlt1KrtQ%3D%3D
M. Cœurdassier A. Gomot-de Vaufleury P.-M. Badot (2000) ArticleTitleDose-dependent growth inhibition and bioaccumulation of hexavalent chromium in the land snail Helix aspersa aspersa Environ. Toxicol. Chem. 19 2571–2578 Occurrence Handle10.1897/1551-5028(2000)019<2571:DDGIAB>2.3.CO;2
B.D. Marais ParticleDe T.E. Dowling W.L. Minckley (1993) ArticleTitlePost-perturbartion genetic changes in populations of endangered Virgin River chubs Conserv. Biol. 7 334–341 Occurrence Handle10.1046/j.1523-1739.1993.07020334.x
H. Wolf ParticleDe R. Blust T. Backeljau (2004) ArticleTitleThe use of RAPD in ecotoxicology Mutat. Res. Rev. Mutat. Res. 566 249–262
S.J. D’Surney L.R. Shugart C.W. Theodorakis (2001) ArticleTitleGenetic markers and genotyping methodologies: an overview Ecotoxicology 10 201–204 Occurrence Handle11501428 Occurrence Handle1:CAS:528:DC%2BD3MXmtF2itrc%3D Occurrence Handle10.1023/A:1016661125807
Y. Duan S.I. Guttman J.T. Oris J.A. Bailer (2000) ArticleTitleGenotype and toxicity relationships among Hyalella azteca: I. Acute exposure to metals or low pH Environ. Toxicol. Chem. 19 1414–1421 Occurrence Handle1:CAS:528:DC%2BD3cXislKjtLs%3D Occurrence Handle10.1897/1551-5028(2000)019<1414:GATRAH>2.3.CO;2
C.F. Facemire T.S. Gross L.J. Guillette (1995) ArticleTitleReproductive impairment in the Florida panther – Nature or nurture? Environ Health Perspect. 103 IssueIDsuppl. 4 79–86 Occurrence Handle7556029 Occurrence Handle1:CAS:528:DyaK2MXmslSntbo%3D
F. Frati P.P. Fanciulli L. Posthuma (1992) ArticleTitleAllozyme variation in reference and metal-exposed natural populations of Orchesella cincta (Insecta: Collembola) Biochem. Syst. Ecol. 20 297–310 Occurrence Handle1:CAS:528:DyaK38XkvVOitLw%3D Occurrence Handle10.1016/0305-1978(92)90041-B
R.B. Gillespie S.I. Guttman (1989) ArticleTitleEffects of contaminants on the frequencies of allozymes in populations of the central stoneroller Environ. Toxicol. Chem. 8 309–317 Occurrence Handle1:CAS:528:DyaL1MXitVOgtb8%3D
Gillespie, R.B. & S.I. Guttman, 1993. Allozyme frequency analysis of aquatic populations as an indicator of contaminant-induced impacts, pp. 134–145 in Environmental Toxicology and Risk Assessment, 2nd volume ASTM STP 1173, edited by J. Gorsuch, F.J. Dwyer, C.G. Ingersool & T.W. LaPointe. American Society for Testing and Materials
Gillespie, R.B. & S.I. Guttman, 1999. Chemical-induced changes in the genetic structure of populations: Effects on allozymes, pp. 55–77 in Genetics and Ecotoxicology, edited by V.E. Forbes. Taylor & Francis
Goudet, J., 2002. FSTAT Version 2.9.3.2. Manual
S.I. Guttman (1994) ArticleTitlePopulation genetic structure and ecotoxicology Environ. Health Persp. 102 IssueIDsuppl. 12 97–100
Harris, H. & Hopkinson, D.A., 1976. Handbook of Enzyme Electrophoresis in Human Genetics. North Holland Pub. Co
P.D.N. Hebert M.M. Luiker (1996) ArticleTitleGenetic effects of contaminant exposure – towards an assessment of impacts on animal populations Sci. Total Environ. 191 23–58 Occurrence Handle8885423 Occurrence Handle1:CAS:528:DyaK28Xlsl2lur8%3D Occurrence Handle10.1016/0048-9697(96)05169-8
K. Jordaens P. Riel ParticleVan R. Verhagen T. Backeljau (1999) ArticleTitleFood-induced esterase electromorphs in Carinarion spp. and their effects on taxonomic data analysis (Gastropoda, Pulmonata, Arionidae) Electrophoresis 20 473–479 Occurrence Handle10217156 Occurrence Handle1:CAS:528:DyaK1MXis1Wjt7Y%3D Occurrence Handle10.1002/(SICI)1522-2683(19990301)20:3<473::AID-ELPS473>3.0.CO;2-F
Kerney, M., 1999. Atlas of the Land and Freshwater Molluscs of Britain and Ireland. Harley Books
R. Laskowski S.P. Hopkin (1996) ArticleTitleEffect of Zn, Cu, Pb, and Cd on fitness in snails (Helix aspersa) Ecotoxicol. Environ. Saf. 34 59–69 Occurrence Handle8793321 Occurrence Handle1:CAS:528:DyaK28XjslKnur4%3D Occurrence Handle10.1006/eesa.1996.0045
B. Lavie E. Nevo (1982) ArticleTitleHeavy metal selection of phosphoglucose isomerase allozymes in marine gastropods Mar. Biol. 71 17–22 Occurrence Handle10.1007/BF00396988
B. Lavie E. Nevo (1986) ArticleTitleGenetic selection of homozygote allozyme genotypes in marine gastropods exposed to cadmium pollution Sci. Total Environ. 57 91–98 Occurrence Handle3810150 Occurrence Handle1:CAS:528:DyaL2sXmt1CqtA%3D%3D Occurrence Handle10.1016/0048-9697(86)90013-6
R. Lewin (1987) ArticleTitleThe surprising genetics of bottlenecked flies Science 235 1325–1327 Occurrence Handle3823885 Occurrence Handle1:STN:280:DyaL2s7kvFSmsw%3D%3D Occurrence Handle10.1126/science.3823885
G. Luikart J.-M. Cornuet F.W. Allendorf W.B. Sherwin (1998) ArticleTitleDistortion of allele frequency distributions provides a test for recent population bottlenecks J. Hered. 89 238–247 Occurrence Handle9656466 Occurrence Handle1:STN:280:DyaK1czitVKhsA%3D%3D Occurrence Handle10.1093/jhered/89.3.238
J. Marchand A. Tanguy J. Laroche L. Quiniou D. Moraga (2003) ArticleTitleResponses of European flounder Platichthys flesus populations to contamination in different estuaries along the Atlantic coast of France Mar. Ecol. Prog. Ser. 260 273–284 Occurrence Handle1:CAS:528:DC%2BD2cXht1aktA%3D%3D
M.D. Moran (2003) ArticleTitleArguments for rejecting the sequential Bonferroni in ecological studies Oikos 100 403–405 Occurrence Handle10.1034/j.1600-0706.2003.12010.x
M.H. Murdoch P.D.N. Hebert (1994) ArticleTitleMitochondrial DNA diversity of brown bullhead from contaminated and relatively pristine sites in the Great Lakesw Environ. Toxicol. Chem. 13 1281–1289 Occurrence Handle1:CAS:528:DyaK2cXlsVWjsL8%3D
M. Nei (1978) ArticleTitleEstimation of average heterozygosity and genetic distance from a small number of individuals Genetics 89 583–590 Occurrence Handle17248844
M.J.M. Notten A.J.P. Oosthoek J. Rozema R. Aerts (2005) ArticleTitleHeavy metal concentrations in a soil–plant–snail food chain along a terrestrial soil pollution gradient Environ. Pollut. 138 178–190 Occurrence Handle16005127 Occurrence Handle1:CAS:528:DC%2BD2MXmt1eitLo%3D Occurrence Handle10.1016/j.envpol.2005.01.011
I. Olsson U.B. Axiö-Fredriksson M. Degerman B. Olsson (1988) ArticleTitleFast horizontal electrophoresis isoelectric focusing and polyacrylamide gel electrophoresis using PhastSystem Electrophoresis 9 16–22 Occurrence Handle2466643 Occurrence Handle1:CAS:528:DyaL1cXht1OrsrY%3D Occurrence Handle10.1002/elps.1150090104
R.S. Pfau K. McBee R.A. Bussche ParticleVan Den (2001) ArticleTitleGenetic diversity of the major histocompatibility complex of cotton rats (Sigmodon hispidus) inhabiting an oil refinery complex Environ. Toxicol. Chem. 20 2224–2228 Occurrence Handle11596754 Occurrence Handle1:CAS:528:DC%2BD38XitlWjuw%3D%3D Occurrence Handle10.1897/1551-5028(2001)020<2224:GDOTMH>2.0.CO;2
Pfenninger, M., 2002. Relationship between microspatial population genetic structure and habitat heterogeneity in Pomatias elegans (O.F. Müller 1774) (Caenogastropoda, Pomatiasidae). Biol. J. Linn. Soc. 76: 565–575
Pfleger, V. & Chatfield, J., 1983. A Guide to Snails of Britain and Europe. Hamlyn Publishing Group Ltd
S. Piry G. Luikart J.M. Cornuet (1999) ArticleTitleBOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data J. Hered. 90 502–503 Occurrence Handle10.1093/jhered/90.4.502
M. Raymond F. Rousset (1995) ArticleTitleGENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism J. Hered. 86 248–249
W.R. Rice (1989) ArticleTitleAnalyzing tables of statistical tests Evolution 43 223–225 Occurrence Handle10.2307/2409177
S. Schneider J.M. Kueffer D. Roessli L. Excoffier (1997) ARLEQUIN, a Software for Population Genetics Data Analysis, Version 2.000 University of Geneva Geneva
O. Schweiger M. Frenzel W. Durka (2004) ArticleTitleSpatial genetic structure in a metapopulation of the land snail Cepaea nemoralis (Gastropoda: Helicidae) Mol. Ecol. 13 3645–3655 Occurrence Handle15548280 Occurrence Handle1:STN:280:DC%2BD2crnvFyrsw%3D%3D Occurrence Handle10.1111/j.1365-294X.2004.02357.x
B.L. Sloss M.A. Romano R.V. Anderson (1998) ArticleTitlePollution-tolerant allele in fingernail clams (Musculium transversum) Arch. Environ. Contam. Toxicol. 35 302–308 Occurrence Handle9680522 Occurrence Handle1:CAS:528:DyaK1cXltVWktbc%3D Occurrence Handle10.1007/s002449900380
T. Sörensen (1948) ArticleTitleA method for establishing groups of equal amplitude in plant sociology based on similarity of species content and its application to analyses of the vegetation on Danish commons K. Danske Vid. Selsk. Biol. Skr. 5 1–34
Statsoft, 2000. Statistica for Windows, v. 5.1. Computer program manual. Tulsa, StatSoft Inc
D.L. Swofford R.B. Selander (1981) ArticleTitleBiosys-1 – A Fortran program for the comprehensive analysis of electrophoretic data in population-genetics and systematics J. Hered. 72 281–283
C.W. Theodorakis (2003) ArticleTitleEstablishing causality between population genetic alterations and environmental contamination in aquatic organisms Hum. Ecol. Risk Assessm. 9 37–58
C.W. Theodorakis J.W. Bickham T. Lamb (2001) ArticleTitleIntegration of genotoxicity and population genetic analysis in kangaroo rats (Dipodomys merriami) exposed to radionuclide contamination at the Nevada test site, USA Environ. Toxicol. Chem. 20 317–326 Occurrence Handle11351431 Occurrence Handle1:CAS:528:DC%2BD3MXnsV2kuw%3D%3D Occurrence Handle10.1897/1551-5028(2001)020<0317:IOGAPG>2.0.CO;2
L. Tranvik M. Sjögren G. Bengtsson (1994) ArticleTitleAllozyme polymorphism and protein profile in Orchesella bifasciata (Collembola): indicative of extended metal pollution? Biochem. Syst. Ecol. 22 13–23 Occurrence Handle1:CAS:528:DyaK2cXitFKjuro%3D Occurrence Handle10.1016/0305-1978(94)90110-4
A. Ugolini F. Borghini P. Calosi M. Bazzicalupo G. Chelazzi S. Focardi (2004) ArticleTitleMediterranean Talitrus saltator (Crustacea, Amphipoda) as a biomonitor of heavy metals contamination Mar. Pollut. Bull. 48 526–532 Occurrence Handle14980468 Occurrence Handle1:CAS:528:DC%2BD2cXht12qs78%3D Occurrence Handle10.1016/j.marpolbul.2003.10.002
B. Vandecasteele P. Quataert B. Vos ParticleDe F.M.G. Tack (2004) ArticleTitleAssessment of the pollution status of alluvial plains: a case-study for the dredged sediment-derived soils along the Leie river Arch. Environ. Contam. Toxicol. 47 14–22 Occurrence Handle15346774 Occurrence Handle1:CAS:528:DC%2BD2cXltlWmt74%3D Occurrence Handle10.1007/s00244-004-3014-4
Weir, B.S., 1996. Genetic Data Analysis II. Sinauer Associates
L.A. Woodward M. Mulvey M.C. Newman (1996) ArticleTitleMercury contamination and population-level responses in chironomids: can allozyme polymorphism indicate exposure? Environ. Toxicol. Chem. 15 1309–1316 Occurrence Handle1:CAS:528:DyaK28XlsVOku7g%3D Occurrence Handle10.1897/1551-5028(1996)015<1309:MCAPLR>2.3.CO;2
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Jordaens, K., De Wolf, H., Van Houtte, N. et al. Genetic variation in two land snails, Cepaea nemoralis and Succinea putris (Gastropoda, Pulmonata), from sites differing in heavy metal content. Genetica 128, 227–239 (2006). https://doi.org/10.1007/s10709-005-5705-9
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10709-005-5705-9