, Volume 141, Issue 7–9, pp 281–292 | Cite as

Taxonomic and population genetic re-interpretation of two color morphs of the decollate snail, Rumina decollata (Mollusca, Pulmonata) in southern France

  • Vanya Prévot
  • Kurt Jordaens
  • Natalie Van Houtte
  • Gontran Sonet
  • Kenny Janssens
  • Rita Castilho
  • Thierry Backeljau


The hermaphroditic terrestrial snail Rumina decollata has a mixed breeding system with a high prevalence of self-fertilization. In the Montpellier area (France), the species is represented by a dark and a light color morph. Based on allozyme data, both morphs have been reported as single, homozygous multilocus genotypes (MLG), differing at 13 out of 26 loci, but still showing occasional hybridization. Recent DNA sequence data suggest that each morph is a different phylogenetic species. In order to further evaluate this new taxonomic interpretation, the present contribution explores to what extent populations or color morphs indeed consist of single or few MLG. As such it is shown that both morphs are not single, homozygous MLG, but instead reveal a considerable amount of allelic variation and substantial numbers of heterozygous microsatellite genotypes. This suggests that outcrossing may be more prevalent than previously reported. Nevertheless, both morphs maintain a diagnostic multimarker differentiation in the presence of outcrossing in sympatric conditions, implying that they may be interpreted as species under the biological species concept. Finally, our data challenge the idea that simultaneous hermaphrodites should be either strict selfers or strict outcrossers.


Allozymes Microsatellites DNA sequences Color polymorphism Population genetics Self-fertilization 



We are indebted to all the persons who collected specimens and helped us in various ways, as well as to Claúdia Patrão (University of Algarve, Portugal), Dr. Patrick Mardulyn (Free University of Brussels, Belgium) and to the Botanical Garden from the University of Montpellier. V. Prévot was a PhD fellow at the FNRS (Belgium). Financial support was provided by the “Fonds David et Alice Van Buuren” to VP and by BELSPO Action 1 project MO/36/017 to TB. This work was conducted within the framework of the BELSPO IUAP program “SPEEDY” and the FWO research community BeBOL.

Supplementary material

10709_2013_9727_MOESM1_ESM.doc (163 kb)
Supplementary material 1 (DOC 163 kb)


  1. Backeljau T (1987) Electrophoretic distinction between Arion hortensis, A. distinctus and A. owenii (Mollusca: Pulmonata). Zool Anz 219:33–39Google Scholar
  2. Backeljau T, Breugelmans K, Leirs H, Rodriguez T, Sherbakov D, Sitnikova T, Timmermans JM, Van Goethem JL, Verheyen E (1994) Application of isoelectric focusing in molluscan systematics. The Nautilus 2:156–167Google Scholar
  3. Backeljau T, de Bruyn L, De Wolf H, Jordaens K, Van Dongen S, Winnepenninckx B (1997) Allozyme diversity in slugs of the Carinarion complex (Mollusca, Pulmonata). Heredity 78:445–451CrossRefGoogle Scholar
  4. Batts JH (1957) Anatomy and life cycle of the snail Rumina decollata (Pulmonata: Achatinidae). Southw Nat 2:74–82CrossRefGoogle Scholar
  5. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996) GENETIX 4.05, logiciel sous WindowsTM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, Université de Montpellier II, Montpellier (France)Google Scholar
  6. Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631PubMedCrossRefGoogle Scholar
  7. Chiba S (2003) Species diversity and conservation of Mandarina, an endemic land snail of the Ogasawara Islands. Global Environ Res 7:29–37Google Scholar
  8. Dakin EE, Avise JC (2004) Microsatellite null alleles in parentage analysis. Heredity 93:504–509PubMedCrossRefGoogle Scholar
  9. David P, Pujol B, Viard F, Castella V, Goudet J (2007) Reliable selfing rate estimates from imperfect population genetic data. Mol Ecol 16:2474–2487PubMedCrossRefGoogle Scholar
  10. Dundee D (1986) Notes on the habits and anatomy of the introduced land snails, Rumina and Lamellaxis (Subulinidae). The Nautilus 100:32–37Google Scholar
  11. Escobar JS, Auld JR, Correa AC, Alonso JM, Bony YK, Coutellec M-A, Koene JM, Pointier J-P, Jarne P, David P (2011) Patterns of mating-system evolution in hermaphroditic animals: correlations among selfing rate, inbreeding depression, and the timing of reproduction. Evolution 65:1233–1253PubMedCrossRefGoogle Scholar
  12. Foltz DW, Schaitkin BM, Selander RK (1982) Gametic disequilibrium in the self-fertilizing slug Deroceras laeve. Evolution 36:80–85CrossRefGoogle Scholar
  13. Geenen S, Jordaens K, Castilho R, Backeljau T (2003) Congruence between starch gel and polyacrylamide gel electrophoresis in detecting allozyme variation in pulmonate land slugs. Electrophoresis 24:622–627PubMedCrossRefGoogle Scholar
  14. Geenen S, Jordaens K, Backeljau T (2006) Molecular systematics of the Carinarion complex (Mollusca: Gastropoda: Pulmonata): a taxonomic riddle caused by a mixed breeding system. Biol J Linn Soc 89:589–604CrossRefGoogle Scholar
  15. Giokas S, Mylonas M, Sotiropoulos K (2000) Gene flow and differential mortality in a contact zone between two Albinaria species (Gastropoda; Clausiliidae). Biol J Linn Soc 71:755–770CrossRefGoogle Scholar
  16. Goodwillie C, Kalisz S, Eckert CG (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annu Rev Ecol Syst 36:47–79CrossRefGoogle Scholar
  17. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from
  18. Harris H, Hopkinson DA (1976) Handbook of enzyme electrophoresis in human genetics. North Holland Publishing Company, AmsterdamGoogle Scholar
  19. Jarne P, Auld JR (2006) Animals mix it up too: the distribution of self-fertilization among hermaphroditic animals. Evolution 60:1816–1824PubMedGoogle Scholar
  20. Jordaens K, Geenen S, Reise H, Van Riel P, Verhagen R, Backeljau T (2000) Is there a geographical pattern in the breeding system of a complex of hermaphroditic slugs (Mollusca: Gastropoda: Carinarion)? Heredity 85:571–579PubMedCrossRefGoogle Scholar
  21. Lance SL, Jones KL, Hagen C, Jordaens K, Backeljau T, Prévot V (2010) Fifteen microsatellite loci for the decollate snail, Rumina decollata. Conserv Genet Resour 2:287–289CrossRefGoogle Scholar
  22. Mayr E (1970) Populations, species, and evolution. Harvard University Press, CambridgeGoogle Scholar
  23. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedGoogle Scholar
  24. Nicklas NL, Hoffman RJ (1981) Apomictic parthenogenesis in a hermaphroditic terrestrial slug, Deroceras laeve (Müller). Biol Bull 160:123–135CrossRefGoogle Scholar
  25. Prévot V, Jordaens K, Sonet G, Backeljau T (2013) Exploring species level taxonomy and species delimitation methods in the facultatively self-fertilizing land snail genus Rumina (Gastropoda: Pulmonata). PLoS ONE 8(4):e60736. doi: 10.1371/journal.pone.0060736 PubMedCrossRefGoogle Scholar
  26. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  27. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  28. Selander RK, Hudson RO (1976) Animal population structure under close inbreeding: the land snail Rumina in southern France. Am Nat 110:695–718CrossRefGoogle Scholar
  29. Selander RK, Kaufman DW (1973) Self-fertilization and genetic population structure in a colonizing land snail. Proc Natl Acad Sci USA 70:1186–1190PubMedCrossRefGoogle Scholar
  30. Selander RK, Ochman H (1983) The genetic structure of populations as illustrated by molluscs. Isozymes: Curr Top Biol Med Res 10: Genet Evol: 93–123Google Scholar
  31. Selander RK, Kaufman DW, Ralin RS (1974) Self-fertilization in the terrestrial snail Rumina decollata. The Veliger 16:265–270Google Scholar
  32. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  33. Viard F, Justy F, Jarne P (1997) The influence of self-fertilization and population dynamics on the genetic structure of subdivided populations: a case study using microsatellite markers in the freshwater snail Bulinus truncatus. Evolution 51:1518–1528CrossRefGoogle Scholar
  34. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  35. Woodruff DS, Gould SJ (1987) Fifty years of interspecific hybridization: genetics and morphometrics of a controlled experiment involving the land snail Cerion in Florida. Evolution 41:1022–1045CrossRefGoogle Scholar
  36. Wright S (1943) Isolation by distance. Genetics 28:114–138PubMedGoogle Scholar
  37. Wright S (1978) Evolution and the genetics of populations. University of Chicago Press, ChicagoGoogle Scholar
  38. Yeh FC, Yang R-C, Boyle TBJ, Ye Z-H, Mao XJ (1997) POPGENE, the user-friendly shareware for population genetic analysis. University of Alberta, Canada, Molecular Biology and Biotechnology CentreGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Vanya Prévot
    • 1
    • 2
  • Kurt Jordaens
    • 3
    • 4
  • Natalie Van Houtte
    • 3
  • Gontran Sonet
    • 4
  • Kenny Janssens
    • 1
  • Rita Castilho
    • 5
  • Thierry Backeljau
    • 1
    • 3
  1. 1.Department of Invertebrates and JEMURoyal Belgian Institute of Natural SciencesBrusselsBelgium
  2. 2.Laboratoire d’Evolution Biologique et EcologieUniversité Libre de Bruxelles (ULB)BrusselsBelgium
  3. 3.Evolutionary Ecology GroupUniversity of AntwerpAntwerpBelgium
  4. 4.Joint Experimental Molecular Unit (JEMU)Royal Museum for Central AfricaTervurenBelgium
  5. 5.Centro de Ciências do Mar (CCMAR)Universidade do AlgarveFaroPortugal

Personalised recommendations