, Volume 709, Issue 1, pp 117–127 | Cite as

Cryptic phenotypic plasticity in populations of the freshwater prosobranch snail, Pleurocera canaliculata

  • Robert T. DillonEmail author
  • Stephen J. Jacquemin
  • Mark Pyron
Primary Research Paper


We sampled four populations of the robustly shelled Pleurocera canaliculata from large rivers and five pleurocerid populations bearing more fusiform shells (nominally P. acuta and P. pyrenellum) from smaller streams in a study area extending from upstate New York to northern Alabama, USA. Gene frequencies at 9 allozyme-encoding loci revealed that each population of P. acuta or P. pyrenellum was more genetically similar to the P. canaliculata population inhabiting the larger river immediately downstream than to any nominal conspecific. Thus, the extensive intraspecific variation in shell robustness displayed by these nine populations has apparently been rendered cryptic by taxonomic confusion. We then employed geometric morphometrics to explore a gradient in shell morphology from the acuta form to the typical canaliculata form in 18 historic samples collected down the length of Indiana’s Wabash River. The shell forms appeared generally distinctive on the major axes yielded by relative warp analysis (increasing robustness and decreasing spire elongation), although some overlap was apparent. MANCOVA returned a significant relationship between multivariate shape variation and stream size, as measured by drainage area. Possible drivers for this phenomenon include an environmental cline in the risk of dislodgement due to hydrodynamic drag and shifts in the community of predators.


Gastropoda Inducible defenses Shell morphology Allozyme electrophoresis Geometric morphometrics Predation 



We thank Dr. Thomas DeWitt for his helpful advice and suggestions on the morphometric analysis.

Supplementary material

10750_2012_1441_MOESM1_ESM.pdf (199 kb)
Supplementary material 1 (PDF 198 kb)


  1. Auld, J. & R. Relyea, 2011. Adaptive plasticity in predator-induced defenses in a common freshwater snail: altered selection and mode of predation due to prey phenotype. Evolutionary Ecology 25: 189–202.CrossRefGoogle Scholar
  2. Blainville, H.-M., 1824. Pleurocere Pleurocerus. Dictionnaire des Sciences Naturelles 32: 236.Google Scholar
  3. Britton, D. & R. McMahon, 2004. Environmentally and genetically induced shell-shape variation in the freshwater pond snail Physa (Physella) virgata (Gould, 1855). American Malacological Bulletin 19: 93–100.Google Scholar
  4. Brönmark, C., T. Lakowitz & J. Hollander, 2011. Predator-induced morphological plasticity across local populations of a freshwater snail. PLoS ONE 6(7): e21773.PubMedCrossRefGoogle Scholar
  5. Brönmark, C., T. Lakowitz, P. Nilson, J. Ahlgren, C. Lennartsdotter & J. Hollander, 2012. Costs of inducible defence along a resource gradient. PLoS ONE 7(1): e30467.PubMedCrossRefGoogle Scholar
  6. Cavalli-Sforza, L. L. & A. F. Edwards, 1967. Phylogenetic analysis: models and estimation procedures. Evolution 21: 550–570.CrossRefGoogle Scholar
  7. Chambers, S., 1980. Genetic divergence between populations of Goniobasis occupying different drainage systems. Malacologia 20: 113–120.Google Scholar
  8. Conrad, T. A., 1834. New Freshwater Shells of the United States. Self-published, Philadelphia.Google Scholar
  9. Dazo, B., 1965. The morphology and natural history of Pleurocera acuta and Goniobasis livescens (Gastropoda: Cerithiacea: Pleuroceridae). Malacologia 3: 1–80.Google Scholar
  10. DeWitt, T., 1998. Costs and limits of phenotypic plasticity: tests with predator-induced morphology and life history in a freshwater snail. Journal of Evolutionary Biology 11: 465–480.CrossRefGoogle Scholar
  11. DeWitt, T., A. Sih & D. S. Wilson, 1998. Costs and limits of phenotypic plasticity. Trends in Ecology and Evolution 13: 77–81.PubMedCrossRefGoogle Scholar
  12. DeWitt, T., A. Sih & J. Hucko, 1999. Trait compensation and cospecialization in a freshwater snail: size, shape, and antipredator behaviour. Animal Behaviour 58: 397–407.PubMedCrossRefGoogle Scholar
  13. DeWitt, T., B. Robinson & D. S. Wilson, 2000. Functional diversity among predators of a freshwater snail imposes an adaptive trade-off for shell morphology. Evolutionary Ecology Research 2: 129–148.Google Scholar
  14. Dillon R, T. Jr, 1984. Geographic distance, environmental difference, and divergence between isolated populations. Systematic Zoology 33: 69–82.CrossRefGoogle Scholar
  15. Dillon R, T. Jr, 1991. Karyotypic evolution in pleurocerid snails: II. Pleurocera, Goniobasis, and Juga. Malacologia 33: 339–344.Google Scholar
  16. Dillon R, T. Jr, 1992. Electrophoresis IV, nuts and bolts. World Aquaculture 23(2): 48–51.Google Scholar
  17. Dillon R, T. Jr, 2000. The Ecology of Freshwater Molluscs. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  18. Dillon R, T. Jr, 2011. Robust shell phenotype is a local response to stream size in the genus Pleurocera (Rafinesque, 1818). Malacologia 53: 265–277.CrossRefGoogle Scholar
  19. Dillon R, T. Jr. & G. Davis, 1980. The Goniobasis of southern Virginia and northwestern North Carolina: genetic and shell morphometric relationships. Malacologia 20: 83–98.Google Scholar
  20. Dillon R, T. Jr. & R. Frankis, 2004. High levels of mitochondrial DNA sequence divergence in isolated populations of the freshwater snail genus Goniobasis. American Malacological Bulletin 19: 69–77.Google Scholar
  21. Dillon R, T. Jr. & J. Herman, 2009. Genetics, shell morphology, and life history of the freshwater pulmonate limpets Ferrissia rivularis and Ferrissia fragilis. Journal of Freshwater Ecology 24: 261–271.CrossRefGoogle Scholar
  22. Dillon R, T. Jr. & A. J. Reed, 2002. A survey of genetic variation at allozyme loci among Goniobasis populations inhabiting Atlantic drainages of the Carolinas. Malacologia 44: 23–31.Google Scholar
  23. Dillon R, T. Jr. & J. Robinson, 2011. The opposite of speciation: genetic relationships among the populations of Pleurocera (Gastropoda, Pleuroceridae) in central Georgia. American Malacological Bulletin 29: 159–168.CrossRefGoogle Scholar
  24. Dunithan, A., S. Jacquemin & M. Pyron, 2012. Morphology of Elimia livescens (Mollusca: Pleuroceridae) in Indiana, U.S.A. covaries with environmental variation. American Malacological Bulletin 30: 127–133.CrossRefGoogle Scholar
  25. Felsenstein, J., 2004. PHYLIP (Phylogeny Inference Package) version 3.65. Privately distributed, University of Washington, Seattle.Google Scholar
  26. Fox, J., M. Friendly & G. Monette, 2012. Heplots: Visualizing tests in multivariate linear models. R package version 1.0-0. = heplots.Google Scholar
  27. Gilbert, J., 1966. Rotifer ecology and embryological induction. Science 151: 1234–1237.PubMedCrossRefGoogle Scholar
  28. Goodrich, C., 1934. Studies of the gastropod family Pleuroceridae – II. Occasional Papers of the Museum of Zoology, University of Michigan 295: 1–6.Google Scholar
  29. Goodrich, C., 1937. Studies of the gastropod family Pleuroceridae – VI. Occasional Papers of the Museum of Zoology, University of Michigan 347: 1–12.Google Scholar
  30. Goodrich, C., 1939a. Pleuroceridae of the St. Lawrence River Basin. Occasional Papers of the Museum of Zoology, University of Michigan 404: 1–4.Google Scholar
  31. Goodrich, C., 1939b. Pleuroceridae of the Mississippi River basin exclusive of the Ohio River system. Occasional Papers of the Museum of Zoology, University of Michigan 406: 1–4.Google Scholar
  32. Goodrich, C., 1940. The Pleuroceridae of the Ohio River system. Occasional Papers of the Museum of Zoology, University of Michigan 417: 1–21.Google Scholar
  33. Goodrich, C. & H. van der Schalie, 1944. A revision of the Mollusca of Indiana. American Midland Naturalist 32: 257–326.CrossRefGoogle Scholar
  34. Hoggatt. R. E., 1975. Drainage areas of Indiana streams. Department of the Interior, U. S. Geological Survey, Indianapolis.Google Scholar
  35. Holomuzki, J. & B. Biggs, 2006. Habitat-specific variation and performance trade-offs in shell armature of New Zealand mudsnails. Ecology 87: 1038–1047.PubMedCrossRefGoogle Scholar
  36. Houp, K., 1970. Population dynamics of Pleurocera acuta in a central Kentucky limestone stream. American Midland Naturalist 83: 81–88.CrossRefGoogle Scholar
  37. Hoverman, J. & R. Relyea, 2007. The rules of engagement: how to defend against combinations of predators. Oecologia 154: 551–560.PubMedCrossRefGoogle Scholar
  38. Hoverman, J. & R. Relyea, 2009. Survival trade-offs associated with inducible defences in snails: the roles of multiple predators and developmental plasticity. Functional Ecology 23: 1179–1188.CrossRefGoogle Scholar
  39. Hoverman, J. & R. Relyea, 2011. The long-term population impacts of predators on prey: inducible defenses, population dynamics, and indirect effects. Oikos 121: 1219–1230.CrossRefGoogle Scholar
  40. Krist, A., 2002. Crayfish induce a defensive shell shape in a freshwater snail. Invertebrate Zoology 121: 235–242.CrossRefGoogle Scholar
  41. Lakowitz, T., C. Brönmark & P. Nyström, 2008. Tuning into multiple predators: conflicting demands for shell morphology in a freshwater snail. Freshwater Biology 53: 2184–2191.Google Scholar
  42. Lam, P. & P. Calow, 1988. Differences in the shell shape of Lymnaea peregra (Muller) (Gastropoda: Pulmonata) from lotic and lentic habitats; environmental or genetic variance? Journal of Molluscan Studies 54: 197–207.CrossRefGoogle Scholar
  43. Langerhans, R. B. & T. DeWitt, 2002. Plasticity constrained: over-generalized induction cues cause maladaptive phenotypes. Evolutionary Ecology Research 4: 857–870.Google Scholar
  44. Langerhans, R. B. & T. DeWitt, 2004. Shared and unique features of evolutionary diversification. The American Naturalist 164: 335–349.PubMedCrossRefGoogle Scholar
  45. Magruder, S., 1935. The anatomy of the freshwater prosobranchiate gastropod, Pleurocera canaliculatum undulatum (Say). American Midland Naturalist 16: 883–912.CrossRefGoogle Scholar
  46. Minton, R., A. Norwood & D. Hayes, 2008. Quantifying phenotypic gradients in freshwater snails: a case study in Lithasia (Gasatropoda: Pleuroceridae). Hydrobiologia 605: 173–182.CrossRefGoogle Scholar
  47. Nei, M., 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583–590.PubMedGoogle Scholar
  48. Ortmann, A., 1920. Correlation of shape and station in freshwater mussels (naiades). Proceedings of the American Philosophical Society 59: 269–312.Google Scholar
  49. Poulik, M., 1957. Starch gel electrophoresis in a discontinuous system of buffers. Nature 180: 1477–1479.PubMedCrossRefGoogle Scholar
  50. R Development Core Team. 2011. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL
  51. Rohlf, F. J., 2007. tpsRelw version 1.45. State University of New York, Stony Brook.Google Scholar
  52. Rohlf, F. J., 2008. tpsDig version 2.11. State University of New York, Stony Brook.Google Scholar
  53. Rohlf, F. J., 2011. tpsRegr version 1.38. State University of New York, Stony Brook.Google Scholar
  54. Rundle, S., J. Spicer, R. Coleman, J. Vosper & J. Soane, 2004. Environmental calcium modifies induced defences in snails. Proceedings of the Royal Society of London B (Suppl.) 271: S67–S70.CrossRefGoogle Scholar
  55. Say, T., 1821. Descriptions of univalve shells of the United States. Journal of the Academy of Natural Sciences of Philadelphia 2: 149–179.Google Scholar
  56. Scheiner, S., 1993. Genetics and the evolution of phenotypic plasticity. Annual Review of Ecology and Systematics 24: 35–68.CrossRefGoogle Scholar
  57. Shaw, C. R. & R. Prasad, 1970. Starch gel electrophoresis of enzymes – a compilation of recipes. Biochemical Genetics 4: 297–320.PubMedCrossRefGoogle Scholar
  58. Strong, E., 2005. A morphological reanalysis of Pleurocera acuta Rafinesque, 1831, and Elimia livescens (Menke, 1830) (Gastropoda: Cerithioidea: Pleuroceridae). Nautilus 119: 119–132.Google Scholar
  59. Swofford, D. & R. Selander, 1981. BIOSYS-1: a FORTRAN program for the comprehensive analysis of electrophoretic data in population genetics and systematics. Journal of Heredity 72: 281–283.Google Scholar
  60. Urabe, M., 1998. Contribution of genetic and environmental factors to shell shape variation in the lotic snail Semisulcospira reiniana (Prosobranchia: Pleuroceridae). Journal of Molluscan Studies 64: 329–343.CrossRefGoogle Scholar
  61. Urabe, M., 2000. Phenotypic modulation by the substratum of shell sculpture in Semisulcospira reiniana (Prosobranchia: Pleuroceridae). Journal of Molluscan Studies 66: 53–60.CrossRefGoogle Scholar
  62. Woltereck, R., 1909. Wietere experimentelle Untersuchungen über Artveränderung, speziell über das Wesen quantitativer Artunterschiede bei Daphniden. Versuche Deutsche Zoologische Geselleschaft 19: 110–172.Google Scholar
  63. Wright, S., 1978. Evolution and the Genetics of Populations. Vol 4, Variability Within and Among Natural Populations. University of Chicago Press, Chicago.Google Scholar
  64. Zelditch, M. L., D. L. Swiderski, H. D. Sheets & W. L. Fink, 2004. Geometric Morphometrics for Biologists: A Primer. Elsevier Academic Press, London.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Robert T. Dillon
    • 1
    Email author
  • Stephen J. Jacquemin
    • 2
  • Mark Pyron
    • 2
  1. 1.Department of BiologyCollege of CharlestonCharlestonUSA
  2. 2.Aquatic Environment and Fisheries Center, Department of BiologyBall State UniversityMuncieUSA

Personalised recommendations