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

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Abstract

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.

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References

  • 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.

    Article  Google Scholar 

  • Blainville, H.-M., 1824. Pleurocere Pleurocerus. Dictionnaire des Sciences Naturelles 32: 236.

    Google Scholar 

  • 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 

  • Brönmark, C., T. Lakowitz & J. Hollander, 2011. Predator-induced morphological plasticity across local populations of a freshwater snail. PLoS ONE 6(7): e21773.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Cavalli-Sforza, L. L. & A. F. Edwards, 1967. Phylogenetic analysis: models and estimation procedures. Evolution 21: 550–570.

    Article  Google Scholar 

  • Chambers, S., 1980. Genetic divergence between populations of Goniobasis occupying different drainage systems. Malacologia 20: 113–120.

    Google Scholar 

  • Conrad, T. A., 1834. New Freshwater Shells of the United States. Self-published, Philadelphia.

    Google Scholar 

  • Dazo, B., 1965. The morphology and natural history of Pleurocera acuta and Goniobasis livescens (Gastropoda: Cerithiacea: Pleuroceridae). Malacologia 3: 1–80.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • DeWitt, T., A. Sih & D. S. Wilson, 1998. Costs and limits of phenotypic plasticity. Trends in Ecology and Evolution 13: 77–81.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • Dillon R, T. Jr, 1984. Geographic distance, environmental difference, and divergence between isolated populations. Systematic Zoology 33: 69–82.

    Article  Google Scholar 

  • Dillon R, T. Jr, 1991. Karyotypic evolution in pleurocerid snails: II. Pleurocera, Goniobasis, and Juga. Malacologia 33: 339–344.

    Google Scholar 

  • Dillon R, T. Jr, 1992. Electrophoresis IV, nuts and bolts. World Aquaculture 23(2): 48–51.

    Google Scholar 

  • Dillon R, T. Jr, 2000. The Ecology of Freshwater Molluscs. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Felsenstein, J., 2004. PHYLIP (Phylogeny Inference Package) version 3.65. Privately distributed, University of Washington, Seattle.

  • Fox, J., M. Friendly & G. Monette, 2012. Heplots: Visualizing tests in multivariate linear models. R package version 1.0-0. CRAN.R-project.org/package = heplots.

  • Gilbert, J., 1966. Rotifer ecology and embryological induction. Science 151: 1234–1237.

    Article  PubMed  CAS  Google Scholar 

  • Goodrich, C., 1934. Studies of the gastropod family Pleuroceridae – II. Occasional Papers of the Museum of Zoology, University of Michigan 295: 1–6.

  • Goodrich, C., 1937. Studies of the gastropod family Pleuroceridae – VI. Occasional Papers of the Museum of Zoology, University of Michigan 347: 1–12.

  • Goodrich, C., 1939a. Pleuroceridae of the St. Lawrence River Basin. Occasional Papers of the Museum of Zoology, University of Michigan 404: 1–4.

  • 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.

  • Goodrich, C., 1940. The Pleuroceridae of the Ohio River system. Occasional Papers of the Museum of Zoology, University of Michigan 417: 1–21.

  • Goodrich, C. & H. van der Schalie, 1944. A revision of the Mollusca of Indiana. American Midland Naturalist 32: 257–326.

    Article  Google Scholar 

  • Hoggatt. R. E., 1975. Drainage areas of Indiana streams. Department of the Interior, U. S. Geological Survey, Indianapolis.

  • Holomuzki, J. & B. Biggs, 2006. Habitat-specific variation and performance trade-offs in shell armature of New Zealand mudsnails. Ecology 87: 1038–1047.

    Article  PubMed  Google Scholar 

  • Houp, K., 1970. Population dynamics of Pleurocera acuta in a central Kentucky limestone stream. American Midland Naturalist 83: 81–88.

    Article  Google Scholar 

  • Hoverman, J. & R. Relyea, 2007. The rules of engagement: how to defend against combinations of predators. Oecologia 154: 551–560.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Krist, A., 2002. Crayfish induce a defensive shell shape in a freshwater snail. Invertebrate Zoology 121: 235–242.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • Langerhans, R. B. & T. DeWitt, 2002. Plasticity constrained: over-generalized induction cues cause maladaptive phenotypes. Evolutionary Ecology Research 4: 857–870.

    Google Scholar 

  • Langerhans, R. B. & T. DeWitt, 2004. Shared and unique features of evolutionary diversification. The American Naturalist 164: 335–349.

    Article  PubMed  Google Scholar 

  • Magruder, S., 1935. The anatomy of the freshwater prosobranchiate gastropod, Pleurocera canaliculatum undulatum (Say). American Midland Naturalist 16: 883–912.

    Article  Google Scholar 

  • Minton, R., A. Norwood & D. Hayes, 2008. Quantifying phenotypic gradients in freshwater snails: a case study in Lithasia (Gasatropoda: Pleuroceridae). Hydrobiologia 605: 173–182.

    Article  Google Scholar 

  • Nei, M., 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583–590.

    PubMed  CAS  Google Scholar 

  • Ortmann, A., 1920. Correlation of shape and station in freshwater mussels (naiades). Proceedings of the American Philosophical Society 59: 269–312.

    Google Scholar 

  • Poulik, M., 1957. Starch gel electrophoresis in a discontinuous system of buffers. Nature 180: 1477–1479.

    Article  PubMed  CAS  Google Scholar 

  • 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 http://www.R-project.org/.

  • Rohlf, F. J., 2007. tpsRelw version 1.45. State University of New York, Stony Brook.

  • Rohlf, F. J., 2008. tpsDig version 2.11. State University of New York, Stony Brook.

  • Rohlf, F. J., 2011. tpsRegr version 1.38. State University of New York, Stony Brook.

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • Scheiner, S., 1993. Genetics and the evolution of phenotypic plasticity. Annual Review of Ecology and Systematics 24: 35–68.

    Article  Google Scholar 

  • Shaw, C. R. & R. Prasad, 1970. Starch gel electrophoresis of enzymes – a compilation of recipes. Biochemical Genetics 4: 297–320.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  Google Scholar 

  • Urabe, M., 2000. Phenotypic modulation by the substratum of shell sculpture in Semisulcospira reiniana (Prosobranchia: Pleuroceridae). Journal of Molluscan Studies 66: 53–60.

    Article  Google Scholar 

  • 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 

  • Wright, S., 1978. Evolution and the Genetics of Populations. Vol 4, Variability Within and Among Natural Populations. University of Chicago Press, Chicago.

    Google Scholar 

  • 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 

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Acknowledgments

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

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Correspondence to Robert T. Dillon.

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Handling editor: John Havel

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Dillon, R.T., Jacquemin, S.J. & Pyron, M. Cryptic phenotypic plasticity in populations of the freshwater prosobranch snail, Pleurocera canaliculata . Hydrobiologia 709, 117–127 (2013). https://doi.org/10.1007/s10750-012-1441-1

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