Biological Invasions

, Volume 16, Issue 12, pp 2615–2626 | Cite as

Parallel variation among populations in the shell morphology between sympatric native and invasive aquatic snails

  • Erica J. KistnerEmail author
  • Mark F. Dybdahl
Original Paper


A phenotypic response, either plastic or evolved, is often required for successful invasion of novel environments. Populations of the invasive snail Potamopyrgus antipodarum have colonized a wide range of environments in the western U. S. since 1985, but the extent of plastic adjustment and evolved adaptation to local environments is largely unknown. We examined variation in shell morphology among four sites in the Snake River, Idaho, including both still-water and free-flowing river habitats and compared the variation to that of a native snail (Pyrgulopsis robusta) using geometric morphometric techniques. Using Generalized Procrustes analysis, we tested for phenotypic responses by determining (1) whether Po. antipodarum from the four locations differed in shell morphology, and (2) whether these snails exhibited corresponding shell shape variation with sympatric populations of a native snail. Both native and invasive snails exhibited similar variation in shell morphology across three of the four sites. The Canonical Variate assignment test grouped 85 % of both snail species to their rightful sample site. In addition, the Principal Component Analysis displayed similar patterns of shell variation across the four sites, indicating parallel variation in shell shape. For three of the four sites, both the native and invasive snails exhibited differences in shell shape consistent with water flow variation (still-water versus fast free-flowing river). Taken together, these results suggest that the shell shape of the invasive snail has changed either through plasticity or evolution, and that both native and invasive snail populations responded to local environmental conditions in a similar manner.


Biological invasions Phenotypic plasticity Adaptive evolution Shell morphology Potamopyrgus antipodarum Pyrgulopsis robusta 



We thank Patrick Carter, Richard Golmulkiewicz, Leslie Riley, Devin Drown, Sarah Redd, Daniel Borkowski, and three anonymous reviewers for valuable feedback in preparation of this manuscript. We extend a special thanks to William Clark at the Orma J. Smith Museum of Natural History for loaning the Py. robusta shell samples used in this study. We are grateful to Marc Evans for statistical advice.


  1. Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294:321–326. doi: 10.1126/science.1060701 PubMedCrossRefGoogle Scholar
  2. Baker HG (1965) Characteristics and modes of origin of weeds. In: Baker HG, Stebbins GL (eds) The genetics of colonizing species. Academic Press, New York, pp 147–168Google Scholar
  3. Bonduriansky R, Crean AJ, Day T (2011) The implications of nongenetic inheritance for evolution in changing environments. Evol Appl 5:192–201. doi: 10.1111/j.1752-4571.2011.00213.x PubMedCentralCrossRefGoogle Scholar
  4. Bourdeau PE (2009) Prioritized phenotypic responses to combined predators in a marine snail. Ecology 90:1659–1669. doi: 10.1890/08-1653.1 PubMedCrossRefGoogle Scholar
  5. Bourdeau PE (2010) An inducible morphological deference is a passive by-product of behavior in a marine snail. Proc R Soc B 277:455-463. doi: 10.1098/rspb.2009.1295
  6. Butin E, Porter AH, Elkington J (2005) Adaptation during biological invasions and the case of Adelges tsuga. Evol Ecol Res 7:887–900Google Scholar
  7. Drown DM, Levri EP, Dybdahl MF (2010) Invasive genotypes are opportunistic specialists not general purpose genotypes. Evol App 4:132–143. doi: 10.1111/j.1752-4571.2010.00149.x CrossRefGoogle Scholar
  8. Dussart GJ (1987) Effects of water flow on the detachment of some aquatic pulmonate gastropods. Am Malacol Bull 5:65–72Google Scholar
  9. Dybdahl MF, Drown DM (2011) The absence of genotypic diversity in a successful parthenogenetic invader. Biol Invasions 13:1663–1672. doi: 10.1007/s10530-010-9923-4 CrossRefGoogle Scholar
  10. Dybdahl MF, Kane SL (2005) Adaptation versus phenotypic plasticity in the success of a clonal invader. Ecology 86:1592–1601. doi: 10.1890/04-0898 CrossRefGoogle Scholar
  11. Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407. doi: 10.1111/j.1365-2435.2007.01283.x CrossRefGoogle Scholar
  12. Haase M (2003) Clinal variation in shell morphology of the freshwater gastropod Po. antipodarum antipodarum along two hill-country streams in New Zealand. J R Soc N Z 33:549–560. doi: 10.1080/03014223.2003.9517743 CrossRefGoogle Scholar
  13. Hall RO, Dybdahl MF, Vanerloop MC (2006) Extremely high secondary production of introduced snails in rivers. Ecol Appl 16:1121–1131. doi: 10.1890/1051-0761(2006)016[1121:EHSPOI]2.0.CO;2 Google Scholar
  14. Hauser L, Carvalho GR, Hughes RN, Carter RE (1992) Clonal structure of the introduced freshwater snail NZ mudsnail (Prosobranchia: Hydrobiidae), as revealed by DNA fingerprinting. Proc R Soc Lond B 249:19–25. doi: 10.1098/rspb.1992.0078 CrossRefGoogle Scholar
  15. Hershler R, Liu H (2004) Taxonomic reappraisal of species assigned to the North American freshwater gastropod subgenus Natricola (Rissooidea: Hydrobiidae). Veliger 47:66–81Google Scholar
  16. Hershler R, Liu HP, Clark WH (2010) Microsatellite evidence of invasion and rapid spread of divergent New Zealand mudsnail (Po. antipodarum antipodarum) clones in the Snake River basin, Idaho USA. Biol Invasions 12:1521–1532. doi: 10.1007/s10530-009-9564-7 CrossRefGoogle Scholar
  17. Holomuzki JR, Biggs BJF (2006) Habitat-specific variation and performance trade-offs in shell armature of New Zealand mud snails. Ecology 87:1038–1047. doi: 10.1890/0012-9658(2006)87[1038:HVAPTI]2.0.CO;2 Google Scholar
  18. Janson K, Sundberg P (1983) Multivariate morphometric analysis of two varieties of Littorina saxatilis from the Swedish west coast. Mar Biol 32:9–15. doi: 10.1007/BF00394274 Google Scholar
  19. Kemp P, Bertness MD (1984) Snail shapes and growth rates: evidence for plastic shell allometry in Littorina littorea. Proc Natl Acad Sci USA 81:811–813PubMedCentralPubMedCrossRefGoogle Scholar
  20. Kerans BL, Dybdahl MF, Gangloff MM, Jannot J (2005) Macroinvertebrate assemblages and the New Zealand mud snail, a recent invader to streams of the greater Yellowstone ecosystem. J North Am Benthol Soc 24:123–138. doi: 10.1899/0887-3593(2005)024<0123:PADDAE>2.0.CO;2
  21. Kistner EK, Dybdahl MF (2013) Adaptive responses and invasion: the role of plasticity and evolution in snail shell morphology. Ecol Evol 3:424–436. doi: 10.1002/ece3.471 PubMedCentralPubMedCrossRefGoogle Scholar
  22. Lee CE (2002) Evolutionary genetics of invasive species. Trend Ecol Evol 17:386–391. doi: CrossRefGoogle Scholar
  23. Lee CE, Gelembiuk GW (2008) Evolutionary origins of invasive populations. Evol Appl 1:427–448. doi: 10.1111/j.1752-4571.2008.00039.x PubMedCentralCrossRefGoogle Scholar
  24. Lee CE, Remfert JL, Gelembiuk GW (2003) Evolution of physiological tolerance and performance during freshwater invasion events. Integr Comp Biol 43:439–449. doi: 10.1093/icb/43.3.439 PubMedCrossRefGoogle Scholar
  25. Legar EA, Rice KJ (2003) Invasive California poppies (Eschscholzia californica Cham.) grow larger than native individuals under reduced competition. Ecol Lett 6:257–264. doi: 10.1046/j.1461-0248.2003.00423.x CrossRefGoogle Scholar
  26. Lele SR, Richtsmeier JT (2010) An invariant approach to statistical analysis of shapes. CRC Press, New YorkGoogle Scholar
  27. Lombaert E, Malausa T, Devred R, Estoup A (2008) Phenotypic variation in invasive and biocontrol populations of the harlequin ladybird, Harmonia axyridis. Biocontrol 53:89–102. doi: 10.1007/s10526-007-9131-z CrossRefGoogle Scholar
  28. McDowell S, Lee C (2002) Photosynthetic characteristics of invasive and non-invasive species of Rubus (Rosaceae). Am J Bot 89:1431–1438. doi: 10.3732/ajb.89.9.1431 PubMedCrossRefGoogle Scholar
  29. Minton R, Resse S, Swanger K, Perez K, Hayes D (2007) Changes in shell morphology of Elimia comalensis (Gastropoda: Pleuroceridae) from the Edwards Plateau, Texas. Southwest Nat 52:475–481. doi: 10.1894/0038-4909(2007)52[475:CISMOE]2.0.CO;2 Google Scholar
  30. Minton R, Lewis E, Netherland B, Hayes D (2011) Large differences over small distances: plasticity in the shells of Elimia potosiensis (Gastopoda: Pleuroceridae). Int J Biol 3:23–32. doi: 10.5539/ijb.v3n1p23 Google Scholar
  31. Mitteroecker P, Gunz P (2009) Advances in geometric morphometrics. Evol Biol 36:235–247. doi: 10.1007/s11692-009-9055-x CrossRefGoogle Scholar
  32. Negovetic S, Jokela J (2001) Life history variation, phenotypic plasticity, and subpopulation structure in a freshwater snail. Ecology 82:2805–2815. doi: 10.1890/0012-9658(2001)082[2805:LHVPPA]2.0.CO;2 Google Scholar
  33. Ponder WF (1988) NZ mudsnail, a Molluscan colonizer of Europe and Australia. J Mollusca Stud 54:271–286CrossRefGoogle Scholar
  34. Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ (2008) Adaptive evolution in invasive species. Trend Plant Sci 13:288–294. doi: 10.1016/j.tplants.2008.03.004 CrossRefGoogle Scholar
  35. Proctor T, Kerans B, Clancey P, Ryce E, Dybdahl M, Gustafson D, Hall R, Pickett F, Richards D, Waldeck RD,Chapman J, Wiltshire RH, Becker D, Anderson M, Pitman B, Lassuy D, Heimowitz P, Dwyer P, Levri EP (2007) National management and control plan for the New ZealandMudsnail (Po. antipodarum antipodarum). US Fish and Wildlife Service Report. 11 Dec 2012
  36. Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993. doi: 10.1111/j.1461-0248.2006.00950.x PubMedCrossRefGoogle Scholar
  37. Riley LA, Dybdahl MF, Hall RO (2008) Invasive species impact: asymmetric interactions between invasive and endemic freshwater snails. J N Benthol Soc 27:509–520. doi: 10.1899/07-119.1 CrossRefGoogle Scholar
  38. Rohlf FJ (1997) TPSDIG2. Department of Ecology and Evolution, State University of New York, Stony Book (available by ftp from Scholar
  39. Rolan-Alvarez E, Johannesson K, Erlandsson J (1997) Maintenance of a cline in the marine snail Littorina saxatilis: the role of home site advantage and hybrid fitness. Evolution 51:1838–1847. doi: 10.2307/2411006 CrossRefGoogle Scholar
  40. SAS Institute (2004) SAS/STAT 9.1 users’ guide. SAS Institute, Cary, North Carolina, USAGoogle Scholar
  41. Schilthuizen M, Haase H (2010) Disentangling true shape differences and experimenter bias: are dextral and sinistral snail shells exact mirror images. J Zool 282:191–200. doi: 10.1111/j.1469-7998.2010.00729.x CrossRefGoogle Scholar
  42. Schweitzer JA, Larson KC (1999) Greater morphological plasticity of exotic honeysuckle species may make them better invaders than native species. J Torre Bot Soc 126:15–23. doi: 10.2307/2997251 CrossRefGoogle Scholar
  43. Sheets DH (2011) IMP software. Department of Physics, Canisius College, Buffalo, NY, 14208, Department of Geology, SUNY at Buffalo, Buffalo NY 14260 (
  44. Statzner B, Holm TF (1989) Morphological adaptation of shape to flow: microcurrents around lotic macroinvertebrates with known Reynolds numbers at quasi-natural flow condition. Oecologia 78:145–157. doi: 10.1007/BF00377150 CrossRefGoogle Scholar
  45. Stearns SC (1989) The evolutionary significance of phenotypic plasticity. Bioscience 7:436–445. doi: 10.2307/1311135 CrossRefGoogle Scholar
  46. Struhsaker JW (1968) Selection mechanisms associated with intraspecific snail variation in Littorina picta (Prosobranchia: Mesgastropoda). Evolution 22:459–480. doi: 10.2307/2406874 CrossRefGoogle Scholar
  47. Taylor DW (1985) Evolution of freshwater drainages and mollusks in Western North America. In: Smiley CJ (ed) Late Cenozoic history of the Pacific Northwest. American Association for the Advancement of Science, Pacific Division, San Francisco, CA, pp 265–321Google Scholar
  48. USGS National Water Information System (2013) USGS Water Data for Idaho. Accessed 10 Feb 2013
  49. Vermeij GJ (1995) A natural history of shells. Princeton University Press, PrincetonGoogle Scholar
  50. Yeh PJ, Price TD (2004) Adaptive plasticity and the successful colonization of a novel environment. Am Nat 164:531–542. doi: 10.1086/423825 PubMedCrossRefGoogle Scholar
  51. Young KA, Snooeks J, Seehausen O (2009) Morphological diversity and the roles of contingency, chance, and determinism in African cichlid radiations. PLoS One 4:1–8. doi: 10.1371/journal.pone.0004740 CrossRefGoogle Scholar
  52. Zaranko DT, Farara DG, Thompson FG (1997) Another exotic mollusk in the laureation great lakes: the New Zealand native Po. antipodarum antipodarum (Gray 1843) (Gastropoda, Hydrobiidae). Can J Fish Aquat Sci 54:809–814. doi: 10.1139/f96-343 CrossRefGoogle Scholar
  53. Zelditch ML, Swiderski DL, Sheets HD, Fink WL (2004) Geometric morphometrics for biologists: a primer. Elseiver Academic Press, New YorkGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.School of Biological SciencesWashington State UniversityPullmanUSA
  2. 2.Department of Biological Sciences, 090 Galvin Life Sciences CenterUniversity of Notre DameNotre DameUSA

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