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Ecomorphology of a generalist freshwater gastropod: complex relations of shell morphology, habitat, and fecundity

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Abstract

Evolutionary and ecological situations in a species’ native and invasive ranges can be drastically different. This is the case for Potamopyrgus antipodarum Gray (1843) a morphologically highly variable freshwater snail native to New Zealand, where sexual and asexual individuals coexist and experience selective pressure by sterilizing endoparasites. By contrast, only a few asexual lineages have been established in invaded regions around the globe, where parasite infection is extremely rare. We analyzed the ecomorphology of 996 native P. antipodarum in a geometric morphometric framework, using brood size as proxy for fecundity, and mtDNA and nuclear SNPs to account for relatedness and identify reproductive mode. As expected, we found genetic and morphological diversity to be higher in native than in invasive snails investigated previously, but surprisingly no higher morphological diversity in sexual versus asexual individuals. The relationships between shell morphology, habitat, and fecundity were complex. Shape variation was primarily linked to genetic relatedness but specific environmental factors including flow rate induced similar shell shapes. By contrast, shell size was largely explained by environmental factors. Fecundity was correlated with size but showed trade-offs with shape in increasingly extreme conditions. With increasing flow and toward small springs, the trend of shell shape becoming wider was reversed, i.e., snails with narrower shells were brooding more embryos. We concluded that both genetic and environmental contributions to variation in shell morphology in P. antipodarum likely play an important role in the ability of this species to adapt to a wide spectrum of habitats.

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References

  • Alonso, Á., & Camargo, J. A. (2003). Short-term toxicity of ammonia, nitrite, and nitrate to the aquatic snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca). Bulletin of Environmental Contamination and Toxicology, 70(5), 1006–1012. https://doi.org/10.1007/s00128-003-0082-5.

    Article  CAS  PubMed  Google Scholar 

  • Alonso, Á., & Castro-Díez, P. (2008). What explains the invading success of the aquatic mud snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca)? Hydrobiologia, 614(1), 107–116.

    Article  Google Scholar 

  • Alonso, Á., & Castro-Díez, P. (2012). The exotic aquatic mud snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca): state of the art of a worldwide invasion. Aquatic Sciences, 74(3), 375–383. https://doi.org/10.1007/s00027-012-0254-7.

    Article  CAS  Google Scholar 

  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.

    Article  CAS  Google Scholar 

  • Bartoń, K. (2017). MuMIn: Multi-Model Inference. R package version 1.40.0. available at: https://CRAN.R-project.org/package=MuMIn.

  • Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1–48. https://doi.org/10.18637/jss.v067.i01.

    Article  Google Scholar 

  • Bell, G. (1982). The masterpiece of nature: the evolution and genetics of sexuality. CUP Archive.

  • Bookstein, F. L. (1991). Morphometric tools for landmark data. New York: Cambridge University Press.

    Google Scholar 

  • Bowler, P. A. (1991). The rapid spread of the freshwater hydrobiid snail Potamopyrgus antipodarum (gray) in the middle Snake River, southern Idaho. Proceedings of the Desert Fishes Council, 21, 173–182.

    Google Scholar 

  • Chambers, J. M., Cleveland, W. S., Kleiner, B., & Tukey, P. A. (1983) Graphical methods for data analysis. Wadsworth & Brooks/Cole.

  • Cichy, A., Marszewska, A., Parzonko, J., Żbikowski, J., & Żbikowska, E. (2017). Infection of Potamopyrgus antipodarum (Gray, 1843) (Gastropoda: Tateidae) by trematodes in Poland, including the first record of aspidogastrid acquisition. Journal of Invertebrate Pathology, 150(August), 32–34. https://doi.org/10.1016/j.jip.2017.09.003.

    Article  PubMed  Google Scholar 

  • Collado, G. A. (2014). Out of New Zealand: molecular identification of the highly invasive freshwater mollusk Potamopyrgus antipodarum (Gray, 1843) in South America. Zoological Studies, 53(1), 1–9. https://doi.org/10.1186/s40555-014-0070-y.

    Article  Google Scholar 

  • Development Core Team, R. (2011). R: a language and environment for statistical computing. Vienna: R foundation for Statistical Computing.

    Google Scholar 

  • DeWitt, T. J., Robinson, B. W., & Wilson, D. S. (2000). Functional diversity among predators of a freshwater snail imposes an adaptive trade-off for shell morphology. Evolutionary Ecology Research, 2(2), 129–148.

    Google Scholar 

  • Dybdahl, M. F., & Drown, D. M. (2011). The absence of genotypic diversity in a successful parthenogenetic invader. Biological Invasions, 13, 1663–1672.

    Article  Google Scholar 

  • Dybdahl, M. F., & Kane, S. L. (2005). Adaptation vs. phenotypic plasticity in the success of a clonal invader. Ecological Society of America, 86(6), 1592–1601.

    Google Scholar 

  • Dybdahl, M. F., & Lively, C. M. (1995). Diverse, endemic and polyphyletic clones in mixed populations of a freshwater snail (Potamopyrgus antipodarum). Journal of Evolutionary Biology, 8(3), 385–398. https://doi.org/10.1046/j.1420-9101.1995.8030385.x.

    Article  Google Scholar 

  • Excoffier, L., & Lischer, H. E. L. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10(3), 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x.

    Article  PubMed  Google Scholar 

  • Excoffier, L., Smouse, P. E., & Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131(2), 479–491. https://doi.org/10.1007/s00424-009-0730-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ficetola, G. F., Miaud, C., Pompanon, F., & Taberlet, P. (2008). Species detection using environmental DNA from water samples. Biology Letters, 4(4), 423–425. https://doi.org/10.1098/rsbl.2008.0118.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fox, J. (2003). Effect displays in R for generalised linear models. Journal of Statistical Software, 8(15), 1–27. https://doi.org/10.2307/271037.

    Article  Google Scholar 

  • Fox, J., & Weisberg, S. (2011). An R companion to applied regression (2nd ed.). Thousand Oaks: Sage.

    Google Scholar 

  • Fox, J., Dybdahl, M. F., Jokela, J., & Lively, C. M. (1996). Genetic structure of coexisting sexual and clonal subpopulations in a freshwater snail (Potamopyrgus antipodarum). Evolution, 50(4), 1541–1548. https://doi.org/10.2307/2410890.

    Article  PubMed  Google Scholar 

  • Fryer, G., & Iles, T. D. (1972). The cichlid fishes of the Great Lakes of Africa: Their biology and evolution. Scotland: Oliver and Boyd Press.

    Google Scholar 

  • Gangloff, M. M. (1998). The New Zealand mud snail in western North America. Aquatic Nuisance Species, 2, 25–30.

    Google Scholar 

  • Gérard, C., & Le Lannic, J. (2003). Establishment of a new host–parasite association between the introduced invasive species Potamopyrgus antipodarum (smith) (Gastropoda) and Sanguinicola sp. Plehn (Trematoda) in Europe. Journal of Zoology, 261, 213–216. https://doi.org/10.1017/S0952836903004084.

    Article  Google Scholar 

  • Gérard, C., Miura, O., Lorda, J., Cribb, T. H., Nolan, M. J., & Hechinger, R. F. (2017). A native-range source for a persistent trematode parasite of the exotic New Zealand mudsnail (Potamopyrgus antipodarum) in France. Hydrobiologia, 785(1), 115–126. https://doi.org/10.1007/s10750-016-2910-8.

    Article  CAS  Google Scholar 

  • Gibson, A. K., Delph, L. F., & Lively, C. M. (2017). The two-fold cost of sex: experimental evidence from a natural system. Evolution Letters, 1(1), 6–15. https://doi.org/10.1002/evl3.1.

    Article  PubMed  PubMed Central  Google Scholar 

  • Goldberg, C. S., Sepulveda, A., Ray, A., Baumgardt, J., & Waits, L. P. (2013). Environmental DNA as a new method for early detection of New Zealand mudsnails (Potamopyrgus antipodarum). Freshwater Science, 32(3), 792–800. https://doi.org/10.1899/13-046.1.

    Article  Google Scholar 

  • Goodfriend, G. a. (1986). Variation in land snail shell form and its causes: a review. Systematic Zoology, 35(2), 204–223.

    Article  Google Scholar 

  • Haase, M. (2003). Clinal variation in shell morphology of the freshwater gastropod Potamopyrgus antipodarum along two hill-country streams in New Zealand. Journal of the Royal Society of New Zealand, 33(2), 549–560.

    Article  Google Scholar 

  • Haase, M. (2008). The radiation of hydrobiid gastropods in New Zealand: a revision including the description of new species based on morphology and mtDNA sequence information. Systematics and Biodiversity, 6(1), 99–159. https://doi.org/10.1017/S1477200007002630.

    Article  Google Scholar 

  • Haase, M., Naser, M. D., & Wilke, T. (2010). Ecrobia grimmi in brackish Lake Sawa, Iraq: indirect evidence for long-distance dispersal of hydrobiid gastropods (Caenogastropoda: Rissooidea) by birds. Journal of Molluscan Studies, 76(1), 101–105. https://doi.org/10.1093/mollus/eyp051.

    Article  Google Scholar 

  • Haase, M., Esch, S., & Misof, B. (2013). Local adaptation, refugial isolation and secondary contact of alpine populations of the land snail Arianta arbustorum. Journal of Molluscan Studies, 79(3), 241–248. https://doi.org/10.1093/mollus/eyt017.

    Article  Google Scholar 

  • Hammer, Ø., Harper, D. A. T., & Ryan, P. D. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1), 9.

    Google Scholar 

  • Hauser, L., Carvalho, G. R., Hughes, R. N., & Carter, R. E. (1992). Clonal structure of the introduced freshwater snail Potamopyrgus antipodarum (Prosobranchia: Hydrobiidae), as revealed by DNA fingerprinting. Proceedings of the Biological Sciences, 249, 19–25.

    Article  CAS  Google Scholar 

  • Hechinger, R. F. (2012). Faunal survey and identification key for the trematodes (Platyhelminthes: Digenea) infecting Potamopyrgus antipodarum (Gastropoda: Hydrobiidae) as first intermediate host. Zootaxa, 27(3418), 1–27.

    Google Scholar 

  • Herbst, D. B., Bogan, M. T., & Lusardi, R. A. (2008). Low specific conductivity limits growth and survival of the New Zealand mud snail from the upper Owens River, California. Western North American Naturalist, 68(3), 324–333. https://doi.org/10.3398/1527-0904(2008)68[324:LSCLGA]2.0.CO;2.

    Article  Google Scholar 

  • Holomuzki, J. R., & Biggs, B. J. F. (1999). Distributional responses to flow disturbance by a stream-dwelling snail. Oikos, 87(1), 36–47.

    Article  Google Scholar 

  • Holomuzki, J. R., & Biggs, B. J. F. (2006). Habitat-specific variation and performance trade-offs in shell armature of New Zealand mudsnails. Ecological Society of America, 87(4), 1038–1047.

    Google Scholar 

  • Hughes, R. N. (1996). Evolutionary ecology of parthenogenetic strains of the prosobranch snail, Potamopyrgus antipodarum (Gray) = P. jenkinsi (Smith). Malacological Review, 28, 101–114.

    Google Scholar 

  • Jacobsen, R., Forbes, V. E., & Skovgaard, O. (1996). Genetic population structure of the prosobranch snail Potamopyrgus antipodarum (gray) in Denmark using PCR-RAPD fingerprints. Proceedings: Biological Sciences, 263, 1065–1070.

    CAS  Google Scholar 

  • Jay, F., Manel, S., Alvarez, N., Durand, E. Y., Thuiller, W., Holderegger, R., Tarbelet, P., & François, O. (2012). Forecasting changes in population genetic structure of alpine plants in response to global warming. Molecular Ecology, 21(10), 2354–2368. https://doi.org/10.1111/j.1365-294X.2012.05541.x.

    Article  PubMed  Google Scholar 

  • Jensen, F. B. (1995). Nitrogen metabolism and excretion. Uptake and effects of nitrite and nitrate in animals. Boca Raton: CRC Press.

    Google Scholar 

  • Jensen, F. B. (2003). Nitrite disrupts multiple physiological functions in aquatic animals. Comparative Biochemistry and Physiology - A Molecular and Integrative. Physiology, 135(1), 9–24. https://doi.org/10.1016/S1095-6433(02)00323-9.

    Article  CAS  Google Scholar 

  • Jerde, C. L., Mahon, A. R., Chadderton, W. L., & Lodge, D. M. (2011). “Sight-unseen” detection of rare aquatic species using environmental DNA. Conservation Letters, 4(2), 150–157. https://doi.org/10.1111/j.1755-263X.2010.00158.x.

    Article  Google Scholar 

  • Johannesson, K., Panova, M., Kemppainen, P., Andre, C., Rolan-Alvarez, E., & Butlin, R. K. (2010). Repeated evolution of reproductive isolation in a marine snail: unveiling mechanisms of speciation. Philosophical Transactions of the Royal Society, B: Biological Sciences, 365(1547), 1735–1747. https://doi.org/10.1098/rstb.2009.0256.

    Article  Google Scholar 

  • Johnson, P. C. D. (2014). Extension of Nakagawa & Schielzeth’s R2GLMM to random slopes models. Methods in Ecology and Evolution, 5(9), 944–946. https://doi.org/10.1111/2041-210X.12225.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jokela, J., Lively, C. M., Dybdahl, M. F., & Fox, J. A. (1997). Evidence for a cost of sex in the freshwater snail Potamopyrgus antipodarum. Ecology, 78(2), 452–460. https://doi.org/10.2307/2266021.

    Article  Google Scholar 

  • Jombart, T. (2008). Adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics, 24(11), 1403–1405. https://doi.org/10.1093/bioinformatics/btn129.

    Article  CAS  PubMed  Google Scholar 

  • Jombart, T., Devillard, & Balloux, S. (2010). Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics, 11(1), 94. https://doi.org/10.1186/1471-2156-11-94.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kalinowski, S. T., Taper, M. L., & Marshall, T. C. (2007). Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology, 16(5), 1099–1106. https://doi.org/10.1111/j.1365-294X.2007.03089.x.

    Article  PubMed  Google Scholar 

  • Karney, C. F. F. (2013). Algorithms for geodesics. Journal of Geodesy, 87, 43–55. https://doi.org/10.1007/s00190-012-0578-z.

    Article  Google Scholar 

  • Karr, J. R., & James, F. C. (1975). Eco-morphological configurations and convergent evolution in species and communities. Ecology and evolution of communities. Cambridge: Harvard University Press.

    Google Scholar 

  • King, K. C., Jokela, J., & Lively, C. M. (2011). Parasites, sex, and clonal diversity in natural snail populations. Evolution, 65(5), 1474–1481. https://doi.org/10.1111/j.1558-5646.2010.01215.x.

    Article  PubMed  Google Scholar 

  • Kingsolver, J. G., & Pfennig, D. W. (2007). Patterns and power of phenotypic selection in nature. BioScience, 57(7), 561–572. https://doi.org/10.1641/B570706.

    Article  Google Scholar 

  • Kistner, E. J., & Dybdahl, M. F. (2013). Adaptive responses and invasion: the role of plasticity and evolution in snail shell morphology. Ecology and Evolution, 3(2), 424–436.

    Article  Google Scholar 

  • Kistner, E. J., & Dybdahl, M. F. (2014). Parallel variation among populations in the shell morphology between sympatric native and invasive aquatic snails. Biological Invasions, 16, 2615–2626. https://doi.org/10.1007/s10530-014-0691-4.

    Article  Google Scholar 

  • Klingenberg, C. P. (2011). MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources, 11(2), 353–357. https://doi.org/10.1111/j.1755-0998.2010.02924.x.

    Article  PubMed  Google Scholar 

  • Klingenberg, C. P. (2016). Size, shape, and form: concepts of allometry in geometric morphometrics. Development Genes and Evolution, 226(3), 113–137. https://doi.org/10.1007/s00427-016-0539-2.

    Article  PubMed  PubMed Central  Google Scholar 

  • Klingenberg, C. P., & Monteiro, L. R. (2005). Distances and directions in multidimensional shape spaces: implications for morphometric applications. Systematic Biology, 54(4), 678–688. https://doi.org/10.1080/10635150590947258.

    Article  PubMed  Google Scholar 

  • Krist, A. C. (2002). Crayfish induce a defensive shell shape in a freshwater snail. Invertebrate Biology, 121(3), 235–242. https://doi.org/10.1111/j.1744-7410.2002.tb00063.x.

    Article  Google Scholar 

  • Lagrue, C., Mcewan, J., Poulin, R., & Keeney, D. B. (2007). Co-occurrences of parasite clones and altered host phenotype in a snail–trematode system. Parasitology, 37, 1459–1467. https://doi.org/10.1016/j.ijpara.2007.04.022.

    Article  Google Scholar 

  • Larkin, K., Tucci, C., & Neiman, M. (2016). Effects of polyploidy and reproductive mode on life history trait expression. Ecology and Evolution, 6(3), 765–778. https://doi.org/10.1002/ece3.1934.

    Article  PubMed  PubMed Central  Google Scholar 

  • Le Pennec, G., Butlin, R. K., Jonsson, P. R., Larsson, A. I., Lindborg, J., Bergström, E., Westram, A. M., & Johannesson, K. (2017). Adaptation to dislodgement risk on waveswept rocky shores in the snail Littorina saxatilis. PLoS One, 12(10), 1–15. https://doi.org/10.1371/journal.pone.0186901.

    Article  CAS  Google Scholar 

  • Leigh, J. W., & Bryant, D. (2015). PopART: full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6(9), 1110–1116.

    Article  Google Scholar 

  • Levri, E. P., Dillard, J., & Martin, T. (2005). Trematode infection correlates with shell shape and defence morphology in a freshwater snail. Parasitology, 130(6), 699–708. https://doi.org/10.1017/S0031182005007286.

    Article  CAS  PubMed  Google Scholar 

  • Levri, E. P., Krist, A. C., Bilka, R., & Dybdahl, M. F. (2014). Phenotypic plasticity of the introduced New Zealand mud snail, Potamopyrgus antipodarum, compared to sympatric native snails. PLoS ONE, 9(4), e93985. https://doi.org/10.1371/journal.pone.0093985.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levri, E. P., Landis, S., Smith, B., Colledge, E., Metz, E., & Li, X. (2017). Variation in predator-induced behavioral changes in introduced and native populations of the invasive New Zealand mud snail (Potamopyrgus antipodarum Gray 1843). Aquatic Invasions, 12, in press, 499–508.

    Article  Google Scholar 

  • Li, W., & Godzik, A. (2006). Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics, 22(13), 1658–1659.

    Article  CAS  Google Scholar 

  • Lively, C. M. (1987). Evidence from a New Zealand snail for the maintenance of sex by parasitism. Nature, 329, 855–857.

    Article  Google Scholar 

  • Lively, C. M. (1992). Parthenogenesis in a fresh-water snail—reproductive assurance versus parasitic release. Evolution, 46(4), 907–913. https://doi.org/10.2307/2409745.

    Article  PubMed  Google Scholar 

  • Losos, J. B. (2009). Lizards in an evolutionary tree: Ecology and adaptive radiation of anoles. University of California Press.

  • Losos, J. B., & Miles, D. B. (1994). Adaptation, constraint, and the comparative method: phylogenetic issues and methods. In Ecological morphology: integrative organismal biology (pp. 60–98). University of Chicago Press.

  • Maynard Smith, J. (1971). The origin and maintenance of sex. In G. C. Williams (Ed.), Group selection. Chicago.

  • Maynard-Smith, J. (1978). The evolution of sex. Cambridge: Cambridge University Press.

    Google Scholar 

  • McKenzie, V. J., Hall, W. E., & Guralnick, R. P. (2013). New Zealand mudsnails (Potamopyrgus antipodarum) in Boulder Creek, Colorado: environmental factors associated with fecundity of a parthenogenic invader. NRC Research Press, 36, 30–36. https://doi.org/10.1139/cjz-2012-0183.

    Article  CAS  Google Scholar 

  • Meirmans, P. G., & Van Tienderen, P. H. (2004). GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Molecular Ecology Notes, 4(4), 792–794. https://doi.org/10.1111/j.1471-8286.2004.00770.x.

    Article  Google Scholar 

  • Monteiro, L. R. (1999). Multivariate regression models and geometric morphometrics: the search for causal factors in the analysis of shape. Systematic Biology, 48(1), 192–199.

    Article  CAS  Google Scholar 

  • Nakagawa, S., & Schielzeth, H. (2013). A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods in Ecology and Evolution, 4(2), 133–142. https://doi.org/10.1111/j.2041-210x.2012.00261.x.

    Article  Google Scholar 

  • Negovetic, S., & Jokela, J. (2001). Life-history variation, phenotypic plasticity and maintenance of subpopulation structure in a freshwater snail. Ecology, 82(10), 2805–2815. https://doi.org/10.1890/0012-9658(2001)082[2805:lhvppa]2.0.co;2.

    Article  Google Scholar 

  • Neiman, M., & Lively, C. M. (2004). Pleistocene glaciation is implicated in the phylogeographical structure of Potamopyrgus antipodarum, a New Zealand snail. Molecular Ecology, 13, 3085–3098.

    Article  CAS  Google Scholar 

  • Neiman, M., Jokela, J., & Lively, C. M. (2005). Variation in asexual lineage age in Potamopyrgus antipodarum, a New Zealand snail. Evolution, 59(9), 1945–1952.

    Article  CAS  Google Scholar 

  • Neiman, M., Paczesniak, D., Soper, D. M., Baldwin, A. T., & Hehman, G. (2011). Wide variation in ploidy level and genome size in a New Zealand freshwater snail with coexisting sexual and asexual lineages. Evolution, 65(11), 3202–3216.

    Article  Google Scholar 

  • Neiman, M., Larkin, K., Thompson, A. R., & Wilton, P. (2012). Male offspring production by asexual Potamopyrgus antipodarum, a New Zealand snail. Heredity, 109(1), 57–62. https://doi.org/10.1038/hdy.2012.13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okajima, R., & Chiba, S. (2011). How does life adapt to a gravitational environment? The outline of the terrestrial gastropod shell. The American Naturalist, 178(6), 801–809. https://doi.org/10.1086/662674.

    Article  PubMed  Google Scholar 

  • Paczesniak, D., Jokela, J., Larkin, K., & Neiman, M. (2013). Discordance between nuclear and mitochondrial genomes in sexual and asexual lineages of the freshwater snail Potamopyrgus antipodarum. Molecular Ecology, 22(18), 4695–4710. https://doi.org/10.1111/mec.12422.

    Article  PubMed  Google Scholar 

  • Parks, D. H., Mankowski, T., Zangooei, S., Porter, M. S., Armanini, D. G., Baird, D. J., Langille, M. G. I., & Beiko, R. G. (2013). GenGIS 2: geospatial analysis of traditional and genetic biodiversity, with new gradient algorithms and an extensible plugin framework. PLoS One, 8(7), e69885. https://doi.org/10.1371/journal.pone.0069885.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips, N. R., & Lambert, D. M. (1989). Genetics of Potamopyrgus antipodarum (Gastropoda: Prosobranchia): evidence for reproductive modes. New Zealand Journal of Zoology, 16(3), 435–445.

    Article  Google Scholar 

  • Ponder, W. F. (1988). Potamopyrgus antipodarum: a molluscan colonizer of Europe and Australia. Journal of Molluscan Studies, 54(3), 271–286.

    Article  Google Scholar 

  • Raffaelli, D. G. (1982). Recent ecological research on some European species of Littorina. Journal of Molluscan Studies, 48(December), 342–354. https://doi.org/10.1093/oxfordjournals.mollus.a065656.

    Article  Google Scholar 

  • Rieseberg, L. H., Widmer, A., Arntz, A. M., & Burke, J. M. (2002). Directional selection is the primary cause of phenotypic diversification. Proceedings of the National Academy of Sciences, 99(19), 12242–12245. https://doi.org/10.1073/pnas.192360899.

    Article  CAS  Google Scholar 

  • Rogstad, S. H., Keane, B., & Beresh, J. (2002). Genetic variation across VNTR loci in central North American Taraxacum surveyed at different spatial scales. Plant Ecology, 161(1), 111–121.

    Article  Google Scholar 

  • Rohlf, F.J. (2010). TpsDig, version 2.16. Department of Ecology and Evolution, State University of New York at Stony Brook, USA, available at: http://life.bio. sunysb.edu/morph/bibr28. Accessed 20/04/2016.

  • Rohlf, F.J. (2012). TpsUtil, file utility program. Version 1.53. Department of Ecology and Evolution, State University of New York at Stony Brook, USA, available at: http://life.bio.sunysb.edu/morph. Accessed 25/04/2016.

  • Rohlf, F. J., & Slice, D. (1990). Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Biology, 39, 40–59.

    Google Scholar 

  • Rosenberg, M. S., & Anderson, C. D. (2011). PASSaGE: pattern analysis, spatial statistics and geographic exegesis. Version 2. Methods in Ecology and Evolution, 2(3), 229–232. https://doi.org/10.1111/j.2041-210X.2010.00081.x.

    Article  Google Scholar 

  • Rousset, F. (2008). GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources, 8(1), 103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x.

    Article  PubMed  Google Scholar 

  • Schindler, D. W., Kling, H., Schmidt, R. V., Prokopowich, J., Frost, V. E., Reid, R. A., & Capel, M. (1973). Eutrophication of Lake 227 by addition of phosphate and nitrate: the second, third, and fourth years of enrichment, 1970, 1971, and 1972. Journal of the Fisheries Board of Canada, 30(10), 1415–1440.

    Article  CAS  Google Scholar 

  • Schreiber, E. S. G., Glaister, A., Quinn, G. P., & Lake, P. S. (1998). Life history and population dynamics of the exotic snail Potamopyrgus antipodarum (Prosobranchia: Hydrobiidae) in Lake Purrumbete, Victoria, Australia. Marine and Freshwater Research, 49, 73–78.

    Article  Google Scholar 

  • Schwarz, G. (1978). Estimating the dimension of a model. The Annals of Statistics, 6(2), 461–464. https://doi.org/10.1214/aos/1176344136.

    Article  Google Scholar 

  • Seeley, R. H. (1986). Intense natural selection caused a rapid morphological transition in a living marine snail. Proceedings of the National Academy of Sciences of the United States of America, 83(18), 6897–6901. https://doi.org/10.1073/pnas.83.18.6897.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimada, K., & Urabe, M. (2003). Comparative ecology of the alien freshwater snail Potamopyrgus antipodarum and the indigenous snail Semisulcospira spp. Venus, 62, 39–53.

    Google Scholar 

  • Slatkin, M. (1995). A measure of population subdivision based on microsatellite allele frequencies. Genetics, 139(1), 457–462.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Soper, D. M., Neiman, M., Savytskyy, O. P., Zolan, M. E., & Lively, C. M. (2013). Spermatozoa production by triploid males in the New Zealand freshwater snail Potamopyrgus antipodarum. Biological Journal of the Linnean Society, 110(1), 1–10. https://doi.org/10.1038/jid.2014.371.

    Article  CAS  Google Scholar 

  • Soper, D. M., Hatcher, K. M., & Neiman, M. (2016). Documentation of copulatory behaviour in triploid male freshwater snails. Ethology Ecology and Evolution, 28(1), 110–116. https://doi.org/10.1080/03949370.2015.1030781.

    Article  Google Scholar 

  • Städler, T., Frye, M., Neiman, M., & Lively, C. M. (2005). Mitochondrial haplotypes and the New Zealand origin of clonal European Potamopyrgus, an invasive aquatic snail. Molecular Ecology, 14, 2465–2473.

    Article  Google Scholar 

  • Stankowski, S. (2011). Extreme, continuous variation in an island snail: local diversification and association of shell form with the current environment. Biological Journal of the Linnean Society, 104(4), 756–769. https://doi.org/10.1111/j.1095-8312.2011.01748.x.

    Article  Google Scholar 

  • Stankowski, S. (2013). Ecological speciation in an island snail: evidence for the parallel evolution of a novel ecotype and maintenance by ecologically dependent postzygotic isolation. Molecular Ecology, 22(10), 2726–2741. https://doi.org/10.1111/mec.12287.

    Article  CAS  PubMed  Google Scholar 

  • Statzner, B., & Holm, T. F. (1989). Morphological adaptation of shape to flow: microcurrents around lotic macroinvertebrates with known Reynolds numbers at quasi-natural flow conditions. Oecologia, 78(2), 145–157. https://doi.org/10.1007/BF00377150.

    Article  CAS  PubMed  Google Scholar 

  • Stumm, W., & Morgan, J. J. (1996). Aquatic chemistry (3rd ed.). New York: Wiley.

    Google Scholar 

  • Vergara, D., Fuentes, J. A., Stoy, K. S., & Lively, C. M. (2016). Evaluating shell variation across different populations of a freshwater snail. Molluscan Research, 5818, 1–13. https://doi.org/10.1080/13235818.2016.1253446.

    Article  Google Scholar 

  • Verhaegen, G., McElroy, K. E., Bankers, L. A., Neiman, N., & Haase, M. (2018). Adaptive phenotypic plasticity in a clonal invader. Ecology and Evolution, 8, 4465–4483. https://doi.org/10.1002/ece3.4009.

    Article  Google Scholar 

  • Vermeij, G. J. (1995). A natural history of shells. Princeton University Press.

  • Vogel, S. (1994). Life in moving fluids: the physical biology of flow. New Jersey: Princeton University Press.

    Google Scholar 

  • Vonesh, E. F., Chinchilli, V. M., & Pu, K. (1996). Goodness-of-fit in generalized nonlinear mixed-effects models. Biometrics, 52(2), 572–587.

    Article  CAS  Google Scholar 

  • Vrijenhoek, R. C. (1979). Factors affecting clonal diversity and coexistence. Integrative and Comparative Biology, 19(3), 787–797. https://doi.org/10.1093/icb/19.3.787.

    Article  Google Scholar 

  • Warwick, T. (1952). Strains in the mollusc Potamopyrgus jenkinsi (Smith). Nature, 169(4300), 551–552.

    Article  CAS  Google Scholar 

  • Weetman, D., Hauser, L., & Carvalho, G. R. (2002). Reconstruction of microsatellite mutation history reveals a strong and consistent deletion bias in invasive clonal snails, Potamopyrgus antipodarum. Genetics Society of America, 162, 813–822.

    CAS  Google Scholar 

  • Weissenberger, J., Emanns, H. S. A., & Schwoerbelt, J. (1991). Measurement of lift and drag forces in the mN range experienced by benthic arthropods at flow velocities below 1.2 m s −1. Freshwater Biology, 25, 21–31. https://doi.org/10.1111/j.1365-2427.1991.tb00469.x.

    Article  Google Scholar 

  • Williams, E. E. (1972). The origin of faunas. Evolution of lizard congeners in a complex island fauna: a trial analysis. In Evolutionary biology (pp. 47–89). New York: Springer.

    Chapter  Google Scholar 

  • Winterbourn, M. J. (1970). Population studies on the New Zealand freshwater gastropod Potamopyrgus antipodarum (Gray). Journal of Molluscan Studies, 39(2–3), 139–149.

    Article  Google Scholar 

  • Winterbourn, M. J. (1974). Larval Trematoda parasitizing the New Zealand species of Potamopyrgus (Gastropoda: Hydrobiidae). Mauri Ora, 2, 17–30.

    Google Scholar 

  • Zbikowski, J., & Zbikowska, E. (2009). Invaders of an invader—trematodes in Potamopyrgus antipodarum in Poland. Journal of Invertebrate Pathology, 101(1), 67–70. https://doi.org/10.1016/j.jip.2009.02.005.

    Article  PubMed  Google Scholar 

  • Zelditch, M. L., Swiderski, D. L., & Sheets, H. D. (2012). Geometric morphometrics for biologists: A primer. Academic Press.

  • Zielske, S., Ponder, W. F., & Haase, M. (2017). The enigmatic pattern of long-distance dispersal of minute freshwater gastropods (Caenogastropoda, Truncatelloidea, Tateidae) across the South Pacific. Journal of Biogeography, 44(1), 195–206. https://doi.org/10.1111/jbi.12800.

    Article  Google Scholar 

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Acknowledgements

We thank K. Collier and I. D. Hogg from The University of Waikato/Hamilton/New Zealand for providing logistic support and help with fieldwork. S. Fregin is acknowledged for her assistance in the lab. We are grateful to S. Puechmaille for population genetic advice. G. Uhl is thanked for providing access to the Zeiss microscope. We also thank two anonymous reviewers for their constructive comments on the previous manuscript. This study was part of the Research Training Group 2010 RESPONSE funded by the Deutsche Forschungsgemeinschaft (DFG).

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Verhaegen, G., Neiman, M. & Haase, M. Ecomorphology of a generalist freshwater gastropod: complex relations of shell morphology, habitat, and fecundity. Org Divers Evol 18, 425–441 (2018). https://doi.org/10.1007/s13127-018-0377-3

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