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Invasion at the population level: a story of the freshwater snails Gyraulus parvus and G. laevis

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Abstract

Biological invasions are common among freshwater molluscs, with the North American planorbid gastropod Gyraulus parvus being reported from Europe (Germany) by the 1970s. It has since spread across Central and Western Europe, mostly living in artificial and highly modified habitats. However, considerable conchological and anatomical similarity exists between it and the native European G. laevis. Using four other European and one North American Gyraulus species as outgroups, separate phylogenetic analyses using mitochondrial and nuclear DNA sequences show that G. parvus and G. laevis are in fact part of the same species-level clade, with the former having nomenclatural priority. However, the structure within the mitochondrial tree suggests a North American origin of the invasive populations. It also makes it possible to track down the distribution of both races. Although native and non-native races in Europe tend to possess some differences in conchology and ecology, the degree of overlap makes it impossible to accurately distinguish between them without the DNA barcode data. Our results change the outlook on the conservation of the rare native race. While interspecific competition among snail species is rare, invasion on an intraspecific level may represent a serious threat for native populations.

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References

  • Alder, J., 1838. Supplement to a catalogue of the land and fresh-water testaceous Mollusca, found in the vicinity of Newcastle. Transactions of the Natural History Society of Northumberland, Durham, and Newcastle upon Tyne 2: 337–342.

    Google Scholar 

  • Armbruster, G. F., & D. Bernhard, 2000. Taxonomic significance of ribosomal ITS‐1 sequence markers in self‐fertilizing land snails of Cochlicopa (Stylommatophora, Cochlicopidae). Zoosystematics and Evolution 76: 11–18.

    Article  Google Scholar 

  • Beran, L., & M. Horsák, 2002. Gyraulus parvus (Mollusca: Gastropoda) in the Czech Republic. Acta Societatis Zoologicae Bohemicae 66: 81–84.

    Google Scholar 

  • Boschi, C., & R. Heim, 2011. Die Schneckenfauna der Schweiz: ein umfassendes Bild- und Bestimmungsbuch. Haupt Verlag, Bern.

    Google Scholar 

  • Burch, J. B., 1982. North American freshwater snails: identification keys, generic synonymy, supplemental notes, glossary, references, index. Society for Experimental and Descriptive Malacology.

  • Clarke, A. H., 1981. The freshwater molluscs of Canada. National Museum of Natural Sciences, National Museums of Canada, Ottawa.

  • Clewing, C., F. Riedel, T. Wilke, & C. Albrecht, 2015. Ecophenotypic plasticity leads to extraordinary gastropod shells found on the “Roof of the World.” Ecology and Evolution 5: 2966–2979.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cope, N. J., & M. J. Winterbourn, 2004. Competitive interactions between two successful molluscan invaders of freshwaters: an experimental study. Aquatic Ecology 38: 83–91.

    Article  Google Scholar 

  • Darriba, D., G. L. Taboada, R. Doallo, & D. Posada, 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772–772.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dillon, R. T., 2000. The ecology of freshwater molluscs. Cambridge University Press, New York.

    Book  Google Scholar 

  • Drummond, A. J., & A. Rambaut, 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Duras, J., 2014. Limnolog a cerkárie. Limnologické noviny 4: 6–12.

    Google Scholar 

  • Falkner, G., T. E. Ripken, M. Falkner, P. Charles-Dominique, & P. Bouchet, 2002. Mollusques continentaux de France (liste de référence annotée et bibliographie). Collection Patrimoines Naturels. Muséum national d’Histoire naturelle, Paris.

    Google Scholar 

  • Fehér, Z., G. Majoros, & A. Varga, 2004. A scoring method for the assessment of rarity and conservation value of the Hungarian freshwater molluscs. Heldia 6: 127–140.

    Google Scholar 

  • Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.

    Article  PubMed  Google Scholar 

  • Genner, M. J., E. Michel, D. Erpenbeck, N. D. Voogd, F. Witte, & J.-P. Pointier, 2004. Camouflaged invasion of Lake Malawi by an Oriental gastropod. Molecular Ecology 13: 2135–2141.

    Article  CAS  PubMed  Google Scholar 

  • Gittenberger, E., W. H. Piel, & D. S. J. Groenenberg, 2004a. The Pleistocene glaciations and the evolutionary history of the polytypic snail species Arianta arbustorum (Gastropoda, Pulmonata, Helicidae). Molecular Phylogenetics and Evolution 30: 64–73.

    Article  CAS  PubMed  Google Scholar 

  • Gittenberger, E., A. W. Janssen, W. J. Kuijper, J. G. J. Kuiper, T. Meijer, G. van der Velde, J. N. de Vries, & G. A. Peeters, 2004b. De Nederlandse Zoetwatermollusken. Recente en fossiele weekdieren uit zoet en brak water. Nederlandse Fauna 2. Nationaal Natuurhistorisch Museum Naturalis, KNNV Uitgeverij & European Invertebrate Survey Nederland, Utrecht.

  • Glöer, P., 2019. The Freshwater Gastropods of the West-Palaearctis: Identification Key, Anatomy, Ecology, Distribution. Biodiversity Research Lab, Hetlingen.

  • Glöer, P., & C. Meier-Brook, 1998. Süsswassermollusken: Ein Bestimmungsschlüssel für die Bundesrepublik Deutschland. Deutscher Jugendbund für Naturbeobachtung, Hamburg.

  • Goloboff, P. A., J. S. Farris, & K. C. Nixon, 2008. TNT, a free program for phylogenetic analysis. Cladistics 24: 774–786.

    Article  Google Scholar 

  • Haase, M., B. Misof, T. Wirth, H. Baminger, & B. Baur, 2003. Mitochondrial differentiation in a polymorphic land snail: evidence for Pleistocene survival within the boundaries of permafrost. Journal of Evolutionary Biology 16: 415–428.

    Article  CAS  PubMed  Google Scholar 

  • Horsák, M., L. Juřičková, & J. Picka, 2013. Molluscs of the Czech and Slovak Republics. Kabourek, Zlín.

  • Horsák, M., M. Chytrý, P. Hájková, M. Hájek, J. Danihelka, V. Horsáková, N. Ermakov, D. A. German, M. Kočí, P. Lustyk, J. C. Nekola, Z. Preislerová, & M. Valachovič, 2015. European glacial relict snails and plants: environmental context of their modern refugial occurrence in southern Siberia. Boreas 44: 638–657.

    Article  Google Scholar 

  • Hošek, J., L. Lisá, U. Hambach, L. Petr, L. Vejrostová, A. Bajer, T. M. Grygar, P. Moska, Z. Gottvald, & M. Horsák, 2017. Middle Pleniglacial pedogenesis on the northwestern edge of the Carpathian basin: a multidisciplinary investigation of the Bíňa pedo-sedimentary section, SW Slovakia. Palaeogeography, Palaeoclimatology, Palaeoecology 487: 321–339.

    Article  Google Scholar 

  • Huelsenbeck, J. P., & F. Ronquist, 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.

    Article  CAS  PubMed  Google Scholar 

  • Hughes, S. J., 1995. Notes on freshwater mollusca of Madeira including records of species new to the region. Boletim do Museu Municipal do Funchal 47(259): 23–37.

    Google Scholar 

  • Jansen, B. 2015. Veldgids Slakken en mossels. KNNV Uitgeverij, Zeist.

    Google Scholar 

  • Jung, Y., & J. B. Burch, 1991. A taxonomic review of the Gyraulus subgenus Torquis. Walkerana 5: 1–18.

    Google Scholar 

  • Kappes, H., & P. Haase, 2012. Slow, but steady: dispersal of freshwater molluscs. Aquatic Sciences 74: 1–14.

    Article  Google Scholar 

  • Katoh, K., J. Rozewicki, & K. D. Yamada, 2019. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20: 1160–1166.

    Article  CAS  PubMed  Google Scholar 

  • Kerney, M. P., 1999. Atlas of the land and freshwater molluscs of Britain and Ireland. Harley Books, Colchester, Essex.

    Google Scholar 

  • Kühn, A. L., & M. Haase, 2020. QUIDDICH: QUick IDentification of DIagnostic CHaracters. Journal of Zoological Systematics and Evolutionary Research 58: 22–26.

    Article  Google Scholar 

  • Kuraku, S., C. M. Zmasek, O. Nishimura, & K. Katoh, 2013. aLeaves facilitates on-demand exploration of metazoan gene family trees on MAFFT sequence alignment server with enhanced interactivity. Nucleic Acids Research 41: W22–W28.

    Article  PubMed  PubMed Central  Google Scholar 

  • Laman, T. G., D. L. Daniell, & H. D. Blankespoor, 1984. The role of Gyraulus parvus as an intermediate host for avian Schistosomes. Proceedings of the Helminthological society of Washington, 51(2): 267–269.

    Google Scholar 

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

    Article  Google Scholar 

  • Leighton, B. J., S. Zervos, & J. M. Webster, 2000. Ecological factors in schistosome transmission, and an environmentally benign method for controlling snails in a recreational lake with a record of schistosome dermatitis. Parasitology International 49: 9–17.

    Article  CAS  PubMed  Google Scholar 

  • Letunic, I., & P. Bork, 2019. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Research 47: W256–W259.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leuven, R. S. E. W., G. van der Velde, I. Baijens, J. Snijders, C. van der Zwart, H. J. R. Lenders, & A. bij de Vaate, 2009. The river Rhine: a global highway for dispersal of aquatic invasive species. Biological Invasions 11: 1989–2008.

    Article  Google Scholar 

  • Lorencová, E., L. Beran, V. Horsáková, & M. Horsák, 2015. Invasion of freshwater molluscs in the Czech Republic: Time course and environmental predictors. Malacologia 59: 105–120.

    Article  Google Scholar 

  • Ložek, V., 1964. Quartärmollusken der Tschechoslowakei. Nakladatelství Československé akademie věd, Praha.

  • Mack, R. N., D. Simberloff, W. M. Lonsdale, H. Evans, M. Clout, & F. A. Bazzaz, 2000. Biotic invasions: Causes, epidemiology, global consequences, and control. Ecological Applications 10: 689–710.

    Article  Google Scholar 

  • Meier-Brook, C., 1983. Taxonomic studies on Gyraulus (Gastropoda: Planorbidae). Malacologia 24: 1–113.

    Google Scholar 

  • Meier-Brook, C., 1984. A preliminary biogeography of freshwater pulmonate gastropods. In Solem, A., & A. C. van Bruggen (eds), World-wide snails: biogeographical studies on non-marine Mollusca. E.J. Brill/W. Backhuys, Leiden: 23–37.

    Google Scholar 

  • Meier-Brook, C., 2002. What makes an aquatic ecosystem susceptible to mollusc invasions. ConchBooks, Hackeinheim, Collectanea Malacologica 405–417.

  • Meyerson, L. A., & J. T. Cronin, 2013. Evidence for multiple introductions of Phragmites australis to North America: detection of a new non-native haplotype. Biological Invasions 15: 2605–2608.

    Article  Google Scholar 

  • Nekola, J. C., S. Chiba, B. F. Coles, C. A. Drost, T. von Proschwitz, & M. Horsák, 2018. A phylogenetic overview of the genus Vertigo O. F. Müller, 1773 (Gastropoda: Pulmonata: Pupillidae: Vertigininae). Malacologia 62: 21–161.

    Article  Google Scholar 

  • Obwaller, A., H. Sattmann, R. Konecny, C. Hörweg, H. Auer, & H. Aspöck, 2001. Cercarial dermatitis in Austria: the recent situation and future aspects. Helminthologia 38: 245.

    Google Scholar 

  • Patzner, R., 1997. Gyraulus parvus (Say 1817) in the country of Salzburg (Austria). Heldia 151.

  • Raw, J. L., N. A. F. Miranda, & R. Perissinotto, 2013. Chemical cues released by an alien invasive aquatic gastropod drive its invasion success. PLoS ONE 8: e64071.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richards, D. C., L. D. Cazier, G. T. Lester, 2001. Spatial distribution of three snail species, including the invader Potamopyrgus antipodarum, in a freshwater spring. Western North American Naturalist 61: 375–380.

    Google Scholar 

  • Roman, J., 2006. Diluting the founder effect: cryptic invasions expand a marine invader’s range. Proceedings of the Royal Society B: Biological Sciences 273: 2453–2459.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rowson, B., H. A. Powell, M. J. Willing, M. Dobson, & H. Shaw, 2021. Freshwater snails of Britain and Ireland. Field Studies Council, Shropshire.

  • Saltonstall, K., 2002. Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proceedings of the National Academy of Sciences 99: 2445–2449.

    Article  CAS  Google Scholar 

  • Schierenbeck, K. A., & N. C. Ellstrand, 2009. Hybridization and the evolution of invasiveness in plants and other organisms. Biological Invasions 11: 1093–1105.

    Article  Google Scholar 

  • Stamatakis, A., 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura, K., G. Stecher, D. Peterson, A. Filipski, & S. Kumar, 2013. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution 30: 2725–2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor, D. W., 1966. Summary of North American Blancan nonmarine mollusks. Malacologia 4: 1–172.

    Google Scholar 

  • Van Leeuwen, C. H. A., G. Van Der Velde, B. Van Lith, & M. Klaassen, 2012. Experimental quantification of long distance dispersal potential of aquatic snails in the gut of migratory birds. PLoS ONE 7: e32292.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van Leeuwen, C. H. A., N. Huig, G. Van Der Velde, T. A. Van Alen, C. A. M. Wagemaker, C. D. H. Sherman, M. Klaassen, & J. Figuerola, 2013. How did this snail get here? Several dispersal vectors inferred for an aquatic invasive species: Dispersal of aquatic snails by several vectors. Freshwater Biology 58: 88–99.

    Article  Google Scholar 

  • Ville, S. P., 1988. Shipping in the Port of Newcastle, 1780–1800. The Journal of Transport History SAGE Publications Ltd 9: 60–77.

    Article  Google Scholar 

  • Wade, C. M., & P. B. Mordan, 2000. Evolution within the gastropod molluscs; using the ribosomal RNA gene-cluster as an indicator of phylogenetic relationships. Journal of Molluscan Studies 66: 565–569.

    Article  Google Scholar 

  • Williamson, M., 1999. Invasions. Ecography 22: 5–12.

    Article  Google Scholar 

  • Yu, Z., 2000. Ecosystem response to Lateglacial and early Holocene climate oscillations in the Great Lakes region of North America. Quaternary Science Reviews 19: 1723–1747.

    Article  Google Scholar 

  • Zhadin, V. I., 1952. Mollyuski presnykh i solonovatykh vod SSSR (Mollusks of Fresh and Brackish Waters of the USSR). Akademiya nauk SSSR, Moscow.

    Google Scholar 

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Acknowledgements

We are grateful to Coen M. Adema (University of New Mexico) and Robert T. Dillon, Jr. (Freshwater Gastropods of North America Project) for providing samples from North America.

Funding

The study was primarily founded by the Czech Science Foundation (20-18827S). The sequencing of UK samples was funded by the National Lottery Heritage Fund; JCH was supported by the Research Plan of the National Museum Prague (No. DKRVO 2019–2023/6.II.c, 00023272).

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Authors and Affiliations

  1. Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 61137, Brno, Czech Republic

    Erika Lorencová, Markéta Nováková, Veronika Horsáková, Jeffrey C. Nekola & Michal Horsák

  2. Nature Conservation Agency of the Czech Republic, Regional Office Kokořínsko – Máchův kraj Protected Landscape Area Administration, Mělník, Czech Republic

    Luboš Beran

  3. Department of Natural Sciences, National Museum of Wales, Cardiff, UK

    Ben Rowson

  4. Department of Zoology, National Museum Prague, Praha, Czech Republic

    Jaroslav Č. Hlaváč

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  1. Erika Lorencová
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  2. Luboš Beran
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  3. Markéta Nováková
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  4. Veronika Horsáková
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  5. Ben Rowson
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  6. Jaroslav Č. Hlaváč
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  7. Jeffrey C. Nekola
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  8. Michal Horsák
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Contributions

EL, VH, JCN and MH contributed to the conception and design of the study. Material preparation and data collection were performed by all authors. VH, MN and EL ran the analyses. The first draft of the manuscript was written by EL and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Erika Lorencová.

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Lorencová, E., Beran, L., Nováková, M. et al. Invasion at the population level: a story of the freshwater snails Gyraulus parvus and G. laevis. Hydrobiologia 848, 4661–4671 (2021). https://doi.org/10.1007/s10750-021-04668-w

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