Understanding the invasive potential of species outside their native range is one of the most pressing questions in applied evolutionary and ecological research. Admixture of genotypes of invasive species from multiple sources has been implicated in successful invasions, by generating novel genetic combinations that facilitate rapid adaptation to new environments. Alternatively, adaptive evolution on standing genetic variation, exposed by phenotypic plasticity and selected by genetic accommodation, can facilitate invasion success. We investigated the population genetic structure of an Asian freshwater mussel with a parasitic dispersal stage, Sinanodonta woodiana, which has been present in Europe since 1979 but which has expanded rapidly in the last decade. Data from a mitochondrial marker and nuclear microsatellites have suggested that all European populations of S. woodiana originate from the River Yangtze basin in China. Only a single haplotype was detected in Europe, in contrast to substantial mitochondrial diversity in native Asian populations. Analysis of microsatellite markers indicated intensive gene flow and confirmed a lower genetic diversity of European populations compared to those from the Yangtze basin, though that difference was not large. Using an Approximate Bayesian Modelling approach, we identified two areas as the probable source of the spread of S. woodiana in Europe, which matched historical records for its establishment. Their populations originated from a single colonization event. Our data do not support alternative explanations for the rapid recent spread of S. woodiana; recent arrival of a novel (cold-tolerant) genotype or continuous propagule pressure. Instead, in situ adaptation, facilitated by repeated admixture, appears to drive the ongoing expansion of S. woodiana. We discuss management consequences of our results.

Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic

Department of Ecology and Vertebrate Zoology University of Łódź Łódź Poland

Department of Zoology and Fisheries Czech University of Life Sciences Prague Czech Republic

Grigore Antipa National Museum of Natural History Bucharest Romania

School of Biology and Bell Pettigrew Museum of Natural History University of St Andrews St Andrews UK

The Czech Academy of Sciences Institute of Vertebrate Biology Brno Czech Republic

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Adam, B. (2010). L'Anodonte chinoise

Anderson, L. G. , White, P. C. L. , Stebbing, P. D. , Stentiford, G. D. , & Dunn, A. M. (2014). Biosecurity and vector behaviour: Evaluating the potential threat posed by anglers and canoeists as pathways for the spread of invasive non‐native species and pathogens. PLoS ONE, 9, e92788 10.1371/journal.pone.0092788 PubMed DOI PMC

Bandelt, H.‐J. , Forster, P. , & Röhl, A. (1999). Median‐joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48. 10.1093/oxfordjournals.molbev.a026036 PubMed DOI

Beaumont, M. A. , Zhang, W. Y. , & Balding, D. J. (2002). Approximate Bayesian computation in population genetics. Genetics, 162, 2025–2035. PubMed PMC

Belkhir, K. , Borsa, P. , Chikhi, L. , Raufaste, N. , & Bonhomme, F. (1996‐2004). GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier (France).

Berg, D. J. , Haag, W. R. , Guttman, S. I. , & Sickel, J. B. (1995). Mantle biopsy: A technique for nondestructive tissue‐sampling of freshwater mussels. Journal of the North American Benthological Society, 14, 577–581. 10.2307/1467542 DOI

Bespalaya, Y. V. , Bolotov, I. N. , Aksenova, O. V. , Gofarov, M. Y. , Kondakov, A. V. , Vikhrev, I. V. , & Vinarski, M. V. (2017). DNA barcoding reveals invasion of two cryptic DOI

Blackburn, T. M. , Essl, F. , Evans, T. , Hulme, P. E. , Jeschke, J. M. , Kühn, I. , … Pergl, J. (2014). A unified classification of alien species based on the magnitude of their environmental impacts. PLoS Biology, 12, e1001850 10.1371/journal.pbio.1001850 PubMed DOI PMC

Bock, D. G. , Caseys, C. , Cousens, R. D. , Hahn, M. A. , Heredia, S. M. , Hübner, S. , … Rieseberg, L. H. (2015). What we still don't know about invasion genetics. Molecular Ecology, 24, 2277–2297. 10.1111/mec.13032 PubMed DOI

Bock, D. G. , Kantar, M. B. , Caseys, C. , Matthey‐Doret, R. , & Rieseberg, L. H. (2018). Evolution of invasiveness by genetic accommodation. Nature Ecology & Evolution, 2, 991 10.1038/s41559-018-0553-z PubMed DOI

Bogan, A. E. , Bowers‐Altman, J. , & Raley, M. E. (2011). A new threat to conservation of North American freshwater mussels: Chinese Pond Mussel (Sinanodonta woodiana) in the United States. Tentacle, 19, 39‐40.

Bolotov, I. N. , Bespalaya, Y. V. , Gofarov, M. Y. , Kondakov, A. V. , Konopleva, E. S. , & Vikhrev, I. V. (2016). Spreading of the Chinese pond mussel, DOI

Chapman, D. C. , Davis, J. J. , Jenkins, J. A. , Kocovsky, P. M. , Miner, J. G. , Farver, J. , & Jackson, P. R. (2013). First evidence of grass carp recruitment in the Great Lakes Basin. Journal of Great Lakes Research, 39, 547–554. 10.1016/j.jglr.2013.09.019 DOI

Chapuis, M.‐P. , & Estoup, A. (2007). Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution, 24, 621–631. 10.1093/molbev/msl191 PubMed DOI

Chen, X. , Liu, H. , Su, Y. , & Yang, J. (2015). Morphological development and growth of the freshwater mussel DOI

Cornuet, J.‐M. , Pudlo, P. , Veyssier, J. , Dehne‐Garcia, A. , Gautier, M. , Leblois, R. , … Estoup, A. (2014). DIYABC v2.0: A software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics, 30, 1187–1189. 10.1093/bioinformatics/btt763 PubMed DOI

Cornuet, J.‐M. , Ravigne, V. , & Estoup, A. (2010). Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0). BMC Bioinformatics, 11, 401 10.1186/1471-2105-11-401 PubMed DOI PMC

Cornuet, J.‐M. , Santos, F. , Beaumont, M. A. , Robert, C. P. , Marin, J.‐M. , Balding, D. J. , … Estoup, A. (2008). Inferring population history with DIY ABC: A user‐friendly approach to approximate Bayesian computation. Bioinformatics, 24, 2713–2719. 10.1093/bioinformatics/btn514 PubMed DOI PMC

Donrovich, S. W. , Douda, K. , Plechingerová, V. , Rylková, K. , Horký, P. , Slavík, O. , … Sousa, R. (2017). Invasive Chinese pond mussel DOI

Douda, K. , & Čadková, Z. (2017). Water clearance efficiency indicates potential filter‐feeding interactions between invasive

Douda, K. , Liu, H.‐Z. , Yu, D. , Rouchet, R. , Liu, F. , Tang, Q.‐Y. , … Reichard, M. (2017). The role of local adaptation in shaping fish‐mussel coevolution. Freshwater Biology, 62, 1858–1868.

Douda, K. , Vrtílek, M. , Slavík, O. , & Reichard, M. (2012). The role of host specificity in explaining the invasion success of the freshwater mussel DOI

Dudgeon, D. , & Morton, B. (1984). Site selection and attachment duration of DOI

Estoup, A. , & Guillemaud, T. (2010). Reconstructing routes of invasion using genetic data: Why, how and so what? Molecular Ecology, 19, 4113–4130. 10.1111/j.1365-294X.2010.04773.x PubMed DOI

Estoup, A. , Jarne, P. , & Cornuet, J. M. (2002). Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Molecular Ecology, 11, 1591–1604. 10.1046/j.1365-294X.2002.01576.x PubMed DOI

Estoup, A. , Lombaert, E. , Marin, J.‐M. , Guillemaud, T. , Pudlo, P. , Robert, C. P. , & Cornuet, J.‐M. (2012). Estimation of demo‐genetic model probabilities with Approximate Bayesian Computation using linear discriminant analysis on summary statistics. Molecular Ecology Resources, 12, 846–855. 10.1111/j.1755-0998.2012.03153.x PubMed DOI

Falush, D. , Stephens, M. , & Pritchard, J. K. (2003). Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics, 164, 1567–1587. PubMed PMC

Galbraith, H. S. , & Vaughn, C. C. (2009). Temperature and food interact to influence gamete development in freshwater mussels. Hydrobiologia, 636, 35–47. 10.1007/s10750-009-9933-3 DOI

Goudet, J. (2001). FSTAT, a programme to estimate and test gene diversities and fixation indices (version 2.9.3). Retrieved from https://www2.unil.ch/popgen/softwares/fstat.htm

Guarneri, I. , Popa, O. P. , Gola, L. , Kamburska, L. , Lauceri, R. , Lopes‐Lima, M. , … Riccardi, N. (2014). A morphometric and genetic comparison of DOI

He, J. , & Zhang, Z. M. (2013). The freshwater bivalves of China. Germany: ConchBooks.

Hubisz, M. J. , Falush, D. , Stephens, M. , & Pritchard, J. K. (2009). Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources, 9, 1322–1332. 10.1111/j.1755-0998.2009.02591.x PubMed DOI PMC

Janáč, M. , Valová, Z. , Roche, K. , & Jurajda, P. (2016). No effect of round goby

Kamburska, L. , Lauceri, R. , & Riccardi, N. (2013). Establishment of a new alien species in Lake Maggiore (Northern Italy): DOI

Kim, B.‐H. , Lee, J.‐H. , & Hwang, S.‐J. (2011). Inter‐and intra‐specific differences in filtering activities between two unionids, DOI

Konečný, A. , Estoup, A. , Duplantier, J.‐M. , Bryja, J. , Ba, K. , Galan, M. , … Cosson, J.‐F. (2013). Invasion genetics of the introduced black rat ( PubMed

Kopelman, N. M. , Mayzel, J. , Jakobsson, M. , Rosenberg, N. A. , & Mayrose, I. (2015). Clumpak: A program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources, 15, 1179–1191. 10.1111/1755-0998.12387 PubMed DOI PMC

Kraszewski, A. (2007). The continuing expansion of

Kraszewski, A. , & Zdanowski, B. (2001). The distribution and abundance of the Chinese mussel

Kraszewski, A. , & Zdanowski, B. (2007).

Lajtner, J. , & Crnčan, P. (2011). Distribution of the invasive bivalve DOI

Lallias, D. , Boudry, P. , Batista, F. M. , Beaumont, A. , King, J. W. , Turner, J. R. , & Lapègue, S. (2015). Invasion genetics of the Pacific oyster DOI

Li, Y. , Yang, H. , Liu, N. , Luo, J. , Wang, Q. , & Wang, L. (2015). Cadmium accumulation and metallothionein biosynthesis in cadmium‐treated freshwater mussel PubMed DOI PMC

Librado, P. , & Rozas, J. (2009). DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452. 10.1093/bioinformatics/btp187 PubMed DOI

Litvak, M. K. , & Mandrak, N. E. (1999). Baitfish trade as a vector of aquatic introductions In Claudi R., & Leach J. H. (Eds.), Nonindigenous freshwater organisms: Vectors, biology, and impacts (pp. 163–180). Boca Raton, FL: Lewis Publishers.

Lockwood, J. L. , Hoopes, M. F. , & Marchetti, M. P. (2013). Invasion ecology, 2nd ed. West Sussex, UK: Wiley‐Blackwell.

Lombaert, E. , Guillemaud, T. , Lundgren, J. , Koch, R. , Facon, B. , Grez, A. , … Estoup, A. (2014). Complementarity of statistical treatments to reconstruct worldwide routes of invasion: The case of the Asian ladybird PubMed DOI

Lopes‐Lima, M. , Sousa, R. , Geist, J. , Aldridge, D. C. , Araujo, R. , Bergengren, J. , … Zogaris, S. (2017). Conservation status of freshwater mussels in Europe: State of the art and future challenges. Biological Reviews, 92, 572–607. 10.1111/brv.12244 PubMed DOI

Miller, N. , Estoup, A. , Toepfer, S. , Bourguet, D. , Lapchin, L. , Derridj, S. , … Guillemaud, T. (2005). Multiple transatlantic introductions of the western corn rootworm. Science, 310, 992 10.1126/science.1115871 PubMed DOI

Modesto, V. , Ilarri, M. , Souza, A. T. , Lopes‐Lima, M. , Douda, K. , Clavero, M. , & Sousa, R. (2017). Fish and mussels: Importance of fish for freshwater mussel conservation. Fish and Fisheries, 19, 244–259. 10.1111/faf.12252, in press. DOI

Morais, P. , & Reichard, M. (2018). Cryptic invasions: A review. Science of the Total Environment, 613, 1438–1448. 10.1016/j.scitotenv.2017.06.133 PubMed DOI

Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89, 583–590. PubMed PMC

Nei, M. (1987). Molecular evolutionary genetics. New York, NY: Columbia University Press.

Nentwig, W. (2009). Handbook of alien species in Europe, Vol. 3 Berlin, Germany: Springer Verlag.

Peakall, R. , & Smouse, P. E. (2012). GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research‐an update. Bioinformatics, 28, 2537–2539. 10.1093/bioinformatics/bts460 PubMed DOI PMC

Pichancourt, J.‐B. , Chades, I. , Firn, J. , van Klinken, R. D. , & Martin, T. G. (2012). Simple rules to contain an invasive species with a complex life cycle and high dispersal capacity. Journal of Applied Ecology, 49, 52–62. 10.1111/j.1365-2664.2011.02093.x DOI

Popa, O. P. , Bartáková, V. , Bryja, J. , Reichard, M. , & Popa, L. O. (2015). Characterization of nine microsatellite markers and development of multiplex PCRs for the Chinese huge mussel DOI

Popa, O. P. , Popa, L. O. , Krapal, A.‐M. , Murariu, D. , Iorgu, E. I. , & Costache, M. (2011). PubMed DOI PMC

Pou‐Rovira, Q. , Araujo, R. , Boix Masafret, D. , Clavero Pineda, M. , Feo, C. , Ordeix‐Rigo, M. , & Zamora Hernández, L. (2009). Presence of the alien chinese pond mussel

Pritchard, J. K. , Stephens, M. , & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959. PubMed PMC

Reichard, M. , Douda, K. , Przybylski, M. , Popa, O. P. , Karbanová, E. , Matasová, K. , … Smith, C. (2015). Population‐specific responses to an invasive species. Proceedings of the Royal Society B‐Biological Sciences, 282, 167–174. PubMed PMC

Reichard, M. , Vrtílek, M. , Douda, K. , & Smith, C. (2012). An invasive species reverses the roles in a host‐parasite relationship between bitterling fish and unionid mussels. Biology Letters, 8, 601–604. 10.1098/rsbl.2011.1234 PubMed DOI PMC

Ricciardi, A. , & MacIsaac, H. J. (2011). Impacts of biological invasions on freshwater ecosystems In Richardson D. M. (Ed.), Fifty years of invasion ecology: The legacy of Charles Elton (pp. 211–224). Oxford, UK: Wiley‐Blackwell.

Roman, J. , & Darling, J. A. (2007). Paradox lost: Genetic diversity and the success of aquatic invasions. Trends in Ecology & Evolution, 22, 454–464. 10.1016/j.tree.2007.07.002 PubMed DOI

Sakai, A. K. , Allendorf, F. W. , Holt, J. S. , Lodge, D. M. , Molofsky, J. , With, K. A. , … Weller, S. G. (2001). The population biology of invasive species. Annual Review of Ecology and Systematics, 32, 305–332. 10.1146/annurev.ecolsys.32.081501.114037 DOI

Sárkány‐Kiss, A. (1986). Anodonta woodiana (Lea, 1834) a new species in Romania (Bivalvia, Unionacea). Travaux du. Muséum National d Histoire Naturelle “Grigore Antipa”, 28, 15–17.

Sayenko, E. M. , Soroka, M. , & Kholin, S. K. (2017). Comparison of the species DOI

Seehausen, O. , van Alphen, J. J. M. , & Witte, F. (1997). Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science, 277, 1808–1811. 10.1126/science.277.5333.1808 DOI

Slatkin, M. (1995). A measure of population subdivision based on microsatellite allele frequencies. Genetics, 139, 1463. PubMed PMC

Smith, C. , Reichard, M. , Jurajda, P. , & Przybylski, M. (2004). The reproductive ecology of the European bitterling ( DOI

Solustri, C. , & Nardi, G. (2006). Una nuova stazione di

Soroka, M. (2000). Age structure and sex ratio of

Soroka, M. , & Zdanowski, B. (2001). Morphological and genetic variability of the population of

Spyra, A. , Jedraszewska, N. , Strzelec, M. , & Krodkiewska, M. (2016). Further expansion of the invasive mussel DOI

Stone, G. N. , White, S. C. , Csoka, G. , Melika, G. , Mutun, S. , Penzes, Z. , … Nicholls, J. A. (2017). Tournament ABC analysis of the western Palaearctic population history of an oak gall wasp, PubMed DOI

Strayer, D. L. (2012). Eight questions about invasions and ecosystem functioning. Ecology Letters, 15, 1199–1210. 10.1111/j.1461-0248.2012.01817.x PubMed DOI

Svensson, M. , & Ekström, L. (2005). Musselinventering I Några Skånska Vattendrag 2005 – Med Särskild Focus Påtjockskalig Målarmussla (Unio crassus). Natur och kulturmiljö, 95 pp.

Tamura, K. , Stecher, G. , Peterson, D. , Filipski, A. , & Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729. 10.1093/molbev/mst197 PubMed DOI PMC

Therriault, T. W. , Orlova, M. I. , Docker, M. F. , MacIsaac, H. J. , & Heath, D. D. (2005). Invasion genetics of a freshwater mussel ( PubMed DOI

Torchin, M. E. , & Mitchell, C. E. (2004). Parasites, pathogens, and invasions by plants and animals. Frontiers in Ecology and the Environment, 2, 183–190. 10.1890/1540-9295(2004)002%5b0183:PPAIBP%5d2.0.CO;2 DOI

Truhlar, A. M. , & Aldridge, D. C. (2015). Differences in behavioural traits between two potentially invasive amphipods, DOI

Urbanska, M. , Lakomy, A. , Andrzejewski, W. , & Mazurkiewicz, J. (2012). The story of one clam. Probably the oldest location of the Chinese pond mussel

van Boheemen, L. A. , Lombaert, E. , Nurkowski, K. A. , Gauffre, B. , Rieseberg, L. H. , & Hodgins, K. A. (2017). Multiple introductions, admixture and bridgehead invasion characterize the introduction history of PubMed DOI

Verhoeven, K. J. F. , Macel, M. , Wolfe, L. M. , & Biere, A. (2011). Population admixture, biological invasions and the balance between local adaptation and inbreeding depression. Proceedings of the Royal Society B‐Biological Sciences, 278, 2–8. 10.1098/rspb.2010.1272 PubMed DOI PMC

Vikhrev, I. V. , Konopleva, E. S. , Gofarov, M. Y. , Kondakov, A. V. , Chapurina, Y. E. , & Bolotov, I. N. (2017). A Tropical biodiversity hotspot under the new threat: Discovery and DNA barcoding of the invasive Chinese pond mussel DOI

Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299. PubMed

Watters, G. T. (1997). A synthesis and review of the expanding range of the asian freshwater mussel

Temporal Dynamics of Biological Invasions: Perception of Host Quality Differs Between Native and Alien Host Species

The impact of invasive Sinanodonta woodiana (Bivalvia, Unionidae) and mussel macroparasites on the egg distribution of parasitic bitterling fish in host mussels

Intensity-dependent energetic costs in a reciprocal parasitic relationship

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