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A Global Invader Is Possibly Two: First Genetic Investigation of Native Populations of the Estuarine Bivalve Mytilopsis leucophaeata (Dreissenidae)

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Abstract

Mytilopsis leucophaeata is an estuarine bivalve native from the Gulf of Mexico and possibly part of the eastern USA, which invaded many regions around the globe. Despite the previous discovery that two genetic lineages of this species exist, one comprising the northeastern USA and Eurasia and another having invaded South America, there were no genetic data about specimens from native areas. We reveal for the first time the COI signatures of two native populations of M. leucophaeata, one in the eastern coast of Florida, another in its western coast, besides analyzing the nuclear gene 28S. The COI sequences from South America (Venezuela and Brazil) are similar to those from Florida, mainly to the population from the western coast, whereas the clade composed of sequences from NE USA and Eurasia diverges by 2.4–3.2% from remaining sequences. The 28S tree also confirmed the distinction of this lineage. We suspect that the cold-tolerant lineage may represent a distinct species originated in the mid-eastern or NE USA, possibly derived from glaciations or the formation of the Labrador Current, and having colonized Eurasia after human introductions. Based on data about ship trades, we also raise the hypothesis that the invasion in South America was composed of two stages, with an initial invasion in Venezuela or nearby Caribbean countries, followed by a secondary invasion in SE Brazil, although requiring further studies. These results may alter deeply our understanding about the invasion of M. leucophaeata around the globe.

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References

  • Armstrong, C., F. Zheng, A. Wachnicka, A. Khan, Z. Chen, and L. Baldwin. 2019. Chapter 8C: St. Lucie and Caloosahatchee River watersheds annual report. In 2019 South Florida Environmental Report, Volume I. South Florida Water Management District.

  • Astudillo, J.C., T.C. Bonebrake, and K.M.Y. Leung. 2017. The recently introduced bivalve Xenostrobus securis has higher thermal and salinity tolerance than the native Brachidontes variabilis and established Mytilopsis sallei. Marine Pollution Bulletin 118: 229–236.

    Article  CAS  Google Scholar 

  • Baeza, J.A., and S. Prakash. 2019. An integrative taxonomic and phylogenetic approach reveals a complex of cryptic species in the ‘peppermint’ shrimp Lysmata wurdemanni sensu stricto. Zoological Journal of the Linnean Society 185: 1018–1038.

    Article  Google Scholar 

  • Bandelt, H.J., P. Forster, and A. Röhl. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37–48.

    Article  CAS  Google Scholar 

  • Bieler, R., P.M. Mikkelsen, T.M. Collins, E.A. Glover, V.L. González, D.L. Graf, E.M. Harper, J. Healy, G.Y. Kawauchi, P.P. Sharma, S. Staubach, E.E. Strong, J.D. Taylor, I. Tëmkin, J.D. Zardus, S. Clark, A. Guzmán, E. McIntyre, P. Sharp, and G. Giribet. 2014. Investigating the Bivalve Tree of Life — An exemplar-based approach combining molecular and novel morphological characters. Invertebrate Systematics 28: 32–115.

    Article  Google Scholar 

  • Brown, E.A., F.J.J. Chain, A. Zhan, H.J. MacIsaac, and M.E. Cristescu. 2016. Early detection of aquatic invaders using metabarcoding reveals a high number of nonindigenous species in Canadian ports. Diversity and Distributions 22: 1045–1059.

    Article  Google Scholar 

  • Combosch, D.J., T.M. Collins, E.A. Glover, D.L. Graf, E.M. Harper, J.M. Healy, G.Y. Kawauchi, S. Lemer, E. McIntyre, E.E. Strong, J.D. Taylor, J.D. Zardus, P.M. Mikkelsen, G. Giribet, and R. Bieler. 2016. A family-level tree of life for bivalves based on a Sanger-sequencing approach. Molecular Phylogenetics and Evolution 107: 191–208.

    Article  Google Scholar 

  • Conrad, T. A. 1831. Description of fifteen new species of Recent, and three of fossil shells, chiefly from the coast of the United States. Journal of the Academy of Natural Sciences of Philadelphia 6: 256–268, plate 11.

  • Conrad, T.A. 1857. Description of a new genus of the family Dreissenidae. Proceedings of the Academy of Natural Sciences of Philadelphia 9: 167.

    Google Scholar 

  • Coolen, J.W.P., A.R. Boon, R. Crooijmans, H. van Pelt, F. Kleissen, D. Gerla, J. Beermann, S.N.R. Birchenough, L.E. Becking, and P.C. Luttikhuizen. 2020. Marine stepping-stones: Connectivity of Mytilus edulis populations between offshore energy installations. Molecular Ecology 29: 686–703.

    Article  CAS  Google Scholar 

  • Corander, J., and J. Tang. 2007. Bayesian analysis of population structure based on linked molecular information. Mathematical Biosciences 205: 19–31.

    Article  Google Scholar 

  • Corander, J., P. Marttinen, J. Sirén, and J. Tang. 2008. Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9: 539.

    Article  Google Scholar 

  • Excoffier, L., and H.E.L. Lischer. 2010. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.

    Article  Google Scholar 

  • Fernandes, M.R., F. Salgueiro, I.C. Miyahira, and C.H.S. Caetano. 2018. mtDNA analysis of Mytilopsis (Bivalvia, Dreissenidae) invasion in Brazil reveals the existence of two species. Hydrobiologia 817: 97–110.

    Article  CAS  Google Scholar 

  • Fernandes, M. R., I. C. Miyahira, C. H. S. Caetano, and F. Salgueiro. 2020. The spreading of the invasive bivalve Mytilopsis leucophaeata (Dreissenidae) into estuaries of Rio de Janeiro, Brazil. Anais da Academia Brasileira de Ciências 92: e20190045.

  • Flemming, A.T., J.E. Weinstein, and A.J. Lewitus. 2008. Survey of PAH in low density residential stormwater ponds in coastal South Carolina: False dark mussels (Mytilopsis leucophaeata) as potential biomonitors. Marine Pollution Bulletin 56: 1598–1608.

    Article  CAS  Google Scholar 

  • Florin, A., K. Mo, F. Svensson, E. Schagerström, L. Kautsky, and L. Bergström. 2013. First records of Conrad’s false mussel, Mytilopsis leucophaeata in the southern Bothnian Sea, Sweden, near a nuclear power plant. BioInvasions Records 2: 303–309.

    Article  Google Scholar 

  • Forsström, T., A.E. Fowler, M. Lindqvist, and O. Vesakoski. 2016. The introduced dark false mussel, Mytilopsis leucophaeata (Conrad, 1831) has spread in the northern Baltic Sea. BioInvasions Records 5: 81–84.

    Article  Google Scholar 

  • Geda, S.R., N.K. Lujan, M. Perkins, E. Abernethy, M.H. Sabaj, and M. Gangloff. 2018. Multilocus phylogeny of the zebra mussel family Dreissenidae (Mollusca: Bivalvia) reveals a fourth Neotropical genus sister to all other genera. Molecular Phylogenetics and Evolution 127: 1020–1033.

    Article  Google Scholar 

  • Geller, J., C. Meyer, M. Parker, and H. Hawk. 2013. Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all-taxa biotic surveys. Molecular Ecology Resources 13: 851–861.

    Article  CAS  Google Scholar 

  • Grant, W.S. 2015. Problems and cautions with sequence mismatch analysis and Bayesian skyline plots to infer historical demography. Journal of Heredity 106: 333–346.

    Article  Google Scholar 

  • Guindon, S., J.F. Dufayard, V. Lefort, M. Anisimova, W. Hordijk, and O. Gascuel. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biology 59: 307–321.

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Heiler, K.C.M., N. Nahavandi, and C. Albrecht. 2010. A new invasion into an ancient lake - the invasion history of the dreissenid mussel Mytilopsis leucophaeata (Conrad, 1831) and its first record in the Caspian Sea. Malacologia 53: 185–192.

    Article  Google Scholar 

  • Kelly, D.W., H.J. MacIsaac, and D.D. Heat. 2006. Vicariance and dispersal effects on phylogeographic structure and speciation in a widespread estuarine invertebrate. Evolution 60: 257–267.

    Google Scholar 

  • Kennedy, V.S. 2011a. The invasive dark falsemussel Mytilopsis leucophaeata (Bivalvia: Dreissenidae): A literature review. Aquatic Ecology 45: 163–183.

    Article  Google Scholar 

  • Kennedy, V.S. 2011b. Biology of the uncommon dreissenid bivalve Mytilopsis leucophaeata (Conrad, 1831) in central Chesapeake Bay. Journal of Molluscan Studies 77: 154–164.

    Article  Google Scholar 

  • Kumar, S., G. Stecher, and K. Tamura. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870–1874.

    Article  CAS  Google Scholar 

  • Librado, P., and J. Rozas. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.

    Article  CAS  Google Scholar 

  • Lodeiros, C., N. Gonzáles-Henríquez, J. Cuéllar-Anjel, D. Hernández-Reyes, C. Medina-Alcaraz, J. Quinteiro, and M. Rey-Méndez. 2019. Invasion of the dark false mussel in shrimp farms in Venezuela: Species identification and genetic analysis. BioInvasions Records 8: 838–847.

    Article  Google Scholar 

  • Maggs, C.A., R. Castilho, D. Foltz, C. Henzler, M.T. Jolly, J. Kelly, J. Olsen, K.E. Perez, W. Stam, R. Väinölä, F. Viard, and J. Wares. 2008. Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology 89: S108–S122.

    Article  Google Scholar 

  • Marelli, D. C. 2021. Incorrect identification of invasive Indo-Pacific member of the bivalve genus Mytilopsis can affect construction of molecular phylogenies. Journal of Sea Research 175: 102084.

  • Marelli, D.C., and S. Gray. 1983. Conchological redescriptions of Mytilopsis sallei and Mytilopsis leucophaeta of the brackish Western Atlantic. The Veliger 25: 185–193.

    Google Scholar 

  • Marko, P.B. 2004. ‘What’s larvae got to do with it?’ Disparate patterns of post-glacial population structure in two benthic marine gastropods with identical dispersal potential. Molecular Ecology 13: 597–611.

    Article  CAS  Google Scholar 

  • Marshall, N.T., and C.A. Stepien. 2019. Invasion genetics from eDNA and thousands of larvae: A targeted metabarcoding assay that distinguishes species and population variation of zebra and quagga mussels. Ecology and Evolution 2019: 3515–3538.

    Article  Google Scholar 

  • Meyer, C.P. 2003. Molecular systematics of cowries (Gastropoda: Cypraeidae) and diversification patterns in the tropics. Biological Journal of the Linnean Society 79: 401–459.

    Article  Google Scholar 

  • Mikkelsen, P.M., and R. Bieler. 2004. Critical catalog and annotated bibliography of marine bivalve records for the Florida Keys. Malacologia 46: 545–623.

    Google Scholar 

  • Minchin, D., and E.J. Cottier-Cook. 2020. First record of the false mussel Mytilopsis sp. (Dreissenidae) from Grand Cayman, Caribbean Sea. Journal of Conchology 43: 503–511.

    Google Scholar 

  • Mohammed, R.S., K. Khan, and D.C. Nieweg. 2018. First report of the freshwater mussel Mytilopsis leucophaeata (Family Dreissenidae) in Trinidad W.I. and a new locality record of the native Anodontites crispata (Family Unionidae). Living World. J. Trinidad and Tobago Field Naturalists’ Club 2018: 102–104.

    Google Scholar 

  • Mumladze, L., A. Bikashvili, B. Japoshvili, and V.V. Anistratenko. 2019. New alien species Mytilopsis leucophaeata and Corbicula fluminalis (Mollusca, Bivalvia) recorded in Georgia and notes on other non-indigenous molluscs invaded the South Caucasus. Vestnik Zoologii 53: 187–194.

    Article  Google Scholar 

  • Neves, R. A. F., C. Naveira, I. C. Miyahira, S. G. M. Portugal, N. Krepsky, and L. N. Santos. 2020. Are invasive species always negative to aquatic ecosystem services? The role of dark false mussel for water quality improvement in a multi-impacted urban coastal lagoon. Water Research 184: 116108.

  • Nuttall, C.P. 1990a. A review of the Tertiary non-marine molluscan faunas of the Pebasian and other inland basins of north-western South America. Bulletin of the British Museum (Natural History). Geology 45: 165–371.

    Google Scholar 

  • Nuttall, C.P. 1990b. Review of the Caenozoic heterodont bivalve superfamily Dreissenacea. Palaeontology 33: 707–737.

    Google Scholar 

  • Oliver, P. G. 2015. Old shell collection casts new light on an alien species. The dark false mussel (Mytilopsis leucophaeata) may have been in Britain as early as 1800! Journal of Conchology 42: 1–4.

  • Park, J.K., and D.Ó. Foighil. 2000. Sphaeriid and corbiculid clams represent separate Heterodont bivalve radiations into freshwater environments. Molecular Phylogenetics and Evolution 14: 75–88.

    Article  CAS  Google Scholar 

  • Pathy, D.A., and G.L. Mackie. 1993. Comparative shell morphology of Dreissena polymorpha, Mytilopsis leucophaeata, and the “quagga” mussel (Bivalvia: Dreissenidae) in North America. Canadian Journal of Zoology 71: 1012–1023.

    Article  Google Scholar 

  • Pointier, J. 2015. Freshwater molluscs of Venezuela and their medical and veterinary importance. Harxheim: ConchBooks.

    Google Scholar 

  • Queiroz, R. N. M., P. M. Silva, A. M. DeSouza, L. B. Silva, and T. L. P. Dias. 2020. Effects of environmental factors on the distribution of the exotic species Mytilopsis sallei (Récluz, 1849) (Bivalvia: Dreissenidae) on the Northeast coast of Brazil. Journal of Sea Research 165: 101954.

  • Ramos-Onsins, S.E., and J. Rozas. 2002. Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution 19: 2092–2100.

    Article  CAS  Google Scholar 

  • Richardson, D.J., and C.I. Hammond. 2016. Dark false mussel, Mytilopsis leucophaeata (Bivalvia: Dreissenidae), in the Lower West River, New Haven, New Haven County, Connecticut. Bulletin of the Peabody Museum of Natural History 57: 117–125.

    Article  Google Scholar 

  • Riesgo, A., E.A. Burke, C. Laumer, and G. Giribet. 2017. Genetic variation and geographic differentiation in the marine triclad Bdelloura candida (Platyhelminthes, Tricladida, Maricola), ectocommensal on the American horseshoe crab Limulus polyphemus. Marine Biology 164: 111.

    Article  Google Scholar 

  • Rizzo, A.E., I.C. Miyahira, G. Moser, and S.B. Santos. 2014. A new record of Mytilopsis leucophaeata (Bivalvia: Dreissenidae) in Rio de Janeiro (Brazil). Marine Biodiversity Records 7: 1–6.

    Article  Google Scholar 

  • Rodrigues, A. J., M. R. Fernandes, I. C. Miyahira, L. N. Santos, and C. H. S. Caetano. 2021. Benthic macrofauna associated to the invasive bivalve Mytilopsis leucophaeata (Dreissenidae) in a coastal lagoon in Rio de Janeiro, Brazil. Anais da Academia Brasileira de Ciênciashttps://doi.org/10.1590/0001-3765202120191221.

  • Ronquist, F., M. Teslenko, P. van der Mark, D.L. Ayres, A. Darling, S. Höhna, B. Larget, L. Liu, M.A. Suchard, and J.P. Huelsenbeck. 2012. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542.

    Article  Google Scholar 

  • Schütz, L. 1969. Ökologische Untersuchungen über die Benthosfauna im Nordostseekanal III. Autökologie der vagilen und hemisessilen Arten im Bewuchs der Pfähle: Makrofauna. Internationale Revue Der Gesamten Hydrobiologie 54: 553–592.

    Article  Google Scholar 

  • Siddall, S.E. 1980. Early development of Mytilopsis leucophaeata (Bivalvia: Dreissenacea). The Veliger 22: 378–379.

    Google Scholar 

  • Stepien, C.A., I.A. Grigorovich, M.A. Gray, T.J. Sullivan, S. Yerga-Woolwine, and G. Kalayci. 2014. Evolutionary, biogeographic, and population genetic relationships of dreissenid mussels, with revision of component taxa. In Quagga and Zebra Mussel: Biology, impacts, and control, 2nd ed., ed. T.F. Nalepa and D.W. Schloesser, 403–444. Boca Raton: CRC Press.

    Google Scholar 

  • Van der Gaag, M., G. Van der Velde, F.P.L. Collas, and R.S.E.W. Leuven. 2020. Shell mass, biomass, condition and reproductive state of the invasive bivalve Mytilopsis leucophaeata (Conrad, 1831) (Dreissenidae). Journal of Shellfish Research 39: 1–7.

    Article  Google Scholar 

  • Verween, A., M. Vincx, and S. Degraer. 2010. Mytilopsis leucophaeata: the brackish water equivalent of Dreissena polymorpha? A review. In The Zebra Mussel in Europe, eds. G. Van der Velde, S. Rajagopal, and A. bij de Vaate, 29–44. Weikersheim and Vienna: Leiden Margraf Publishers.

  • Wares, J.P., S. Crickenberger, A.F. Govindarajan, J.L. Hamrick, K.M. Skoczen, D.W. Trapnell, and D.S. Wethey. 2018. The cryptic population biology of Chthamalus fragilis Darwin, 1854 (Cirripedia, Thoracica) on the Atlantic coast of North America. Journal of Crustacean Biology 38: 754–764.

    Article  Google Scholar 

  • Zhulidov, A.V., A.V. Kozhara, G. Van der Velde, R.S.E.W. Leuven, D.A. Zhulidov, T.Y. Gurtovaya, T.F. Nalepa, and V.J.R. Santiago-Fandino. 2015. New records from the Ponto-Azov region demonstrate the invasion potential of Mytilopsis leucophaeata (Conrad, 1831) (Bivalvia: Dreissenidae). Journal of Molluscan Studies 81: 412–416.

    Article  Google Scholar 

  • Zhulidov, A.V., A.V. Kozhara, M.O. Son, H. Morhun, G. van der Velde, R.S.E.W. Leuven, T.Y. Gurtovaya, D.A. Zhulidov, E.A. Kalko, Y.A. Kuklina, L.S. Kosmenko, V.J.R. Santiago-Fandino, and T.F. Nalepa. 2021. Additional records of the bivalves Mytilopsis leucophaeata (Conrad, 1831) (Dreissenidae) and Arcuatula senhousia (Benson, 1842) (Mytilidae) in the Ponto-Caspian region. BioInvasions Records 10: 119–135.

    Article  Google Scholar 

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Acknowledgements

We are very grateful to Dr. Amanda Bemis and Dr. John Slapcinsky (FLMNH) for the loan of samples of Mytilopsis cf. sallei, Dr. Yolanda Villacampa (NMNH) for photographing some shells of Mytilopsis leucophaeata, Dr. José H. Leal (BMSM) for providing support for the research conducted by MRF in Fort Myers, Dr. Marcelo H. Prado and MSc. Danilo Gonçalves (IME) for providing access to the SEM equipment, two anonymous reviewers for improving an initial version of the manuscript, and the section of Herpetology of MNRJ for sharing the available infrastructure and proper equipment during initial stages of the research.

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Correspondence to Maurício R. Fernandes.

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Fernandes, M.R., Salgueiro, F. & Miyahira, I.C. A Global Invader Is Possibly Two: First Genetic Investigation of Native Populations of the Estuarine Bivalve Mytilopsis leucophaeata (Dreissenidae). Estuaries and Coasts 45, 812–826 (2022). https://doi.org/10.1007/s12237-021-01007-z

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