, Volume 784, Issue 1, pp 349–365 | Cite as

Genetic characterization of the Asian clam species complex (Corbicula) invasion in the Iberian Peninsula

  • Luis Peñarrubia
  • Rosa-Maria Araguas
  • Oriol Vidal
  • Carles Pla
  • Jordi Viñas
  • Nuria SanzEmail author
Primary Research Paper


The Asian clam (Corbicula sp.) is an invasive freshwater bivalve native to Asia, the Middle East, Australia, and Africa. It is now widely distributed around the world producing large ecological and economic impacts. Three well-described invasive lineages form a cryptic species complex with asexual reproduction based on androgenesis. In this study, we collected 175 individuals from different Iberian, European, and North American locations to genetically study Corbicula invasion in the Iberian Peninsula using COI and 28S genes. The use of mitochondrial and nuclear markers allows us to characterize both maternal and paternal inheritance from androgenetic Corbicula locations and to deal with the incongruences caused by egg parasitism. We identified 7 COI and 10 28S haplotypes that grouped individuals within the three invasive Corbicula lineages. Haplotype distribution of mitochondrial and nuclear markers detected genetic divergence between the Ebro Delta location and the rest of Iberian sites, suggesting that at least two invasion episodes occurred in the Iberian Peninsula. Haplotype distribution also suggested secondary contacts between Iberian and other European invaded regions. Additionally, results revealed that nuclear hybridization, a feature more widespread than previously reported, contributes to retain gene diversity in the Corbicula invasion.


Corbicula Iberian Peninsula Invasive species Mitochondrial COI Nuclear 28S Population structure 



We are indebted to different colleagues for Corbicula sample collections: J.C Pérez-Quintero (Universidad de Huelva), R. Araujo (CSIC), R. Miranda (Universidad de Navarra), J. Checa (Equipos y Suministros, S.L.), C. Alcaraz (IRTA, Spain), I. Planas and R. Puig (Nyctibios Association), J. F. Fruget (Université de Lyon), O. Popa and A. M. Krapaland (National Museum of Natural History, Romania), C. Robertson (Texas Parks and Wildlife Department, TX, USA) and J. Alvarado-Bremer (A&M University at Galveston, TX, USA). This research was carried out within the objectives of the research project CGL200909407 of the Spanish Ministerio de Ciencia e Innovación (MICINN). LP received a PhD fellowship support of the Spanish MICINN with reference BES—2010037446.

Supplementary material

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Supplementary material 1 (DOCX 75 kb)


  1. Araujo, R., D. Moreno & M. A. Ramos, 1993. The asiatic clam Corbicula fluminea (Müller, 1774) (Bivalvia: Corbiculidae) in Europe. American Malacological Bulletin 10: 39–49.Google Scholar
  2. Bandelt, H. J., P. Forster & A. Röhl, 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37–48.CrossRefPubMedGoogle Scholar
  3. Counts, C. L., 1981. Corbicula fluminea (Bivalvia: Corbiculidae) in British Columbia. Nautilus 95: 12–13.Google Scholar
  4. Darrigran, G., 2002. Potential impact of filter-feeding invaders on temperate inland freshwater environments. Biological Invasions 4: 145–156.CrossRefGoogle Scholar
  5. Drake, J. M., 2006. Heterosis, the catapult effect and establishment success of a colonizing bird. Biology letters 2: 304–307.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Excoffier, L. & H. E. Liescher, 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.CrossRefPubMedGoogle Scholar
  7. Folmer, O., M. Black, W. Hoeh, R. Lutz & R. Vrijenhoek, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.Google Scholar
  8. Foster, A. M., P. Fuller, A. Benson, S. Constant & D. Raikow, 2011. Corbicula fluminea. USGS Nonindigenous Aquatic Species Database, Gainesville.
  9. Hanna, G. D., 1966. Introduced mollusks of western North America. California Academy of Sciences Occasional Papers 48: 1–108.Google Scholar
  10. Hasegawa, M., H. Kishino & T. Yano, 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22: 160–174.CrossRefPubMedGoogle Scholar
  11. Hedgecock, D. & J. P. Davis, 2007. Heterosis for yield and crossbreeding of the Pacific oyster Crassostrea gigas. Aquaculture 272: S17–S19.CrossRefGoogle Scholar
  12. Hedtke, S. M., K. Stanger-Hall, R. J. Baker & D. M. Hillis, 2008. All-male asexuality: origin and maintenance of androgenesis in the Asian clam Corbicula. Evolution 62: 1119–1136.CrossRefPubMedGoogle Scholar
  13. Hedtke, S. M., M. Glaubrecht & D. M. Hillis, 2011. Rare gene capture in predominantly androgenetic species. PNAS 108(23): 9520–9524.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Ituarte, C. F., 1994. Corbicula and Neocorbicula (Bivalvia: Corbiculidae) in the Paraná, Uruguay, and Río de La Plata basins. Nautilus 107: 129–135.Google Scholar
  15. Karatayev, A. Y., L. E. Burlakova & D. K. Padilla, 2005. Contrasting distribution and impacts of two freshwater exotic suspension feeders, Dreissena polymorpha and Corbicula fluminea. In Dame, R. & S. Olenin (eds), The Comparative Roles of Suspension Feeders in Ecosystems. Springer, Netherlands: 239–262.CrossRefGoogle Scholar
  16. Karatayev, A. Y., D. K. Padilla, D. Minchin, D. Boltovskoy & L. E. Burlakova, 2007. Changes in global economies and trade: the potential spread of exotic freshwater bivalves. Biological Invasions 9: 161–180.CrossRefGoogle Scholar
  17. Kearse, M., R. Moir, A. Wilson, S. Stones-Havas, M. Cheung, S. Sturrock, S. Buxton, A. Cooper, S. Markowitz, C. Duran, T. Thierer, B. Ashton, P. Meintjes & A. Drummond, 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Komaru, A., M. Yamada & S. Houki, 2013. Relationship between two androgenetic clam species, Corbicula leana and Corbicula fluminea, inferred from mitochondrial Cytochrome b and nuclear 28S rRNA markers. Zoological Science 30: 360–365.CrossRefPubMedGoogle Scholar
  19. Komaru, A., S. Houki, M. Yamada, T. Miyake, M. Obata & K. Kawamura, 2012. 28S rDNA haplotypes of males are distinct from those of androgenetic hermaphrodites in the clam Corbicula leana. Development Genes and Evolution 222: 181–187.CrossRefPubMedGoogle Scholar
  20. Lee, T., S. Siripattrawan, C. F. Ituarte & D. Ó. Foighil, 2005. Invasion of the clonal clams: Corbicula lineages in the New World. American Malacology Bulletin 20: 113–122.Google Scholar
  21. Librado, T. & J. Rozas, 2009. DnaSP v5: a software for comprehensive analyses of DNA polymorphism data. Bioinformatics 25: 1451–1452.CrossRefPubMedGoogle Scholar
  22. Lois, S., 2010. New records of Corbicula fluminea (Müller, 1774) in Galicia (Northwest of the Iberian Peninsula): Mero, Sil and Deva rivers. Aquatic Invasions 5: S17–S20.CrossRefGoogle Scholar
  23. Lucy, F. E., A. Y. Karatayev & L. Burlakova, 2012. Predictions for the spread, population density, and impacts of Corbicula fluminea in Ireland. Aquatic Invasions 7: 465–474.CrossRefGoogle Scholar
  24. Lopez, M. A. & C. R. Altaba, 1997. Presencia de Corbicula fluminea (Müller, 1774) (Bivalvia, Corbiculidae) al Delta de L´Ebre. Bulleti del Parc Natural Delta de L´Ebre 10: 20–22.Google Scholar
  25. Marescaux, J., L. M. Pigneur & K. Van Doninck, 2010. New records of Corbicula clams in French rivers. Aquatic Invasions 5: S35–S39.CrossRefGoogle Scholar
  26. McMahon, R. F., 1982. The occurrence and spread of the introduced asiatic freshwater clam, Corbicula fluminea (Müller), in North-America – 1924-1982. Nautilus 96: 134–141.Google Scholar
  27. McMahon, R. F., 1999. Invasive characteristics of the freshwater bivalve Corbicula fluminea. In Claudi, R. & J. H. Leach (eds), Nonindigenous Freshwater Organisms: Vectors, Biology and Impacts. Lewis Publishers, Boca Raton: 315–343.Google Scholar
  28. Minchin, D., 2009. Corbicula fluminea (Müller), Asian clam (Corbiculidae, Mollusca). In DAISIE (ed.), Handbook of alien species in Europe. Springer, Dordrecht: 306.Google Scholar
  29. Mito, T., T. Tanaka & F. Aranish, 2014. Genetic variability and reproduction structure of Corbicula japonica in major fishing brackish lakes in Japan. Open Journal of Marine Science 4: 174–184.CrossRefGoogle Scholar
  30. MMARM (Ministerio Medio Ambiente, Rural y Marino), 2007. Estrategia Nacional para el Control del Mejillón Cebra (Dreissena polymorpha) en España. Accessed 31 July 2015.
  31. Mouthon, J., 1981. Sur la présence en France et au Portugal de Corbicula (Bivalvia, Corbiculidae) originaire d’Asie. Basteria 45: 109–116.Google Scholar
  32. Oscoz, J., P. Tomás & C. Durán, 2010. Review and new records of non-indigenous freshwater invertebrates in the Ebro River basin (Northeast Spain). Aquatic Invasions 5: 263–284.CrossRefGoogle Scholar
  33. Park, J. K. & D. Ó. Foighil, 2000. Sphaeriid and corbiculid clams represent separate heterodont bivalve radiations into freshwater environments. Molecular Phylogenetics and Evolution 14: 75–88.CrossRefPubMedGoogle Scholar
  34. Park, J. K. & W. Kim, 2003. Two Corbicula (Corbiculidae: Bivalvia) mitochondrial lineages are widely distributed in Asian freshwater environment. Molecular Phylogenetics and Evolution 29: 529–539.CrossRefPubMedGoogle Scholar
  35. Park, J. K., J. S. Lee & W. Kim, 2002. A single mitochondrial lineage is shared by morphological and allozymatically distinct freshwater Corbicula clones. Molecules and Cells 14: 315–322.Google Scholar
  36. Peñarrubia, L., N. Sanz, C. Pla, O. Vidal & J. Viñas, 2015. Using Massive Parallel Sequencing for the development, validation, and application of population genetics markers in the invasive bivalve zebra mussel (Dreissena polymorpha). PLoS One 10: e0120732.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Pérez-Bote, J. L. & J. Fernández, 2008. First record of the Asian clam Corbicula fluminea (Müller, 1774) in the Guadiana River Basin (southwestern Iberian Peninsula). Aquatic Invasions 3: 87–90.CrossRefGoogle Scholar
  38. Pfenninger, M., F. Reinhardt & B. Streit, 2002. Evidence for cryptic hybridization between different evolutionary lineages of the invasive clam genus Corbicula (Veneroida, Bivalvia). Journal of Evolutionary Biology 15: 818–829.CrossRefGoogle Scholar
  39. Pigneur, L. M., E. Etoundi, D. C. Aldridge, J. Marescaux, N. Yasuda & K. Van Doninck, 2014. Genetic uniformity and long-distance clonal dispersal in the invasive androgenetic Corbicula clams. Molecular Ecology 23: 5102–5116.CrossRefPubMedGoogle Scholar
  40. Pigneur, L. M., S. Hedtke, E. Etoundi & K. Van Doninck, 2012. Androgenesis: a review through the study of the selfish shellfish Corbicula spp. Heredity 108: 581–591.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Pigneur, L. M., J. Marescaux, K. Roland, E. Etoundi, J. P. Descy & K. Van Doninck, 2011. Phylogeny and androgenesis in the invasive Corbicula clams (Bivalvia, Corbiculidae) in Western-Europe. BMC Evolutionary Biology 11: 147.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Pimentel, D., R. Zuniga & D. Morrison, 2005. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52: 273–288.CrossRefGoogle Scholar
  43. Renard, E., V. Bachmann, M. L. Cariou & J. C. Moreteau, 2000. Morphological and molecular differentiation of invasive freshwater species of the genus Corbicula (Bivalvia, Corbiculidae) suggest the presence of three taxa in French rivers. Molecular Ecology 9: 2009–2016.CrossRefPubMedGoogle Scholar
  44. Ronquist, F., M. Teslenko, P. Van der Mark, D. Ayres, A. Darling, S. Höhna, B. Larget, L. Liu, M. A. Suchard & J. P. Huelsenbeck, 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Rueda, J., E. Gómez, J. M. Benavent, F. Collado, C. Peña, J. M. Rabasa, V. Sanz & A. Sebastián, 2012. First record of invasive exotic bivalve Corbicula fluminea (Müller, 1774) (Bivalvia, Corbiculidae) in the Júcar River basin (East Iberian Peninsula). Boletín de la Real Sociedad Española de Historia Natural, Actas 109: 21–22.Google Scholar
  46. Sanz, N., R. M. Araguas, O. Vidal, D. Diez-del-Molino, R. Fernández-Cebrián & J. L. García-Marín, 2013. Genetic characterization of the invasive mosquitofish (Gambusia spp.) introduced to Europe: population structure and colonization routes. Biological Invasions 15: 2333–2346.CrossRefGoogle Scholar
  47. Scheet, P. & M. Stephens, 2006. A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. American Journal of Human Genetics 78: 629–644.CrossRefPubMedPubMedCentralGoogle Scholar
  48. Siripattrawan, S., J. K. Park & D. Ó. Foighil, 2000. Two lineages of the introduced Asian freshwater clam Corbicula occur in North America. Journal of Molluscan Studies 66: 423–429.CrossRefGoogle Scholar
  49. Sousa, R., C. Antunes & L. Guilhermino, 2006. Factors influencing the occurrence and distribution of Corbicula fluminea (Müller, 1774) in the River Lima estuary. Annales de Limnologie – International Journal of Limnology 42: 165–171.CrossRefGoogle Scholar
  50. Sousa, R., R. Freire, M. Rufino, J. Méndez, M. Gaspar, C. Antunes & L. Guilhermino, 2007. Genetic and shell morphological variability of the invasive bivalve Corbicula fluminea (Müller, 1774) in two Portuguese estuaries. Estuarine, Coastal and Shelf Science 74: 166–174.CrossRefGoogle Scholar
  51. Sousa, R., C. Antunes & L. Guilhermino, 2008. Ecology of the invasive Asian clam Corbicula fluminea (Müller, 1774) in aquatic ecosystems: an overview. Annales de Limnologie – International Journal of Limnology 44: 85–94.CrossRefGoogle Scholar
  52. Sousa, R., A. Novais, R. Costa & D. L. Strayer, 2014. Invasive bivalves in fresh waters: impacts from Individuals to ecosystems and possible control strategies. Hydrobiologia 735: 233–251.CrossRefGoogle Scholar
  53. Tamura, K., 1992. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C content biases. Molecular Biology and Evolution 9: 678–687.PubMedGoogle Scholar
  54. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Wang, G. P., T. Zhang, J. Zhang, D. L. Li & T. Y. Xiao, 2014. Morphological and molecular differentiation of genus Corbicula suggests that two species are sympatrically distributed in Datong Lake in the Central Yangtze River Basin. Zoological Studies 53: 64.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Laboratori d’Ictiologia Genètica, Departament de BiologiaUniversitat de GironaGironaSpain

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