Abstract
A plethora of unionid names was established in the nineteenth century by the “Nouvelle Ecole”. Although naiad morphological plasticity is well documented, the currently recognized fauna, with 17 species and subspecies included in the French checklist for the Unio genus, is still based upon morphological characters only. Insights have been provided from molecular data elsewhere in Europe and North Africa, but the French fauna remains unstudied. We present a molecular phylogeny of the Unio genus in France based on COI, 16S and 28S genes; taking up all available data in Europe plus 273 specimens collected in all main French drainages. The results show that there are either three valid species in France, with U. pictorum and U. mancus synonymized, or five, with the subspecies U. crassus courtillieri elevated to species level. Subspecies were generally not recovered, which questions the evolutionary units tacitly implied by subspecific names. Although sampling topotypes is the most reliable way to evaluate the status of a nominal subspecies, major human-induced changes in aquatic hydrosystems challenge the method. Nevertheless, operational taxonomy has to rely on ground-truthed data and we propose to reduce the actual number of valid taxa in France to the seven observed operational taxonomic units.
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References
Agrell, I., 1948. The shell morphology of some Swedish unionids as affected by ecological conditions. Arkiv för Zoologi 41A: 1–30.
Araujo, R., I. Gómez & A. Machordom, 2005. The identity and biology of Unio mancus Lamarck, 1819 (= U. elongatulus) (Bivalvia: Unionidae) in the Iberian Peninsula. Journal of Molluscan Studies 71: 25–31.
Araujo, R., C. Toledo, D. V. Damme, M. Ghamizi & A. Machordom, 2009a. Margaritifera marocana (Pallary, 1918): a valid species inhabiting Moroccan rivers. Journal of Molluscan Studies 75: 95–101.
Araujo, R., C. Toledo & A. Machordom, 2009b. Redescription of Unio gibbus Spengler, 1793, a west palaearctic freshwater mussel with hookless glochidia. Malacologia 51: 131–141.
Backeljau, T., 2001. Genetic and phylogentic data in Molluscan conservation. 17. In Salvini-Plawen, L., J. Voltzow, H. Sattmann & G. Steiner (eds), World Congress of Malacology. Unitas Malacologia, Vienna, Austria.
Bouchet, P., 2006. Valid until synonymized, or invalid until proven valid? A response to Davis (2004) on species check-lists. Malacologia 48: 311–319.
Cappelletti, C., S. Cianfanelli, M. E. Beltrami & F. Ciutti, 2009. Sinanodonta woodiana (Lea, 1834) (Bivalvia: Unionidae): a new non-indigenous species in Lake Garda (Italy). Aquatic invasions 4: 685–688.
Chase, M. W., N. Salamin, M. Wilkinson, J. M. Dunwell, R. P. Kesanakurthi, N. Haidar & V. Savolainen, 2005. Land plants and DNA barcodes: short-term and long-term goals. Philosophical Transactions of the Royal Society B 360: 1889–1895.
Dayrat, B., 2005. Towards integrative taxonomy. Biological Journal of the Linnean Society 85: 407–415.
de Queiroz, K., 1999. The general lineage concept of species and the defininig properties of the species category. In Wilson, R. A. (ed.), Species: New Interdisciplinary Essays. MIT Press, Cambridge: 79–89.
Falkner, G., 1991. Schnecken und Muscheln. In O. Aßmann (ed.), Stützkraftstufe Landau a. d. Isar – Entwicklung der Pflanzen- und Tierwelt in den ersten 5 Jahren. Schriftenreihe des Bayerischen Landesamtes für Wasserwirtschaft, München: 95–108, 149–154.
Falkner, G., T. E. J. Ripken & M. Falkner, 2002. Mollusques continentaux de la France. Liste de référence annotée et bibliographie. Patrimoine Naturels 52: 1–350.
Funk, D. J. & K. E. Omland, 2003. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology Evolution and Systematics 34: 397–423.
Gargominy, O., V. Prié, J.-M. Bichain, X. Cucherat & B. Fontaine, 2011. Liste de référence annotée des mollusques continentaux de France. MalaCo 7: 307–382.
Geist, J., 2010. Strategies for the conservation of endangered freshwater pearl mussels (Margaritifera margaritifera L.): a synthesis of Conservation Genetics and Ecology. Hydrobiologia 644: 69–88.
Geist, J., H. Wunderlich & R. Kuehn, 2008. Use of mollusc shells for DNA-based molecular analyses. Journal of Molluscan Studies 74: 337–343.
Geist, J., H. Söderberg, A. Karlsberg & R. Kuehn, 2010. Drainage-independent genetic structure and high genetic diversity of endangered freshwater pearl mussels (Margaritifera margaritifera) in northern Europe. Conservation Genetics 11: 1339–1350.
Germain, L., 1931. Mollusques terrestres et fluviatiles (seconde partie). Paul Lechevalier, Paris.
Gherardi, F., S. Bertolino, M. Bodon, S. Casellato, S. Cianfanelli, M. Ferraguti, E. Lori, G. Mura, A. Nocita, N. Riccardi, G. Rossetti, E. Rota, R. Scalera, S. Zerunian & E. Tricarico, 2008. Animal xenodiversity in Italian inland waters: distribution, modes of arrival, and pathways. Biological Invasions 10: 435–454.
Graf, D. L., 2011. Types of French freshwater mussels (Mollusca, Bivalvia, Unionoidea) in the Arnould Locard Collection at the Muséum national d’Histoire naturelle, Paris. Zoosystema 33: 451–514.
Graf, D. L. & K. Cummings, 2007. Review of the systematics and global diversity of freshwater mussel species (Bivalvia: Unionoida). Journal of Molluscan Studies 73: 291–314.
Haas, F., 1940. A tentative classification of the Palearctic unionids. Zoological Series of Field Museum of Natural History 24: 115–141.
Haas, F., 1969. Superfamilia Unionacea. De Gruyter, Berlin.
Hall, T. A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.
Huelsenbeck, J. P., F. Ronquist & B. Hall, 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.
Isaac, N. J. B., J. Mallet & G. M. Mace, 2004. Taxonomic inflation: its influence on macroecology and conservation. Trends in Ecology & Evolution 19: 464–469.
Jovelin, R. & J.-L. Justine, 2001. Phylogenetic relationships within the polyopisthocotylean monogeneans (Platyhelminthes) inferred from partial 28S rDNA sequences. International Journal for Parasitology 31: 393–401.
Källersjö, M., T. von Proschwitz, S. Lundberg, P. Eldenäs & C. Erséus, 2005. Evaluation of ITS rDNA as a complement to mitochondrial gene sequences for phylogenetic studies of freshwater mussels: an example using Unionidae from north-western Europe. Zoologica Scripta 34: 415–424.
Khalloufi, N., C. Toledo, A. Machordom, M. Boumaïza & R. Araujo, 2011. The Unionids of Tunisia: taxonomy and phylogenetic relationships, with redescription of Unio ravoisieri Deshayes, 1847 and U. durieui Deshayes 1847. Journal of Molluscan Studies 77: 103–115.
Locard, A., 1893. Conchyliologie française. Les Coquilles des eaux douces et saumâtres de France. Description des familles, genres et espèces. J.-B. Baillière & fils, Paris.
Lydeard, C., R. H. Cowie, W. F. Ponder, A. E. Bogan, P. Bouchet, S. A. Clark, K. S. Cummings, T. J. Frest, O. Gargominy, D. G. Herbert, R. Hershler, K. E. Perez, B. Roth, M. B. Seddon, E. E. Strong & F. G. Thompson, 2004. The global decline of nonmarine Mollusks. BioScience 54: 321–330.
Mace, G. M., 2004. The role of taxonomy in species conservation. Philosophical Transactions of the Royal Society of London 359: 711–719.
Machordom, A., R. Araujo, D. Erpenbeck & M. A. Ramos, 2003. Phylogeography and conservation genetics of endangered European Margaritiferidae (Bivalvia: Unionoidea). Biological Journal of the Linnean Society 78: 235–252.
May, R., 1990. Taxonomy as destiny. Nature 347: 129–130.
Mcmurray, S. E., G. A. Schuster & B. A. Ramey, 1999. Recruitment in a freshwater Unionid (Mollusca: Bivalvia) community downstream of Cave Run Lake in the Licking River, Kentucky. American Malacological Bulletin 15: 57–63.
Miller, M. A., W. Pfeiffer & T. Schwartz, 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans: 1–8.
Morrison, W. R., J. L. Lohr, P. Duchen, R. Wilches, D. Trujillo, M. Mair & S. S. Renner, 2009. The impact of taxonomic change on conservation: does it kill, can it save, or is it just irrelevant? Biological Conservation 142: 3201–3206.
Mouthon, J., 2012. Les mollusques de deux rivières franc-comtoises le Drugeon et la Clauge, comparaison entre les inventaires 1977–1978 et 2009–2010. MalaCo 8: 412–419.
Mulvey, M., C. Lydeard, D. L. Pyer, K. M. Hicks, J. Brim-Box, J. D. Williams & R. S. Butler, 1997. Conservation genetics of North American freshwater mussels Amblema and Megalonaias. Conservation Biology 11: 867–878.
Nagel, K.-O., 1992. Das Schalenwachstum dreier Muschelarten (Bivalvia: Unionidae) in der Schwalm, einem nordhessischen Mittelgebirgsfluβ. Decheniana 145: 165–176.
Nagel, K.-O., 2000. Testing hypotheses on the dispersal and evolutionary history of freshwater mussels (Mollusca: Bivalvia: Unionidae). Journal of Evolution Biology 13: 854–865.
Nagel, K.-O. & G. Badino, 2001. Population genetics and systematics of the European Unionidae. In Bauer, G. & K. Wächtler (eds), Ecology and Evolution of the Freshwater Mussels Unionidae. Springer, Berlin: 51–81.
Nesemann, H., 1993. Zoogeographie und Taxonomie der Muschel-Gattungen Unio Philipsson, 1788, Pseudanodonta Bourguignat, 1877 und Pseudunio Haas, 1910, im oberen und mittleren Donausystem (Bivalvia: Unionidae, Margaritiferidae). Nachrichtenblatt der Ersten Vorarlberger Malakologischen Gesellschaft 1: 20–40.
Ortmann, A. E., 1920. Correlation of shape and station in freshwater mussels (Naiades). Proceedings of the American Philosophical Society 59: 268–312.
Padial, J. M., A. Miralles, I. De la Riva & M. Vences, 2010. The integrative future of taxonomy. Frontiers in Zoology 7: 16.
Palumbi, S. R., 1996. Nucleic acids II: the Polymerase Chain Reaction. In Hillis, D. M., C. Moritz & B. K. Mable (eds), Molecular Systematics, 2nd ed. Sinauer, Sunderland, MA: 205–247.
Pillon, Y. & M. W. Chase, 2006. Taxonomic exaggeration and its effects on orchid conservation. Conservation Biology 21: 263–265.
Posada, D., 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.
Prié, V., 2012. Les sous-espèces de la Mulette méridionale Unio mancus Lamarck 1819 (Bivalvia, Unionidea) en France : descriptions originales et matériel topotypique. MalaCo 8: 428–446.
Prié, V., N. Puillandre & P. Bouchet, 2012. Bad taxonomy can kill: molecular reevaluation of Unio mancus Lamarck, 1819 (Bivalvia: Unionidae) and its accepted subspecies. Knowledge and Management of Aquatic Ecosystems 405: 18.
Puillandre, N., M. V. Modica, Y. Zhang, L. Sirovitch, M.-C. Boisselier, C. Cruaud, M. Holford & S. Samadi, 2012. Large scale species delimitation method for hyperdiverse groups. Molecular Ecology 21: 2671–2691.
Rambaut, A. & A. J. Drummond, 2007. Tracer v1.4. Available from http://beast.bio.ed.ac.uk/Tracer.
Reis, J. & R. Araujo, 2009. Redescription of Unio tumidiformis Castro, 1885 (Bivalvia, Unionidae), an endemism from the south-western Iberian Peninsula. Journal of Natural History 43: 1929–1945.
Rozas, J. & R. Rozas, 1999. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15: 174–175.
Sabater, S., 2008. Alteration of the global water cycle and their effects on river structure, function and services. Freshwater reviews 1: 75–88.
Sabater, S. & K. Tockner, 2010. Effects of hydrologic alterations on the ecological quality of river ecosystems. In Sabater, S. & D. Barcelo (eds), Water Scarcity in the Mediterranean: Perspectives Under Global Change. Springer, Berlin: 15–39.
Samadi, S. & A. Barberousse, 2006. The tree, the network, and the species. Biological Journal of the Linnean Society 89: 509–521.
Skidmore, R., C. Leach, J. Hoffman, W. Amos & D. C. Aldridge, 2010. Conservation genetics of the endangered depressed river mussel, Pseudonodonta complanata, using amplified fragment length polymorphism (AFLP) markers. Aquatic Conservation: Marine and Freshwater Ecosystems 20: 560–567.
Soroka, M., 2010. Characteristics of mitochondrial DNA of Unionid bivalves (Mollusca: Bivalvia: Unionidae). I. Detection and characteristics of doubly uniparental inheritance (DUI) of Unionid mitochondrial DNA. Folia Malacologica 18: 147–188.
Srivathsana, A. & R. Meier, 2012. On the inappropriate use of Kimura-2-parameter (K2P) divergences in the DNA-barcoding literature. Cladistics 28: 190–194.
Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei & S. Kumar, 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731–2739.
Watters, G. T., 1994. Form and function of unionoidean shell sculpture and shape (Bivalvia). American Malacological Bulletin 11: 1–20.
Will, K. P., B. D. Mishler & Q. D. Wheeler, 2005. The perils of DNA barcoding and the need for integrative taxonomy. Systematic Biology 54: 844–851.
Wilson, C. D., D. Roberts & N. Reid, 2010. Applying species distribution modelling to identify areas of high conservation value for endangered species: a case study using Margaritifera margaritifera (L.). Biological Conservation 144: 821–829.
Zieritz, A. & D. C. Aldridge, 2009. Identification of ecophenotypic trends within three European freshwater mussel species (Bivalvia: Unionoida) using traditional and modern morphometric techniques. Biological Journal of the Linnean Society 98: 814–825.
Zieritz, A., A. G. Checa, D. C. Aldridge & E. M. Harper, 2010a. Variability, function and phylogenetic significance of periostracal microprojections in unionid bivalves (Mollusca). Journal of Zoological Systematics and Evolutionary Research 49: 6–15.
Zieritz, A., J. I. Hoffman, W. Amos & D. C. Aldridge, 2010b. Phenotypic plasticity and genetic isolation-by-distance in the freshwater mussel Unio pictorum. Evolutionary Ecology 24: 923–938.
Acknowledgments
Benjamin Adam (Biotope), Jean-Michel Bichain, Michel Bramard (Office National de l’Eau et des Milieux Aquatiques), Gilbert Cochet, Xavier Cucherat (Biotope), Erwann Jacquin (Deli-Sports), Florent Lamand (Office National de l’Eau et des Milieux Aquatiques), Olivier Hesnard, Patrick Le Mao, Joseph Mateï (Office National de l’Eau et des Milieux Aquatiques), Marie-Lilith Patou (Biotope), Pierre-Yves Pasco (Bretagne vivante), Henri Persat (Laboratoire d’Ecologie des Hydrosystèmes Naturels et Anthropisés), Laurent Philippe (Biotope), Ludwick Simon (Biotope), Sylvain Vrignaud and Antoine Wagner all took part in the sampling effort. Gérard Tardivo (Direction Régionale de l’Environnement, de l’Aménagement et du Logement de la région Centre) and Stephane Laine (Ministère de l’Ecologie, du Développement Durable et de l’Energie) sanctioned a special authorization for sampling the protected species U. crassus. The authors also thank Barbara Buge for her help in curating the MNHN collection and Rafael Araujo and Gargo Fontaine for constructive discussions during the redaction of this paper. Ian Killeen has edited the English. We also thank two anonymous reviewers for their constructive comments that allowed improving the overall quality of the manuscript. This study was completed with financial support of Biotope (PI Frederic Melki) and grants from Muséum national d’Histoire naturelle à Paris ATM Barcode (PIs Sarah Samadi and Jean-Noël Labat) and Agence Nationale de la Recherche “6eme extinction” (PI Philippe Bouchet).
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Guest editors: Manuel P. M. Lopes-Lima, Ronaldo G. Sousa, Simone G. P. Varandas, Elsa M. B. Froufe & Amílcar A. T. Teixeira / Biology and Conservation of Freshwater Bivalves
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Prié, V., Puillandre, N. Molecular phylogeny, taxonomy, and distribution of French Unio species (Bivalvia, Unionidae). Hydrobiologia 735, 95–110 (2014). https://doi.org/10.1007/s10750-013-1571-0
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DOI: https://doi.org/10.1007/s10750-013-1571-0