Organisms Diversity & Evolution

, Volume 16, Issue 3, pp 597–611 | Cite as

Who lives where? Molecular and morphometric analyses clarify which Unio species (Unionida, Mollusca) inhabit the southwestern Palearctic

  • Elsa Froufe
  • Duarte V. Gonçalves
  • Amílcar Teixeira
  • Ronaldo Sousa
  • Simone Varandas
  • Mohamed Ghamizi
  • Alexandra Zieritz
  • Manuel Lopes-Lima
Original Article


Many doubts still exist about which freshwater mussel Unio species inhabit Northwest Africa. While some authors refer to the presence of Unio delphinus in the Atlantic North African basins of Morocco, a recent International Union for Conservation of Nature (IUCN) assessment performed on Moroccan Unio species, recognised the existence of a distinct species, Unio foucauldianus, with a critically endangered conservation status. The present study delivered new genetic, morphological, and geographical distribution data on two Unio species (i.e. U. delphinus and U. foucauldianus) greatly increasing the almost non-existent data on these taxa. Bayesian phylogenetic analysis revealed two highly supported geographically concordant clades, which diverged by 3.2 ± 0.6 % (uncorrected p distance): the first distributed across Iberia and corresponding to U. delphinus, and the second distributed across Morocco, corresponding to U. foucauldianus. These results were corroborated by the analysis of ten newly developed microsatellite loci as well as shell morphometry. We suggest that the IUCN critically endangered conservation status of U. foucauldianus should be revised and probably down-listed since its actual distribution is much wider than previously described. Phylogenetic relationships with the other Unio species were resolved, showing that U. delphinus and U. foucauldianus fall inside the pictorum lineage. The estimated molecular rate reported herein (0.265 ± 0.06 % per million years) represents the first for the Unionida and could be used as a reference in future studies.


Freshwater molluscs Unionidae Microsatellites Messinian Molecular clock 



The authors wish to thank the two anonymous reviewers for helpful remarks and suggestions that improved the quality of the manuscript. Financial support was provided by Portuguese Foundation for Science and Technology (FCT) project PTDC/AAC-AMB/117688/2010 and by Mohamed bin Zayed Species Conservation Fund (reference 15256799). Official capture and sampling licenses were issued by the following agencies: (1) Junta de Castilla y León (Consejería de Fomento y Medio Ambiente EP/CYL/331/2012, de 17 de Abril de 2012); (2) Junta de Andalucia (Consejería de Medio Ambiente-SGYB/FOA/AFR/SFS, de 17 de Julio de 2012); and (3) Université Cadi Ayyad (Faculté des Sciences, Semlalia, Marrakech, Maroc).

Supplementary material

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Table S1 (DOCX 27 kb)
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Table S2 (DOCX 17 kb)
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Table S3 (DOCX 19 kb)
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Table S4 (DOCX 14 kb)


  1. Appleton, C. C. (1996). Freshwater mollusks of southern Africa, with a chapter on bilharzia and its snail hosts. Pietermaritzburg: University of Natal Press. 64 pp.Google Scholar
  2. Araujo, R. (2011a). Unio gibbus. In IUCN red list of threatened species 2011: e.T171953A6812362. Accessed 15 Oct 2015.Google Scholar
  3. Araujo, R. (2011b). Unio delphinus. In IUCN red list of threatened species. Version 2015.3. Available at Accessed 15 Oct 2015.
  4. Araujo, R. (2011c). Unio delphinus. In IUCN red list of threatened species 2011: e.T195510A8975648. doi: 10.2305/IUCN.UK.2011-2. RLTS.T195510A8975648.en. Accessed 08 Nov 2015.
  5. Araujo, R., Gómez, I., & Machordom, A. (2005). The identity and biology of Unio mancus (= U. elongatulus) (Bivalvia: Unionidae) in the Iberian Peninsula. Journal of Molluscan Studies, 71, 25–31.CrossRefGoogle Scholar
  6. Araujo, R., Reis, J., Machordom, A., Toledo, C., Madeira, M. J., Gómez, I., Velasco, J. C., Morales, J., Barea, J. M., Ondina, P., & Ayala, I. (2009a). The naiades of the Iberian Peninsula. Iberus, 27, 7–72.Google Scholar
  7. Araujo, R., Toledo, C., & Machordom, A. (2009b). Redescription of Unio gibbus Spengler, 1793, a west palaearctic freshwater mussel with hookless glochidia. Malacologia, 51, 131–141.CrossRefGoogle Scholar
  8. Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N., & Bonhomme, F. (2004). GENETIX 4.05, population genetics software for Windows TM. Montpellier: Université de Montpellier II.Google Scholar
  9. Breton, S., Beaupre, H. D., Stewart, D. T., Hoeh, W. R., & Blier, P. U. (2007). The unusual system of doubly uniparental inheritance of mtDNA: isn’t one enough? Trends in Genetics, 23, 465–474.CrossRefPubMedGoogle Scholar
  10. Brook, B. W., Sodhi, N. S., & Bradshaw, C. J. A. (2008). Synergies among extinction drivers under global change. Trends in Ecology and Evolution, 25, 453–460.CrossRefGoogle Scholar
  11. Caballero, S., Islas-Villanueva, V., Tezanos-Pinto, G., Duchene, S., Delgado-Estrella, A., Sanchez-Okrucky, R., & Mignucci-Giannoni, A. A. (2012). Phylogeography, genetic diversity and population structure of common bottlenose dolphins in the Wider Caribbean inferred from analyses of mitochondrial DNA control region sequences and microsatellite loci: conservation and management implications. Animal Conservation, 15, 95–112.CrossRefGoogle Scholar
  12. Carranza, S., Arnold, E. N., & Pleguezuelos, J. M. (2006). Phylogeny, biogeography, and evolution of two Mediterranean snakes, Malpolon monspessulanus and Hemorrhois hippocrepis (Squamata, Colubridae), using mtDNA sequences. Molecular Phylogenetics and Evolution, 40, 532–546.CrossRefPubMedGoogle Scholar
  13. Chapuis, M. P., & Estoup, A. (2007). Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution, 24, 621–631.CrossRefPubMedGoogle Scholar
  14. Clement, M., Posada, D., & Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657.CrossRefPubMedGoogle Scholar
  15. Company, R., Serafim, A., Lopes, B., Cravo, A., Shepherd, T. J., Pearson, G., & Bebianno, M. J. (2008). Using biochemical and isotope geochemistry to understand the environmental and public health implications of lead pollution in the lower Guadiana River, Iberia: a freshwater bivalve study. Science of the Total Environment, 405, 109–119.CrossRefPubMedGoogle Scholar
  16. Crampton, J. S., & Haines, A. J. (1996). Users’ manual for programs HANGLE, HMATCH and HCURVE for the Fourier shape analysis of two-dimensional outlines. Institute of Geological and Nuclear Sciences Science Report, 96, 1–28.Google Scholar
  17. Cuttelod, A., Seddon, M. B., & Neubert, E. (2011). European red list of non-marine molluscs. Luxembourg: Publications Office of the European Union.Google Scholar
  18. Di Rienzo, A., Peterson, A. C., Garcza, J. C., Valdes, A. M., Slatkin, M., & Freimer, N. B. (1994). Mutational processes of simple-sequence repeat loci in human populations. Proceedings of the National Academy of Sciences of the United States of America, 91, 3166–3170.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Drummond, A. J., & Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Drummond, A. J., Ho, S. Y., Phillips, M. J., & Rambaut, A. (2006). Relaxed phylogenetics and dating with confidence. PLoS Biology, 4, 699.CrossRefGoogle Scholar
  21. Earl, D. A., & Von Holdt, B. M. (2012). Structure harvester: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359–361.CrossRefGoogle Scholar
  22. Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611–2620.CrossRefPubMedGoogle Scholar
  23. Fonseca, M. M., Brito, J. C., Paulo, O. S., Carretero, M. A., & Harris, D. J. (2009). Systematic and phylogeographical assessment of the Acanthodactylus erythrurus group (Reptilia: Lacertidae) based on phylogenetic analyses of mitochondrial and nuclear DNA. Molecular Phylogenetics and Evolution, 51, 131–142.CrossRefPubMedGoogle Scholar
  24. Froufe, E., Sobral, C., Teixeira, A., Lopes, A., Sousa, R., Varandas, S., & Lopes-Lima, M. (2013). Development and multiplexing of microsatellite loci for the near threatened freshwater mussel Potomida littoralis (Cuvier, 1798) using 454 sequencing. Aquatic Conservation: Marine and Freshwater Ecosystems, 23, 619–623.CrossRefGoogle Scholar
  25. Froufe, E., Sobral, C., Teixeira, A., Lopes, A., Sousa, R., Varandas, S., Aldridge, D. C., & Lopes-Lima, M. (2014). Genetic diversity of the pan-European freshwater mussel Anodonta anatina (Bivalvia: Unionoida) based on COI: new insights on the genus phylogeny and implications for its conservation. Aquatic Conservation: Marine and Freshwater Ecosystems, 24, 561–574.CrossRefGoogle Scholar
  26. Froufe, E., Gan, H. M., Lee, Y. P., Carneiro, J., Varandas, S., Teixeira, A., Zieritz, A., Sousa, R., & Lopes-Lima. (2016). The Male and Female complete mitochondrial genome sequences of the Endangered Freshwater Mussel Potomida littoralis, (Cuvier, 1798) (Bivalvia: Unionidae). mtDNA Journal. doi: 10.3109/19401736.2015.1074223.Google Scholar
  27. García-París, M., Alcobendas, M., Buckley, D., & Wake, D. B. (2003). Dispersal of viviparity across contact zones in Iberian populations of fire salamanders (Salamandra) inferred from discordance of genetic and morphological traits. Evolution, 57, 129–143.CrossRefPubMedGoogle Scholar
  28. Gaubert, P., Machordom, A., Morales, A., López-Bao, J. V., Veron, G., Amin, M., Barros, T., Basuony, M., Djagoun, C. A. M. S., Do Linh San, E., Fonseca, C., Geffen, E., Ozkurt, S. O., Cruaud, C., Couloux, A., & Palomares, F. (2010). Comparative phylogeography of two African carnivorans presumably introduced into Europe: disentangling natural versus human-mediated dispersal across the Strait of Gibraltar. Journal of Biogeography, 38, 341–358.CrossRefGoogle Scholar
  29. Gómez, A., & Lunt, D. H. (2007). Refugia within refugia: patterns of phylogeographic concordance in the Iberian Peninsula. In S. Weiss & N. Ferrand (Eds.), Phylogeography in southern European refugia: evolutionary perspectives on the origin and conservation of European biodiversity (pp. 155–188). Dordrecht: Springer.CrossRefGoogle Scholar
  30. Goudet, J. (1995). FSTAT: a computer program to calculate F-statistics. Journal of Heredity, 86, 485–486.Google Scholar
  31. Graf, D. L. (2007). Palearctic freshwater mussel (Mollusca: Bivalvia: Unionoida) diversity and the Comparatory Method as a species concept. Proceedings of the Academy of Natural Sciences of Philadelphia, 156, 71–88.CrossRefGoogle Scholar
  32. Graf, D. L., & Cummings, K. S. (2007). Review of the systematics and global diversity of freshwater mussel species (Bivalvia: Unionoida). Journal of Molluscan Studies, 73, 291–314.CrossRefGoogle Scholar
  33. Graf, D. L., & Cummings, K. S. (2015). The freshwater mussels (Unionoida) of the world (and other less consequential bivalves) In MUSSEL Project. Available at Accessed 1 Aug 2015.
  34. Haas, F. (1969). Superfamilia Unionacea. Das Tierreich Vol. 88. De Gruyter, Berlin. [in German].Google Scholar
  35. Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nuclear Acids Symposium Series, 41, 95–98.Google Scholar
  36. Hammer, Ø., & Harper, D. A. T. (2006). PAST, Version 1.57. Available at:
  37. Hedrick, P. W., Parker, K. M., & Lee, R. N. (2001). Using microsatellite and MHC variation to identify species, ESUs, and MUs in the endangered Sonoran topminnow. Molecular Ecology, 10, 1399–1412.CrossRefPubMedGoogle Scholar
  38. Hoeh, W. R., Stewart, D. T., Sutherland, B. W., & Zouros, E. (1996). Multiple origins of gender-associated mitochondrial DNA lineages in bivalves (Mollusca: Bivalvia). Evolution, 50, 2276–2286.CrossRefGoogle Scholar
  39. Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics, 6, 65–70.Google Scholar
  40. Huang, X. C., Rong, J., Liu, Y., Zhang, M. H., Wan, Y., Ouyang, S., Zhou, C. H., & Wu, X. P. (2013). The complete maternally and paternally inherited mitochondrial genomes of the endangered freshwater mussel Solenaia carinatus (Bivalvia: Unionidae) and implications for Unionidae taxonomy. PloS One, 8, e84352.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Husemann, M., Ray, J. W., King, R. S., Hooser, E. A., & Danley, P. D. (2012). Comparative biogeography reveals differences in population genetic structure of five species of stream fishes. Biological Journal of the Linnean Society, 107, 867–885.CrossRefGoogle Scholar
  42. Jakobsson, M., & Rosenberg, N. A. (2007). CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics, 23, 1801–1806.CrossRefPubMedGoogle Scholar
  43. Khalloufi, N., & Boumaïza, M. (2009). First record and biology of Unio gibbus Spengler, 1793 in Tunisia. Biologia, 64, 1–6.CrossRefGoogle Scholar
  44. Khalloufi, N., Toledo, C., Machordom, A., Boumaïza, M., & Araújo, R. (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.CrossRefGoogle Scholar
  45. Kingman, J. (1982). The coalescent. Stochastic Processes and Their Applications, 13, 235–248.CrossRefGoogle Scholar
  46. Krijgsman, W., Hilgen, F. J., Raffi, I., Sierro, F. J., & Wilson, D. S. (1999). Chronology, causes and progression of the Messinian salinity crisis. Nature, 400, 652–655.CrossRefGoogle Scholar
  47. Kristensen, T. K., Stensgaard, A-S., & Appleton, C. (2010). In IUCN Red List of Threatened Species. Version 2015.3. Available at Accessed 15 Oct 2015.
  48. Le Houérou, H. N. (1992). Vegetation and land use in the Mediterranean basin by the year 2050: a prospective study. Climatic Change and the Mediterranean, 1, 175–232.Google Scholar
  49. Li, W. H. (1997). Molecular evolution. Sunderland: Sinauer. 432 pp.Google Scholar
  50. Liu, H. P., Mitton, J. B., & Wu, S. K. (1996). Paternal mitochondrial DNA differentiation far exceeds maternal mitochondrial DNA and allozyme differentiation in the freshwater mussel, Anodonta grandis grandis. Evolution, 50, 952–957.CrossRefGoogle Scholar
  51. Lopes-Lima, M., Teixeira, A., Froufe, E., Lopes, A., Varandas, S., & Sousa, R. (2014). Biology and conservation of freshwater bivalves: past, present and future perspectives. Hydrobiologia, 735, 1–13.CrossRefGoogle Scholar
  52. Lopes-Lima, M., Sousa, R., Teixeira, A., Varandas, S., Riccardi, N., Aldridge, D. C., & Froufe, E. (2016a). Newly developed microsatellite markers for the pan-European duck mussel, Anodonta anatina: revisiting the main mitochondrial lineages. Aquatic Conservation: Marine and Freshwater Ecosystems. doi: 10.1002/aqc.2575. Published online (19 Jun 2015) in Wiley Online Library.Google Scholar
  53. Lopes-Lima, M., Sousa, R., Geist, J., Aldridge, D., Araujo, R., Bergengren, J., Bespalaja, Y., Bodis, E., Burlakova, L., Van Damme, D., Douda, K., Froufe, E., Georgiev, D., Gumpinger, C., Karatayev, A., Kebapci, U., Killeen, I., Lajtner, J., Larsen, B., Lauceri, R, Legakis, A., Lois, S., Lundberg, S., Moorkens, E., Motte, G., Nagel, K-O., Ondina, P., Outeiro, A., Paunovic, M., Prié, V., Von Proschwitz, T., Riccardi, N., Rudzīte, M., Rudzītis, M., Scheder, C., Seddon, M., Sereflisan, H., Simić, V., Sokolova, S., Stoeckl, K., Taskinen, J., Teixeira, A., Thielen, F. Trichkova, T., Varandas, S., Vicentini, H., Zajac, K., Zajac, T. & Zogaris, S. (2016b). Conservation Status of Freshwater Mussels in Europe: state of the art and future challenges. Biological Reviews. doi: 10.1111/brv.12244. Published online (4 Jan 2016) in Wiley Online Library.
  54. Luikart, G., Allendorf, F. W., Cornuet, J. M., & Sherwin, W. B. (1998). Distortion of allele frequency distributions provides a test for recent population bottlenecks. Journal of Heredity, 89, 238–247.CrossRefPubMedGoogle Scholar
  55. Luttikhuizen, P. C., Drent, J., & Baker, A. J. (2003). Disjunct distribution of highly diverged mitochondrial lineage clade and population subdivision in a marine bivalve with pelagic larval dispersal. Molecular Ecology, 12, 2215–2229.CrossRefPubMedGoogle Scholar
  56. Machordom, A., Araujo, R., Toledo, C., Zouros, E., & Ladoukakis, E. D. (2015). Female‐dependent transmission of paternal mtDNA is a shared feature of bivalve species with doubly uniparental inheritance (DUI) of mitochondrial DNA. Journal of Zoological Systematics and Evolutionary Research, 53, 200–204.CrossRefGoogle Scholar
  57. Malausa, T., Gilles, A., Meglécz, E., Blanquart, H., Duthoy, S., Costedoat, C., Dubut, V., Pech, N., Castagnone-Sereno, P., Délye, C., Feau, N., Frey, P., Gauthier, P., Guillemaud, T., Hazard, L., Le Corre, V., Lung-Escarmant, B., Malé, P. J., Ferreira, S., & Martin, J. F. (2011). High-throughput microsatellite isolation through 454 GS-FLX Titanium pyrosequencing of enriched DNA libraries. Molecular Ecology Resources, 11, 638–644.CrossRefPubMedGoogle Scholar
  58. Marko, P. B. (2002). Fossil calibration of molecular clocks and the divergence times of geminate species pairs separated by the Isthmus of Panama. Molecular Biology and Evolution, 19, 2005–2021.CrossRefPubMedGoogle Scholar
  59. Miraldo, A., Hewitt, G. M., Paulo, O. S., & Emerson, B. C. (2011). Phylogeography and demographic history of Lacerta lepida in the Iberian Peninsula: multiple refugia, range expansions and secondary contact zones. BMC Evolutionary Biology, 11, 170.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Mock, K. E., Brim Box, J. C., Chong, J. P., Howard, J. K., Nez, D. A., Wolf, D., & Gardner, R. S. (2010). Genetic structuring in the freshwater mussel Anodonta corresponds with major hydrologic basins in the western United States. Molecular Ecology, 19, 569–591.CrossRefPubMedGoogle Scholar
  61. Morais, P., Rufino, M. M., Reis, J., Dias, E., & Sousa, R. (2013). Assessing the morphological variability of Unio delphinus Spengler, 1783 (Bivalvia: Unionidae) using geometric morphometry. Journal of Molluscan Studies, 80, 17–23.Google Scholar
  62. Naimo, T. J., Damschen, E. D., Rada, R. G., & Monroe, E. M. (1998). Nonlethal evaluation of the physiological health of unionid mussels: methods for biopsy and glycogen analysis. Journal of the North American Benthological Society, 17, 121–128.CrossRefGoogle Scholar
  63. Novais, A., Dias, E., & Sousa, R. (2016). Inter and intraspecific variation of carbon and nitrogen stable isotopes ratios in freshwater bivalves. Hydrobiologia, 765, 149–158.Google Scholar
  64. Ortmann, A. E. (1912). Notes upon the families and genera of the najades. Annals of the Carnegie Museum, 8, 222–365.Google Scholar
  65. Piry, S., Luikart, G., & Cornuet, J. M. (1999). BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity, 90, 502–503.CrossRefGoogle Scholar
  66. Plazzi, F., & Passamonti, M. (2010). Towards a molecular phylogeny of Mollusks: Bivalves’ early evolution as revealed by mitochondrial genes. Molecular Phylogenetics and Evolution, 57, 641–657.CrossRefPubMedGoogle Scholar
  67. Posada, D. (2008). JModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.CrossRefPubMedGoogle Scholar
  68. Prié, V., & Puillandre, N. (2014). Molecular phylogeny, taxonomy, and distribution of French Unio species (Bivalvia, Unionidae). Hydrobiologia, 735, 95–110.CrossRefGoogle Scholar
  69. Prié, V., Puillandre, N., & Bouchet, P. (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, 08.CrossRefGoogle Scholar
  70. Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.PubMedPubMedCentralGoogle Scholar
  71. Rambaut, A., Suchard, M. A., Xie, D., & Drummond, A. J. (2014). Tracer v1.6, Available from
  72. Ramos-Onsins, S. E., & Rozas, J. (2002). Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution, 12, 2092–2100.CrossRefGoogle Scholar
  73. Rasband, W. (2008). ImageJ. Image processing and analysis in Java. Bethesda, MD: National Institutes of Health, USA. Available from
  74. Raymond, M., & Rousset, F. (1995). GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248–249.Google Scholar
  75. Reis, J., Machordom, A., & Araujo, R. (2013). Morphological and molecular diversity of unionidae (Mollusca, Bivalvia) from Portugal. Graellsia, 69, 17–36.Google Scholar
  76. Renard, E., Bachmann, V., Cariou, M. L., & Moreteau, C. (2000). Morphological and molecular differentiation of invasive freshwater species of the genus Corbicula (Bivalvia, Corbiculidea) suggest the presence of three taxa in French rivers. Molecular Ecology, 9, 2009–2016.CrossRefPubMedGoogle Scholar
  77. Riccardi, N., Froufe, E., Lopes-Lima, M., & Mazzoli, C. (2016). When and how? Freshwater mussel recolonization in Lake Orta? Journal of Limnology (Accepted, 2015).Google Scholar
  78. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., & Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.CrossRefPubMedPubMedCentralGoogle Scholar
  79. Rosenberg, N. A. (2004). DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes, 4, 137–138.CrossRefGoogle Scholar
  80. Sambrook, J., Fritsch, E. F., & Maniatis, T. (1989). Molecular cloning: a laboratory manual. New York: Cold Harbor Spring Press.Google Scholar
  81. Schmitt, T., Hewitt, G. M., & Müller, P. (2006). Disjunct distributions during glacial and interglacial periods in mountain butterflies: Erebia epiphron as an example. Journal of Evolutionary Biology, 19, 108–113.CrossRefPubMedGoogle Scholar
  82. Sousa, R., Antunes, C., & Guilhermino, L. (2007). Species composition and monthly variation of the Molluscan fauna in the freshwater subtidal area of the River Minho estuary. Estuarine, Coastal and Shelf Science, 75, 90–100.CrossRefGoogle Scholar
  83. Sousa, R., Dias, S., Guilhermino, L., & Antunes, C. (2008). Minho River tidal freshwater wetlands: threats to faunal biodiversity. Aquatic Biology, 3, 237–250.CrossRefGoogle Scholar
  84. Sousa, R., Varandas, S., Teixeira, A., Ghamizi, M., Froufe, E., & Lopes-Lima, M. (2016). Pearl mussels (Margaritifera marocana) in Morocco: conservation status of the rarest bivalve in African fresh waters. Science of the Total Environment, 547, 405–412.Google Scholar
  85. Steinfartz, S., Veith, M., & Tautz, D. (2000). Mitochondrial sequence analysis of Salamandra taxa suggests old splits of major lineages and postglacial recolonizations of Central Europe from distinct source populations of Salamandra salamandra. Molecular Ecology, 9, 397–410.CrossRefPubMedGoogle Scholar
  86. Strayer, D. L. (2008). Freshwater mussel ecology: a multifactor approach to distribution and abundance. London: University of California Press.CrossRefGoogle Scholar
  87. Strayer, D. L., Downing, J. A., Haag, W. R., King, T. L., Layzer, J. B., Newton, T. J., & Nichols, S. J. (2004). Changing perspectives on pearly mussels, North America's most imperilled animals. BioScience, 54, 429–439.CrossRefGoogle Scholar
  88. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  89. Van Damme, D. (1984). The freshwater Mollusca of northern Africa: distribution, biogeography and palaeoecology. Dordrecht: Dr. W. Junk Publishers. 164 pp.Google Scholar
  90. Van Damme, D. (2011). Unio pictorum. In IUCN Red List of Threatened Species. Version 2015.3. Available from Accessed 15 Oct 2015.
  91. Van Damme, & Ghamizi. (2010). Unio foucauldianus. In IUCN Red List of Threatened Species. Version 2015.3. Available from Accessed 15 Oct 2015.
  92. Van Oosterhout, C., Hutchinson, W. F., Wills, D. P., & Shipley, P. (2004). MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535–538.CrossRefGoogle Scholar
  93. Walker, J. M., Curole, J. P., Wade, D. E., Chapman, E. G., Bogan, A. E., & Watters, G. T. (2006). Taxonomic distribution and phylogenetic utility of gender-associated mitochondrial genomes in the Unionoida (Bivalvia). Malacologia, 48, 265–282.Google Scholar
  94. Walker, J. M., Bogan, A. E., Bonfiglio, E. A., Campbell, D. C., Christian, A. D., Curole, J. P., Harris, J. L., Wojtecki, R. J., & Hoeh, W. R. (2007). Primers for amplifying the hypervariable, male-transmitted COII-COI junction region in amblemine freshwater mussels (Bivalvia: Unionoidea: Ambleminae). Molecular Ecology Notes, 7, 489–491.CrossRefGoogle Scholar
  95. Weir, B. S., & Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358–1370.Google Scholar
  96. Zieritz, A., & Aldridge, D. C. (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.CrossRefGoogle Scholar
  97. Zieritz, A., Hoffman, J. I., Amos, H. W., & Aldridge, D. C. (2010). Phenotypic plasticity and genetic isolation-by-distance in the freshwater mussel Unio pictorum (Mollusca: Unionidae). Evolutionary Ecology, 24, 923–938.CrossRefGoogle Scholar
  98. Zouros, E., Ball, A. O., Saavedra, C., & Freeman, K. R. (1994a). Mitochondrial DNA inheritance. Nature, 368, 8–18.CrossRefGoogle Scholar
  99. Zouros, E., Ball, A. O., Saavedra, C., & Freeman, K. R. (1994b). An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proceedings of the National Academy of Sciences of the United States of America, 91, 7463–7467.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2016

Authors and Affiliations

  • Elsa Froufe
    • 1
  • Duarte V. Gonçalves
    • 2
    • 3
    • 4
  • Amílcar Teixeira
    • 5
  • Ronaldo Sousa
    • 1
    • 6
  • Simone Varandas
    • 7
  • Mohamed Ghamizi
    • 8
  • Alexandra Zieritz
    • 9
  • Manuel Lopes-Lima
    • 1
  1. 1.CIIMAR/CIMAR-Interdisciplinary Centre of Marine and Environmental ResearchUniversity of PortoPortoPortugal
  2. 2.CIBIO/InBIO-Centro de Investigação em Biodiversidade e Recursos Genéticos da Universidade do PortoVairãoPortugal
  3. 3.Departamento de Biologia da Faculdade de Ciências da Universidade do PortoPortoPortugal
  4. 4.Institute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra)BarcelonaSpain
  5. 5.CIMO-ESA-IPB-Mountain Research Centre, School of AgriculturePolytechnic Institute of BragançaBragançaPortugal
  6. 6.CBMA-Centre of Molecular and Environmental Biology, Department of BiologyUniversity of MinhoBragaPortugal
  7. 7.CITAB-UTAD-Centre for Research and Technology of Agro-Environment and Biological Sciences, Forestry DepartmentUniversity of Trás-os-Montes and Alto DouroVila RealPortugal
  8. 8.Muséum d’Histoire Naturelle de Marrakech, Faculté des SciencesUniversité Cadi AyyadSemlaliaMorocco
  9. 9.School of GeographyUniversity of Nottingham Malaysia CampusJalan BrogaMalaysia

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