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Type: Article
Published: 2020-07-20
Page range: 457–490
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A new species of freshwater mussel in the genus Popenaias Frierson, 1927, from the Gulf coastal rivers of central Mexico (Bivalvia: Unionida: Unionidae) with comments on the genus

Natural Resources Institute, Texas A&M University, College Station, Texas, USA Daniel P. Haerther Center for Conservation and Research, John G. Shedd Aquarium, Chicago, IL, USA
Illinois Natural History Survey, Prairie Research Institute, University of Illinois, Champaign, Illinois, USA
Illinois Natural History Survey, Prairie Research Institute, University of Illinois, Champaign, Illinois, USA
Environmental Science Center, Laredo Community College, Laredo, Texas, USA
Wetland and Aquatic Research Center, U.S. Geological Survey, Gainesville, Florida, USA
Biology Department, Baylor University, Waco, Texas, USA.
Natural Resources Institute, Texas A&M University, College Station, Texas, USA
Mollusca Fourier shape morphometrics biodiversity phylogenetics species delimitation endemic species


The Gulf coastal drainages of central Mexico are a faunal transition zone between North and South America and harbor a unique assemblage of freshwater mussels (Bivalvia: Unionida). However, little information is available regarding the taxonomy, distribution, and evolutionary history of the Mexican mussel fauna due to limited sampling over the last 100 years. To address these knowledge gaps, we evaluated species-level diversity in the genus Popenaias Frierson, 1927, in Mexican Gulf coastal drainages as part of a larger effort to inform conservation efforts for members of this genus both in Mexico and the United States of America. Based on our analyses, we describe Popenaias berezai n. sp. from the Río Valles of the Río Pánuco basin, San Luis Potosí, Mexico. We also provide presumptive distributional range, phylogenetic structure, and molecular and morphological diagnoses of the new species and provide comments on the other species currently in Popenaias. Our findings highlight the high levels of endemism among freshwater mussels in Mexican Gulf coastal drainages and will help guide impending conservation actions for P. popeii, which is listed as “endangered” in the United States.



  1. Audzijonyte, A. & Vrijenhoek, R.C. (2010) Three nuclear genes for phylogenetic, SNP and population genetic studies of molluscs and other invertebrates. Molecular Ecology Resources, 10 (1), 200–204.

    Binney, W.G. (1858) The complete writings of Thomas Say on the conchology of the United States. H. Bailliere Co., New York, 252 pp.

    Bogan, A.E. (1996) Popenaias popeii. The IUCN Red List of Threatened Species, 1996, e.T17992A7641578.

    Bogan, A.E. & Roe, K.J. (2008) Freshwater bivalve (Unioniformes) diversity, systematics, and evolution: status and future directions. Journal of the North American Benthological Society, 27 (2), 349–369.

    Burch, J.B. (1975) Freshwater Unionacean Clams (Mollusca, Pelecypoda) of North America. Malacological Publications, Hamburg, Michigan, 204 pp.

    Burlakova, L.E., Campbell, D. & Karatayev, A.Y. (2019) Status of rare endemic species: molecular phylogeny, distribution and conservation of freshwater molluscs Truncilla macrodon and Truncilla cognata in Texas. Malacologia, 62 (2), 345–363.

    Campbell, D.C. & Lydeard, C. (2012) The genera of Pleurobemini (Bivalvia: Unionidae: Ambleminae). American Malacological Bulletin, 30 (1), 19–38.

    Campbell, D.C., Serb, J.M., Buhay, J.E., Roe, K.J., Minton, R.L. & Lydeard, C. (2005) Phylogeny of North American amblemines (Bivalvia: Unionoida): prodigious polyphyly proves pervasive across genera. Invertebrate Biology, 124 (2), 131–164.

    Carman, S.M. (2007) Texas hornshell Popenaias popeii recovery plan. New Mexico Department of Game and Fish, Santa Fe, 57 pp.

    Chapman, E.G., Gordon, M.E., Walker, J.M., Lang, B.K., Campbell, D., Watters, G.T., Curolé, J.P., Piontkivska, H. & Hoeh, W.R. (2008) Evolutionary relationships of Popenaias popeii and the early evolution of lampsiline bivalves (Unionidae): phylogenetic analyses of DNA and amino acid sequences from F and M mitochondrial genomes. Malacologia, 50 (1–2), 303–318.

    Crosse, H. & Fischer, P. (1893) Diagnoses molluscorum novorum, Republicae Mexicanae incolarum. Journal de Conchyliologie, 41, 293–297.

    De la Maza-Benignos, M., Ornelas-García, C.P., Lozano-Vilano, M. de L., García-Ramírez, M.E. & Doadrio, I. (2014) Phylogeographic analysis of genus Herichthys (Perciformes: Cichlidae), with descriptions of Nosferatu new genus and H. tepehua n. sp. Hydrobiologia, 748 (1), 201–231.

    Fischer, P. & Crosse, H. (1894) Études sur les mollusques terrestres et fluviatiles du Mexique et du Guatemala. Mission Scientifique au Mexique et dans l’Amérique Central, Recherches Zoologiques, 2 (15), 489–576.

    Frierson, L.S. (1927) A Classification and Annotated Check List of the North American Naiades. Baylor University Press, Waco, Texas, 111 pp.

    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 (4), 291–314.

    Haag, W.R. (2012) North American Freshwater Mussels: Natural History, Ecology, and Conservation. Cambridge University Press, Cambridge, 505 pp.

    Haas, F. (1929) Bemerkungen über mittelamerikanische Najaden. Senckenbergiana, 11, 310–344.

    Haas, F. (1969) Superfamilia Unionacea. Das Tierrich, Berlin, 88, 1–663.

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

    Hart, M.A., Miller, T.D. & Randklev, C.R. (2019) Salinity tolerance of a rare and endangered unionid mussel, Popenaias popeii (Texas Hornshell) and its implications for conservation and water management. Ecotoxicology and Environmental Safety, 170, 1–8.

    Heard, W.H. & Guckert, R.H. (1970) A re-evaluation of the recent Unionacea (Pelecypoda) of North America. Malacologia, 10 (2), 333–355.

    Helaers, R. & Milinkovitch, M.C. (2010) MetaPIGA v2.0: maximum likelihood large phylogeny estimation using the metapopulation genetic algorithm and other stochastic heuristics. BMC Bioinformatics, 11, 379.

    Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q. & Vinh, L.S. (2018a) UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 35 (2), 518–522.

    Hoang, D.T., Vinh, L.S., Flouri, T., Stamatakis, A., von Haeseler, A. & Minh, B.Q. (2018b) MPBoot: fast phylogenetic maximum parsimony tree inference and bootstrap approximation. BMC Evolutionary Biology, 18 (1), 11.

    Howells, R.G., Neck, R.W. & Murray, H.D. (1996) Freshwater Mussels of Texas. Texas Parks and Wildlife Department, Austin, Texas, 218 pp.

    Hudson, P.F., Hendrickson, D., Benke, A.C., Varela-Romero, A., Rodiles-Hernández, R. & Minckley, W.L. (2005) Rivers of Mexico. In: Benke, A.C. & Cushing, C.E. (Eds.), Rivers of North America. Elsevier Academic Press, Burlington, Massachusetts, pp. 1030–1084.

    Inoue, K., Harris, J.L., Robertson, C.R., Johnson, N.A. & Randklev, C.R. (2019) A comprehensive approach uncovers hidden diversity in freshwater mussels (Bivalvia: Unionidae) with the description of a novel species. Cladistics, 36 (1), 88–113.

    Inoue, K., Hayes, D.M., Harris, J.L., Johnson, N.A., Morrison, C.L., Eackles, M.S., King, T.L., Jones, J.W., Hallerman, E.M., Christian, A.D. & Randklev, C.R. (2018) The Pleurobemini (Bivalvia : Unionida) revisited: molecular species delineation using a mitochondrial DNA gene reveals multiple conspecifics and undescribed species. Invertebrate Systematics, 32 (3), 689–702.

    Inoue, K., Lang, B.K. & Berg, D.J. (2013) Development and characterization of 20 polymorphic microsatellite markers for the Texas hornshell, Popenaias popeii (Bivalvia: Unionidae), through next-generation sequencing. Conservation Genetics Resources, 5 (1), 195–198.

    Inoue, K., Lang, B.K. & Berg, D.J. (2015) Past climate change drives current genetic structure of an endangered freshwater mussel species. Molecular Ecology, 24 (8), 1910–1926.

    Inoue, K., Levine, T.D., Lang, B.K. & Berg, D.J. (2014) Long-term mark-and-recapture study of a freshwater mussel reveals patterns of habitat use and an association between survival and river discharge. Freshwater Biology, 59 (9), 1872–1883.

    Iwata, H. & Ukai, Y. (2002) SHAPE: a computer program package for quantitative evaluation of biological shapes based on elliptic Fourier descriptors. The Journal of Heredity, 93 (5), 384–385.

    Johnson, R.I. (1956) The types of Naiades (Mollusca: Unionidae) in the Museum of Comparative Zoology. Bulletin of the Museum of Camparative Zoology, 115 (4), 102–142.

    Johnson, R.I. (1974) Lea’s unionid types or recent and fossil taxa of Unionacea and Mutelacea introduced by Isaac Lea, including the location of all the extant types. Museum of Comparative Zoology, Harvard University, Special Occasional Publication, 2, 1–159.

    Johnson, R.I. (1979) The types of Unionacea (Mollusca: Bivalvia) in the Museum of Zoology, University of Michigan. Malacological Review, 12 (1–2), 29–36.

    Johnson, R.I. (1999) Unionidae of the Rio Grande (Rio Bravo del Norte) system of Texas and Mexico. Occasional Papers on Mollusks, 6, 1–66.

    Johnson, R.I. & Baker, H.B. (1973) The types of Unionacea (Mollusca: Bivalvia) in the Academy of Natural Science of Philadelphia. Proceedings of the Academy of Natural Sciences of Philadelphia, 125, 145–186.

    Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14 (6), 587–589.

    Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version7: Improvements in performance and usability. Molecular Biology and Evolution, 30 (4), 772–780.

    Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33 (7), 1870–1874.

    Lamarck, J. (1819) Histoire Naturelle des Animaux sans vertèbres. Vol. 6. Verdière, Libraire, Paris, 343 pp.

    Lea, I. (1831) Observations on the Naïades, and descriptions of new species of that and other families. Transactions of the American Philosophical Society, 4, 63–121.

    Lea, I. (1841) Continuation of paper on fresh water and land shells. Proceedings of the American Philosophical Society, 2, 30–34.

    Lea, I. (1857) Description of six new species of fresh water and land shells of Texas and Tamaulipas, from the collection of the Smithsonian Institution. Proceedings of the Academy of Natural Sciences of Philadelphia, 9, 101–102.

    Lea, I. (1858) Description of four new fresh-water molluscs, from the Isthmus of Darien and Honduras. Proceedings of the Academy of Natural Sciences of Philadelphia, 10, 118.

    Lea, I. (1859) Descriptions of twenty-one new species of exotic Unionidæ. Proceedings of the Academy of Natural Sciences of Philadelphia, 11, 151–154.

    Lea, I. (1860) New Unionidæ of the United States and northern Mexico. Journal of the Academy of Natural Sciences, 4, 327–374.

    Lea, I. (1870) A synopsis of the family Unionidae. Henry C. Lea, Philadelphia, Pennsylvania, 184 pp.

    Lopes-Lima, M., Bolotov, I.N., Do, V.T., Aldridge, D.C., Fonseca, M.M., Gan, H.M., Gofarov, M.Y., Kondakov, A.V., Prie, V., Sousa, R., Varandas, S., Vikhrev, I.V., Teixeira, A., Wu, R.W., Wu, X., Zieritz, A., Froufe, E. & Bogan, A.E. (2018) Expansion and systematics redefinition of the most threatened freshwater mussel family, the Margaritiferidae. Molecular Phylogenetics and Evolution, 127, 98–118.

    Lopes-Lima, M., Froufe, E., Do, V.T., Ghamizi, M., Mock, K.E., Kebapci, U., Klishko, O., Kovitvadhi, S., Kovitvadhi, U., Paulo, O.S., Pfeiffer, J.M., III, Raley, M., Riccardi, N., Sereflisan, H., Sousa, R., Teixeira, A., Varandas, S., Wu, X., Zanatta, D.T., Zieritz, A. & Bogan, A.E. (2017) Phylogeny of the most species-rich freshwater bivalve family (Bivalvia: Unionida: Unionidae): Defining modern subfamilies and tribes. Molecular Phylogenetics and Evolution, 106, 174–191.

    Luebke, C.M. & Graf, D.L. (2013) Curation of the Daniel J. Bereza collection of freshwater mollusks at the Smithsonian National Museum of Natural History: Phase I. In: University of Wisconsin Stevens-Point College of Letters and Sciences Undergraduate Research Symposium. University of Wisconsin Stevens-Point College, Stevens Point, Wisconsin, pp. 1–62.

    Lydeard, C., Mulvey, M. & Davis, G.M. (1996) Molecular systematics and evolution of reproductive traits of North American freshwater Unionacean mussels (Mollusca: Bivalvia) as inferred from 16S rRNA gene sequences. Philosophical Transactions: Biological Sciences, 351 (1347), 1593–1603.

    Von Martens, E. (1890–1901) Biologia Centrali-Americana, Land and freshwater Mollusca. Published for the editors by R. H. Porter, London, 675 pp.

    Miller, R.R. & Smith, M.L. (1986) Origin and geography of the fishes of Central Mexico. In: Hocutt, C.H. & Wiley, E.O. (Eds.), The zoogeography of North American freshwater fishes. John Wiley & Sons, Inc., New York, pp. 487–517.

    Morelet, A. (1849) Testacea Novissima Insulæ Cubanæ et Americæ Centralis 1. J.-B. Baillière, Paris, 31 pp.

    Nguyen, L.T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32 (1), 268–274.

    Ortmann, A.E. (1912) Notes upon the families and genera of the najades. Annals of the Carnegie Museum, 8 (2), 222–365.

    Pfeiffer, J.M., Atkinson, C.L., Sharpe, A.E., Capps, K.A., Emery, K.F. & Page, L.M. (2019a) Phylogeny of Mesoamerican freshwater mussels and a revised tribe-level classification of the Ambleminae. Zoologica Scripta, 48 (1), 106–117.

    Pfeiffer, J.M., Breinholt, J.W. & Page, L.M. (2019b) Unioverse: A phylogenomic resource for reconstructing the evolution of freshwater mussels (Bivalvia, Unionoida). Molecular Phylogenetics and Evolution, 137, 114–126.

    Pfeiffer, J.M., Sharpe, A.E., Johnson, N.A., Emery, K.F. & Page, L.M. (2018) Molecular phylogeny of the Neartic and Mesoamerican freshwater mussel genus Megalonaias. Hydrobiologia, 811 (1), 139–151.

    Pilsbry, H.A. (1910) Unionidae of the Panuco River system, Mexico. Proceedings of the Academy of Natural Sciences of Philadelphia, 61 (3), 532–539.

    Pilsbry, H.A. & Hinkley, A.A. (1910) Melaniidae of the Panuco River system, Mexico. Proceedings of the Academy of Natural Sciences of Philadelphia, 61 (3), 519–531.

    Rafinesque, C.S. (1820) Monographie des coquilles bivalves fluviatiles de la Riviére Ohio, contenant douze genres et soixante-huit espèces. Annales générales des Sciences Physiques, Bruxelles, 5 (5), 287–322.

    Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systems Biology, 67 (5), 901–904.

    Randklev, C.R., Miller, T., Hart, M., Morton, J., Johnson, N.A., Skow, K., Inoue, K., Tsakiris, E.T., Oetker, S., Smith, R., Robertson, C. & Lopez, R. (2018) A semi-arid river in distress: Contributing factors and recovery solutions for three imperiled freshwater mussels (Family Unionidae) endemic to the Rio Grande basin in North America. Science of the Total Environment, 631–632, 733–744.

    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 (3), 539–542.

    Sabaj, M.H. (2019) Standard symbolic codes for institutional resource collections in herpetology and ichthyology: An Online Reference. Version 7.1. 21 March 2019. American Society of Ichthyologists and Herpetologists, Washington, D.C. Electronically accessible. Available from: (accessed 17 June 2020)

    Saghai-Maroof, M.A., Soliman, K.M., Jorgensen, R.A. & Allard, R.W. (1984) Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proceedings of the National Academy of Sciences of the United States of America, 81, 8014–8018.

    Say, T. (1831) New terrestrial and fluviatile shells of North America. (cont.). The Disseminator. Series 2. 1 (29). New Harmony, Indiana, no pagination.

    Schönhuth, S., Doadrio, I., Dominguez-Dominguez, O., Hillis, D.M. & Mayden, R.L. (2008) Molecular evolution of southern North American Cyprinidae (Actinopterygii), with the description of the new genus Tampichthys from central Mexico. Molecular Phylogenetics and Evolution, 47 (2), 729–756.

    Seehausen, O. & Wagner, C.E. (2014) Speciation in Freshwater Fishes. Annual Review of Ecology, Evolution, and Systematics, 45 (1), 621–651.

    Simpson, C.T. (1900) Synopsis of the naiades, or pearly fresh-water mussels. Proceedings of the United State National Museum, 22, 501–1044.

    Simpson, C.T. (1914) A descriptive catalogue of the naiades, or pearly fresh-water mussels. Parts I–III. Bryant Walker, Detroit, Michigan, 1540 pp.

    Singley, J.A. (1893) Contributions to the Natural History of Texas. Part I. Mollusca: A preliminary list of the land, fresh water, and marine Mollusca of Texas. Geological Survey of Texas, 4th Annual Report, 299–343. [1892]

    Smith, C.H., Johnson, N.A., Inoue, K., Doyle, R.D. & Randklev, C.R. (2019) Integrative taxonomy reveals a new species of freshwater mussel, Potamilus streckersoni sp. nov. (Bivalvia: Unionidae): implications for conservation and management. Systematics and Biodiversity, 17 (4), 331–348.

    Sowerby, G.B. (1868) Genus Unio. Conchologica Iconica, 16, 61–96.

    Tanabe, A.S. (2011) Kakusan4 and Aminosan: Two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Molecular Ecology Resources, 11 (5), 914–921.

    Texas Parks and Wildlife Department (2020) Threatened and endangered nongame species. Chapter 65. In: Wildlife Subchapter G. Rule §65.175. Texas Secretary of State, Austin, Texas. [Adopted rules]

    Thiele, J. (1934) Scaphopoda; Bivalvia; Cephalopoda. In: Handbuch der systematischen Weichtierkunde. Teil 3. Gustav Fischer, Jena, pp. 779–1022.

    Tristram, H.B. (1863) Supplemental catalogue of terrestrial and fluviatile mollusks collected in Guatemala by O. Salvin, Esq., M.A., F.Z.S. Proceedings of the Zoological Soceity of London, 1863, 411–414.

    Turgeon, D.D., Bogan, A.E., Coan, E.V., Emerson, W.K., Lyons, W.G., Pratt, W.L., Roper, C.F.E., Scheltema, A., Thompson, F.G. & Williams, J.D. (1988) Common and Scientific Names of Aquatic Invertebrates from the United States and Canada: Mollusks. American Fisheries Society Special Publication 16. American Fisheries Society, Bethesda, Maryland, 277 pp.

    Turgeon, D.D., Quinn, J.F., Jr., Bogan, A.E., Coan, E.V., Hochberg, F.G., Jr., Lyons, W.G., Mikkelsen, P.M., Neves, R.J., Roper, C.F.E., Rosenberg, G., Roth, B., Scheltema, A., Thompson, F.G., Vecchione, M. & Williams, J.D. (1998) Common and Scientific Names of Aquatic Invertebrates from the United States and Canada: Mollusks. American Fisheries Society Special Publication 26. 2nd Edition. American Fisheries Society, Bethesda, Maryland, 528 pp.

    USFWS (US Fish and Wildlife Service) (2018) Endangered and threatened wildlife and plants; endangered species status for Texas hornshell. Federal Register, 83 (28), 5720–5735.

    Walker, J.M., Curolé, J.P., Wade, D.E., Chapman, E.G., Bogan, A.E., Watters, G.T. & Hoeh, W.R. (2006) Taxonomic distribution and phylogenetic utility of gender-associated mitochondrial genomes in the Unionoida (Bivalvia). Malacologia, 48 (1–2), 265–282.

    Williams, J.D., Bogan, A.E., Butler, R.S., Cummings, K.S., Garner, J.T., Harris, J.L., Johnson, N.A. & Watters, G.T. (2017) A revised list of the freshwater mussels (Mollusca: Bivalvia: Unionida) of the United States and Canada. Freshwater Mollusk Biology and Conservation, 20 (2), 33–58.

    Williams, J.D., Warren, M.L. Jr., Cummings, K.S., Harris, J.L. & Neves, R.J. (1993) Conservation status of freshwater mussels of the United States and Canada. Fisheries, 18 (9), 6–22.<0006:CSOFMO>2.0.CO;2

    Zanatta, D.T. & Murphy, R.W. (2006) Evolution of active host-attraction strategies in the freshwater mussel tribe Lampsilini (Bivalvia: Unionidae). Molecular Phylogenetics and Evolution, 41 (1), 195–208.