Abstract
The Caspian Sea as the largest continental water body in the world is known for its comparably high levels of biodiversity and endemism, also in mollusks. The evolution of a euryhaline taxon of cardiid bivalves, the Lymnocardiinae of the Ponto-Caspian region, remains unclear today. We studied material from the whole recent range of Lymnocardiinae (i.e., the Caspian, the Azov, and the Black Seas) using a LSU rDNA phylogeny aiming at (a) testing the monophyly of Lymnocardiinae and (b) determining the phylogenetic relationships within Cardiidae. Lymnocardiinae s.str. were monophyletic, i.e., a distinct group that included species of Hypanis, Didacna, and Monodacna. Lymnocardiinae as often understood, i.e., including Cerastoderma, are not monophyletic in our analysis and Cerastoderma should thus be transferred to Cardiinae. The Lymnocardiinae s.str. had a shallow tree topology and were poorly resolved. No clearcut biogeographical pattern could be derived from the phylogeny, i.e., species stemming from respective Ponto-Caspian regions, do not necessarily cluster together. We discuss a scenario of the evolutionary history and biogeographical (as well as taxonomic) implications. Given the complex history of the Ponto-Caspian region and the Caspian Sea in particular, the Lymnocardiinae would represent an interesting study object for addressing the consequences of environmental changes on biotic evolution at various spatial and temporal scales.
Similar content being viewed by others
References
Albrecht, C., K. Kuhn & B. Streit, 2007. A molecular phylogeny of Planorboidea (Gastropoda, Pulmonata): insights from enhanced taxon sampling. Zoologica Scripta 36: 27–39.
Anistratenko, V. V., I. A. Khaliman & O. Y. Anistratenko, 2011. The Molluscs of the Sea of Azov. Naukova dumka, Kiev, 173 pp (in Russian with English abstract).
Bahr, A., F. Lamy, H. Arz, H. Kuhlmann & G. Wefer, 2005. Late glacial to Holocene climate and sedimentation history in the NW Black Sea. Marine Geology 214: 309–322.
Birstein, Y. A., Y. A. Vinogradova, L. G. Kondakova, M. S. Kun, T. V. Astakchova & N. N. Romanova, 1968. Atlas of the Invertebrates of the Caspian Sea. Izvetiya Pischevaya Promyshlennost’, Moscow: 415 pp (in Russian).
Bogan, A. E., 2008. Global diversity of freshwater mussels (Mollusca, Bivalvia) in freshwater. Hydrobiologia 595: 139–147.
Bouchet, P., J. P. Rocroi, R. Bieler, J. G. Carter & E. V. Coan, 2010. Nomenclator of bivalve families with a classification of bivalve families. Malacologia 52: 1–184.
Chepalyga, A. L., 2007. The late glacial great flood in the Ponto-Caspian basin. In Yanko-Hombach, V., A. S. Gilbert, N. Panin & P. M. Dolukhanov (eds), The Black Sea Flood Question: Changes in Coastline, Climate, and Human Settlement. Springer, Netherlands: 119–148.
Cohen, A. S., 2012. Scientific drilling and biological evolution in ancient lakes: lessons learned and recommendations for the future. Hydrobiologia 68: 3–25.
Dayrat, B., M. Conrad, S. Balayan, T. R. White, C. Albrecht, R. Golding, S. R. Gomes, M. G. Harasewych & A. M. de Frias Martins, 2011. Phylogenetic relationships and evolution of pulmonate gastropods (Mollusca): new insights from increased taxon sampling. Molecular Phylogenetics and Evolution 59: 425–437.
DeBoer, T. S., M. D. Subia, M. V. Erdmann, K. Kovitvongsa & P. H. Barber, 2008. Phylogeography and limited genetic connectivity in the endangered boring giant clam across the Coral Triangle. Conservation Biology 22: 1255–1266.
Dreyer, H. & G. Steiner, 2006. The complete sequences and gene organization of the mitochondrial genomes of the heterodont bivalves Acanthocarida tuberculata and Hiatella arctica—and the first record for a putative Atpase subunit 8 gene in marine bivalves. Frontiers in Zoology 3: 13.
Dumont, H. J., 1998. The Caspian Lake: history, biota, structure, and function. Limnology and Oceanography 43: 44–52.
Dumont, H. J., 2000. Endemism in the Ponto-Caspian fauna, with special emphasis on the Onychopoda (Crustacea). Advances in Ecological Research 31: 181–196.
Esin, N. V., V. Yanko-Hombach & O. N. Kukleva, 2010. Mathematical model of the Late Pleistocene and Holocene transgressions of the Black Sea. Quaternary International 225: 180–190.
Filippov, A. & F. Riedel, 2009. The late Holocene mollusc fauna of the Aral Sea and its biogeographical and ecological interpretation. Limnologica 39: 67–85.
Geary, D. H., I. Magyar & P. Müller, 2000. Ancient Lake Pannon and its endemic molluscan fauna (Central Europe; Mio-Pliocene). Advances in Ecological Research 31: 463–482.
Geary, D. H., G. Hunt, I. Magyar & H. Schreiber, 2010. The paradox of gradualism: phyletic evolution in two lineages of lymnocardiid bivalves (Lake Pannon, central Europe). Paleobiology 36: 592–614.
Grigorovich, I. A., T. W. Therriault & H. J. MacIsaac, 2003. History of aquatic invertebrate invasions in the Caspian Sea. Biological Invasions 5: 103–115.
Harzhauser, M. & O. Mandic, 2008. Neogene lake systems of Central and South-Eastern Europe: faunal diversity, gradients and interrelations. Palaeogeography, Palaeoclimatology, Palaeoecology 260: 417–434.
Harzhauser, M., O. Mandic, A. K. Kern, W. E. Piller, T. A. Neubauer, C. Albrecht & T. Wilke, 2013. Explosive demographic expansion by dreissenid bivalves as a possible result of astronomical forcing. Biogeosciences Discussions 10: 12009–12027.
Hoogendoorn, R. M., J. F. Boels, S. B. Kroonenberg, M. D. Simmons, E. Aliyeva, A. D. Babazadeh & D. Huseynov, 2005. Development of the Kura delta, Azerbaijan; a record of Holocene Caspian sea-level changes. Marine Geology 222–223: 359–380.
Hudson, S. M., C. L. Johnson, M. A. Efendiyeva, H. D. Rowe, A. A. Feyzuallayev & C. S. Aliyev, 2008. Stratigraphy and geochemical characterization of the Oligocene–Miocene Maikop series: implications for the paleogeography of Eastern Azerbaijan. Tectonophysics 451: 40–55.
Ivanova, E. V., I. O. Murdmaa, A. L. Chepalyga, T. M. Cronin, I. V. Pasechnik, O. V. Levchenko, S. S. Howe, A. V. Manushkina & E. A. Platonova, 2007. Holocene sea-level oscillations and environmental changes on the Eastern Black Sea shelf. Palaeogeography, Palaeoclimatology, Palaeoecology 246: 228–259.
Kerey, E., E. Meriç, C. Tunoğlu, G. Kelling, R. L. Brenner & A. U. Doğan, 2004. Black Sea–Marmara Sea Quaternary connections: new data from the Bosphorus, Istanbul, Turkey. Palaeogeography, Palaeoclimatology, Palaeoecology 204: 277–295.
Kirkendale, L., 2009. Their day in the sun: molecular phylogenetics and origin of photosymbiosis in the ‘other’ group of photosymbiotic marine bivalves (Cardiidae: Fraginae). Biological Journal of the Linnean Society 97: 448–465.
Kocsis, L., T. W. Vennemann, E. Hegner, D. Fontignie & T. Tütken, 2009. Constraints on Miocene oceanography and climate in the Western and Central Paratethys: O-, Sr-, and Nd-isotope compositions of marine fish and mammal remains. Palaeogeography, Palaeoclimatology, Palaeoecology 271: 117–129.
Korniushin, A. V., 2004. A revision of some Asian and African freshwater clams assigned to Corbicula fluminalis (Müller, 1774) (Mollusca: Bivalvia: Corbiculidae), with a review of anatomical characters and reproductive features based on museum collections. Hydrobiologia 529: 251–270.
Kosarev, A. N. & E. A. Yablonskaya, 1994. The Caspian Sea. SPB Academic Publishing, The Hague, Netherlands. 259 pp.
Kowalke, T. & B. Reichenbacher, 2005. Early Miocene (Ottnangian) Mollusca of the Western Paratethys—ontogenetic strategies and palaeo-environments. Geobios 38: 609–635.
Kroonenberg, S. B., G. V. Rusakov & A. A. Svitoch, 1997. The wandering of the Volga delta: a response to rapid Caspian sea-level change. Sedimentary Geology 107: 189–209.
Lahijani, H., V. Tavakoli & M. Hosseindoost, 2007. History of Caspian environmental changes by molluscan stable isotope records. Journal of Coastal Research 50: 438–442.
Mathews, D. H., J. Sabina, M. Zuker & D. H. Turner, 1999. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. Journal of Molecular Biology 288: 911–940.
Millard, V., 2001. Classification of Mollusca. South Africa: 1447 pp.
Müller, P., D. H. Geary & I. Magyar, 1999. The endemic molluscs of the Late Miocene Lake Pannon: their origin, evolution, and family-level taxonomy. Lethaia 32: 47–60.
Munasypova-Motyash, I. A., 2006. Morphometrical characters of the shell of the bivalvial mollusks of the subfamily Limnocardiinae (Bivalvia, Cardiidae) and its significance in their taxonomy. Vestnik Zoologii 40: 521–527 (in Russian with English abstract).
Nabozhenko, M. V., 2008. Distribution of mollusks of the subfamily Limnocardiinae (Bivalvia, Cardiidae) in the Azov Sea Basin. Vestnik Yuzhnogo Nauchnogo Centra RAN 4: 78–82.
Nevesskaja, L. A., 2007. History of the genus Didacna (Bivalvia: Cardiidae). Palaeontological Journal 41: 861–949.
Nevesskaja, L. A., N. P. Paramonova & S. V. Popov, 2001. History of Lymnocardiinae (Bivalvia, Cardiidae). Paleontological Journal 35(Supplement 3): 147–217.
Nikula, R. & R. Väinölä, 2003. Phylogeography of Cerastoderma glaucum (Bivalvia: Cardiidae) across Europe: a major break in the Eastern Mediterranean. Marine Biology 143: 339–350.
Palumbi, S. R., A. Martin, S. Romano, W. O. McMillan, L. Stice & G. Grabowski, 1991. The Simple Fool’s Guide to PCR. University of Hawaii, Honolulu, Hawaii: 94 pp.
Popa, O. P., A. Sarkani-Kiss, B. S. Kelemen, D. Murariu & L. O. Popa, 2009. Contributions to the knowledge of the present Limnocardiidae fauna (Mollusca: Bivalvia) from Romania. Travaux du Muséum National d’Histoire Naturelle “Grigore Antipa” 52: 7–15.
Popa, O. P., E. I. Iorgu, B. S. Kelemen, D. Murariu & L. O. Popa, 2010. Morphometric analysis of some populations of Lymnocardiid species (Mollusca: Bivalvia) from Razelm Lake Complex (Romania). Travaux du Muséum National d’Histoire Naturelle “Grigore Antipa” 53: 13–19.
Popa, L., O. Popa & E. Iorgu, 2011. Molecular insights into the taxonomy of Hypanis (Bivalvia, Cardiidae, Lymnocardiinae) in the Black Sea lagoons. Helgoland Marine Research 66: 153–158.
Reid, D. F. & M. I. Orlova, 2002. Geological and evolutionary underpinnings for the success of Ponto-Caspian species invasions in the Baltic Sea and North America Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences 59: 1144–1158.
Riedel, F., A. Audzijonyte & N. Mugue, 2006. Aliens associating with Caspian Sea endemic bivalves. Biological Invasions 8: 1067–1071.
Riedel, F., A. Kossler, P. Tarasov & B. Wünnemann, 2011. A study on Holocene foraminifera from the Aral Sea and West Siberian lakes and its implication for migration pathways. Quaternary International 229: 105–111.
Rögl, F. & F. F. Steininger, 1983. Vom Zerfall der Tethys zu Mediterran und Paratethys. Die neogene Paläogeographie und Palinspastik des zirkum-mediterranen Raumes. Annalen des Naturhistorischen Museums Wien 84A: 135–163.
Ronquist, F. & J. P. Huelsenbeck, 2005. Bayesian analysis of molecular evolution using Mr Bayes. In Nielsen, R. (ed.), Statistical Methods in Molecular Evolution. Springer, New York: 183–232.
Sakinç, M., C. Yaltirak & F. Y. Oktay, 1999. Palaeogeographical evolution of the Thrace Neogene Basin and the Tethys-Paratethys relations at northwestern Turkey (Thrace). Palaeogeography, Palaeoclimatology, Palaeoecology 153: 17–40.
Schneider, J. A., 1998. Phylogeny of the Cardiidae (Bivalvia): phylogenetic relationships and morphological evolution within the subfamilies Clinocardiinae, Lymnocardiinae, Fraginae and Tridacninae. Malacologia 40: 321–373.
Schneider, J. A., 2002. Phylogeny of cardiid bivalves (cockles and giant clams): revision of the Cardiinae and the importance of fossils in explaining disjunct biogeographical distributions. Zoological Journal of Linnean Society 136: 321–369.
Schneider, J. A. & D. Ó. Foighil, 1999. Phylogeny of giant clams (Cardiidae: Tridacninae) based on partial mitochondrial 16S rDNA gene sequences. Molecular Phylogenetics and Evolution 13: 59–66.
Schultheiß, R., C. Albrecht, U. Bößneck & T. Wilke, 2008. The neglected side of speciation in ancient lakes: phylogeography of an inconspicuous mollusc taxon in lakes Ohrid and Prespa. Hydrobiologia 615: 141–156.
Schultheiß, R., B. Van Bocxlaer, T. Wilke & C. Albrecht, 2009. Old fossils—young species: evolutionary history of an endemic gastropod assemblage in Lake Malawi. Proceedings of the Royal Society B: Biological Sciences 276: 2837–2846.
Schulz, H. M., A. Bechtel & R. F. Sachsenhofer, 2005. The birth of the Paratethys during the early Oligocene: from Tethys to an ancient Black Sea analogue. Global and Planetary Change 49: 163–176.
Seibel, P. N., T. Müller, T. Dandekar, J. Schultz & M. Wolf, 2006. 4SALE—a tool for synchronous RNA sequence and secondary structure alignment and editing. BMC Bioinformatics 7: 498.
Seibel, P. N., T. Müller, T. Dandekar & M. Wolf, 2008. Synchronous visual analysis and editing of RNA sequence and secondary structure alignments using 4SALE. BMC Research Notes 1: 91.
Slugina, Z. V., 2006. Endemic bivalves in ancient lakes. Hydrobiologia 568: 213–217.
Soulet, G., G. Delaygue, C. Vallet-Coulomb, M. E. Böttcher, C. Sonzogni, G. Lericlais & E. Bard, 2010. Glacial hydrologic conditions in the Black Sea reconstructed using geochemical pore water profiles. Earth and Planetary Science Letters 296: 57–66.
Stanley, S. M., 1975. A theory of evolution above the species level. Proceedings of the National Academy of Sciences of the United States of America 72: 646–650.
Terriault, T. W., M. F. Docker, M. I. Orlova, D. D. Heath & H. J. MacIsaac, 2004. Molecular resolution of the family Dreissenidae (Mollusca: Bivalvia) with emphasis on Ponto-Caspian species, including first report of Mytilopsis leucophaeata in the Black Sea basin. Molecular Phylogenetics and Evolution 30: 479–489.
Thom, N., 2010. A hydrological model of the Black and Caspian Seas in the late Pleistocene and early-middle Holocene. Quaternary Science Reviews 29: 2989–2995.
Vokes, H. E., 1980. Genera of the Bivalvia: A Systematic and Bibliographic Catalogue. Paleontological Research Institution Ithaca, New York, USA. 307 pp.
von Rintelen, T. & M. Glaubrecht, 2006. Rapid evolution of sessility in an ancient lake freshwater mussel. Biology Letters 2: 73–77.
Wesselingh, F. P., 2007. Long-lived lake molluscs as island faunas: a bivalve perspective. In Renema, W. (ed.), Biogeography, Time and Place: Distributions, Barriers and Islands. Springer, Dordrecht: 275–314.
Wesselingh, F. P. & H. Alçiçek, 2010. A new cardiid bivalve from the Pliocene Baklan Basin (Turkey) and the origin of modern Ponto-Caspian taxa. Palaeontology 53: 711–719.
Wesselingh, F. P., M. E. Räsänen, G. Irion, H. B. Vonhof, R. Kaandorp, W. Renema, L. Romero Pittman & M. Gingras, 2001. Lake Pebas: a palaeoecological reconstruction of a Miocene, long-lived lake complex in western Amazonia. Cainozoic Research 1: 35–81.
Wesselingh, F. P., H. Alçiçek & I. Magyar, 2008. A late Miocene mollusc fauna from the Denizli Basin (southwestern Anatolia, Turkey) and its regional palaeobiogeographic implications. Geobios 41: 861–879.
Wilke, T., G. M. Davis, D. Qiu & R. C. Spear, 2006. Extreme mitochondrial sequence diversity in the intermediate schistosomiasis host Oncomelania hupensis robertsoni: another case of ancestral polymorphism? Malacologia 48: 143–157.
Wilke, T., C. Albrecht, V. V. Anistratenko, S. K. Sahin & M. Z. Yildirim, 2007. Testing biogeographical hypotheses in space and time: faunal relationships of the putative ancient Lake Egirdir in Asia Minor. Journal of Biogeography 34: 1807–1821.
Yanina, T. A., 2012. Correlation of the Late Pleistocene paleogeographical events of the Caspian Sea and Russian Plain. Quaternary International 271: 120–129.
Zuker, M., 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31: 3406–3415.
Acknowledgments
Many thanks go to N. Aladin (Zoological Institute, Russian Academy of Sciences, St. Petersburg), A. Audzijonyte (CSIRO, Hobart), K. Bandel (Hamburg University), A. Filippov (ECOPROJECT JSC, St. Petersburg), J. Klute (formerly FU Berlin), N. Mugue (Institute of Developmental Biology, Russian Academy of Sciences, Moscow) for their help during field work, to P. Tarasov (FU Berlin) for translating Russian literature. V. Anistratenko (Institute of Zoology, National Academy of Sciences of Ukraine, Kiev) kindly provided important material for this study. An anonymous reviewer and F. Wesselingh (Naturalis Leiden) provided important suggestions on an earlier version of this paper/manuscript. F. Wesselingh kindly helped with species identification and taxonomic issues. The CEMarin—Center of Excellence in Marine Sciences—is acknowledged for its support of this study. The Deutsche Forschungsgemeinschaft provided financial support.
Author information
Authors and Affiliations
Corresponding author
Additional information
Guest editors: T. von Rintelen, R. M. Marwoto, G. D. Haffner & F. Herder / Speciation in Ancient Lakes – Classic Concepts and New Approaches
Rights and permissions
About this article
Cite this article
Albrecht, C., von Rintelen, T., Sereda, S. et al. Evolution of ancient lake bivalves: the Lymnocardiinae (Cardiidae) of the Caspian Sea. Hydrobiologia 739, 85–94 (2014). https://doi.org/10.1007/s10750-014-1908-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-014-1908-3