Unraveling a new lineage of Hydrobiidae genera (Caenogastropoda: Truncatelloidea) from the Ponto-Caspian region

  • Diana Delicado Justus Liebig University Giessen, Department of Animal Ecology & Systematics, Heinrich-Buff-Ring 26-32 IFZD-35392, Giesse
  • Vladimir Pešić University of Montenegro, Department of Biology, 81000, Podgorica, Montenegro
  • Peter Glöer Biodiversity Research Laboratory, Schulstr. 3, D-25491, Hetlingen
Keywords: Freshwater snails, Pseudamnicola, Cryptic taxa, Anatomy, mtDNA


Phylogenetic analyses of the highly diverse (non-marine aquatic) gastropod family Hydrobiidae Stimpson, 1865 have revealed seven main lineages, most of which represent subfamilies. The subfamily Pseudamnicolinae Radoman, 1977, and specifically the genus Pseudamnicola Paulucci, 1878 (mainly inhabiting western and central Mediterranean regions), contributes substantially to this hydrobiid richness. Most of its congeners have been described in terms of their shell and penis features, which are of limited diagnostic value. Hence, the taxonomic status of some Pseudamnicola species needs to be revised, particularly of those inhabiting marginal regions, such as the Ponto-Caspian domain, largely occupied by the subfamily Pyrgulinae Brusina, 1882. Here we present a molecular phylogeny including species of both subfamilies along with extended morphological descriptions to confirm assignments of the Iranian species Pseudamnicola zagrosensis Glöer & Pešić, 2009; Sarkia kermanshahensis Glöer & Pešić, 2009 (originally within Pseudamnicola) and P. saboori Glöer & Pešić, 2009. Our COI-based tree rejects these assignments suggesting a new potential lineage, sister to the pyrgulinid species, and comprising three genera: Shadinia Akramowski, 1976, Intermaria gen. nov. and Persipyrgula gen. nov. These genera differ molecularly by 3.6%–8.5%, and are diagnosable by penis, female genitalia and radula features. Our findings evidence the high morphological variability of pyrgulinid species and provide insight into the origins and evolution of the freshwater Ponto-Caspian fauna.


Akaike H. 1974. A new look at the statistical model identification. IEEE Transactions on Automatic Control 19: 716–723. http://dx.doi.org/10.1109/TAC.1974.1100705

Akramowski N.N. 1952. O nakhozhdenii sovremennogo predstavitelya roda Pyrgula Cristof. et Jan v doline srednego techeniya Araksa (Gastropoda – Prosobranchia, Hydrobiidae). Akademiya Nauk Armyanskoj SSR 84: 631–632.

Akramovski N.N. 1976. Fauna of Armenian SSR: Mollusks (Mollusca). Akademiya Nauk Armyanskoj SSR, Armenia.

Arconada B. & Ramos M.A. 2003. The Ibero-Balearic region: one of the areas of highest Hydrobiidae (Gastropoda, Prosobranchia, Rissooidea) diversity in Europe. Graellsia 59: 91–104.

Badzoshvili T.I. 1979. Mollyuski meotisa zapadnoy Gruzii. Metsniereba, Tbilisi.

Boeters H.D. 1988. Moitessieriidae und Hydrobiidae in Spanien und Portugal. Archiv für Molluskenkunde 118: 181–261.

Darriba D., Taboada G.L., Doallo R. & Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772–772. http://dx.doi.org/10.1038/nmeth.2109

Davis G.M., Chen C.E., Wu C., Kuang T.F., Xing X.G., Li L., Liu W.J. & Yan Y.L. 1992. The Pomatiopsidae of Hunan, China (Gastropoda: Rissoacea). Malacologia 34: 143–342. Available from http://biodiversitylibrary.org/page/13129606 [accessed 30 May 2016]

Davis G.M., Guo Y.H., Hoagland K.E., Chen P.L., Zheng L.C., Yang H.M., Chen D.J. & Zhou Y.F. 1986. Anatomy and Systematics of Triculini (Prosobranchia: Pomatiopsidae: Triculinae), freshwater snails from Yunnan, China, with descriptions of new species. Proceedings of the Academy of Natural Sciences of Philadelphia 138: 466–575.

Davis G.M., Kitikoon V. & Temcharoen P. 1976. Monograph on ‘Lithoglyphosis’ aperta, the snail of Mekong river Schistosomiasis. Malacologia 15: 241–287. Available from http://biodiversitylibrary.org/page/13122908 [accessed 30 May 2016]

Davis G.M., Kuo Y.H., Hoagland K.E., Chen P.L., Yang H.M. & Chen D.J. 1984. Kunmingia, a new genus of Triculinae (Gastropoda: Pomatiopsidae) from China: Phenetic and cladistic relationships. Proceedings of the Academy of Natural Sciences of Philadelphia 136: 165–193.

Delicado D., Machordom A. & Ramos M.A. 2012. Underestimated diversity of hydrobiid snails. The case of Pseudamnicola (Corrosella) (Mollusca: Caenogastropoda: Hydrobiidae). Journal of Natural History 46: 25–89. http://dx.doi.org/10.1080/00222933.2011.623358

Delicado D., Machordom A. & Ramos M.A. 2014. Vicariant versus dispersal processes in the settlement of Pseudamnicola (Caenogastropoda, Hydrobiidae) in the Mediterranean Balearic Islands. Zoological Journal of the Linnean Society 171: 38–71. http://dx.doi.org/10.1111/zoj.12124

Delicado D., Machordom A. & Ramos M.A. 2015. Effects of habitat transition on the evolutionary patterns of the microgastropod genus Pseudamnicola (Mollusca, Hydrobiidae). Zoologica Scripta 44: 403–417. http://dx.doi.org/10.1111/zsc.12104

Delicado D. & Ramos M.A. 2012. Morphological and molecular evidence for cryptic species of springsnails [genus Pseudamnicola (Corrosella) (Mollusca, Caenogastropoda, Hydrobiidae)]. ZooKeys 190: 55–79. http://dx.doi.org/10.3897/zookeys.190.2555

Egorov R. 2006. Treasure of Russian shells, Supplement 4. Illustrated Catalogue with Selected Identification Keys of the Recent Fresh- and Brackish-water Pectinibranch Molluscs (Gastropoda: Pectinibranchia) of Russia and adjacent regions. Colus, Moscow.

Felsenstein J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783. http://dx.doi.org/10.2307/2408678

Folmer O., Black M., Hoeh W., Lutz R. & Vrijenhoek R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular marine biology and biotechnology 3: 294–299.

Glöer P., Böβneck U., Walther F. & Neiber M.T. 2016. New taxa of freshwater molluscs from Armenia (Caenogastropoda: Truncatelloidea: Hydrobiidae). Folia Malacologica 24 (1): 3–8.

Glöer P. & Georgiev D. 2012. Three new gastropod species from Greece and Turkey (Mollusca: Gastropoda: Rissooidea) with notes on the anatomy of Bythinella charpentieri cabirius Reischütz 1988. North-western journal of Zoology 8: 278–282.

Glöer P., Gürlek M. & Kara C. 2014. New Pseudamnicola species of Turkey (Mollusca: Gastropoda: Hydrobiidae). Ecologica Montenegrina 1: 103–108.

Glöer P. & Pešić V. 2009. New freshwater gastropod species of the Iran (Gastropoda: Stenothyridae, Bithyniidae, Hydrobiidae). Mollusca 27: 33–39.

Glöer P. & Pešić V. 2012. The freshwater snails (Gastropoda) of Iran, with descriptions of two new genera and eight new species. ZooKeys 219: 11–61. http://dx.doi.org/10.3897/zookeys.219.3406

Glöer P., Yıldırım M.Z. & Kebapçi Ü. 2015. Description of two new species of Pseudamnicola from southern Turkey (Mollusca: Gastropoda: Hydrobiidae). Zoology in the Middle East 61: 139–143. http://dx.doi.org/10.1080/09397140.2015.1008189

Guindon S. & Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic biology 52: 696–704.

Hershler R. & Ponder W.F. 1998. A review of morphological characters of hydrobioid snails. Smithsonian Contributions to Zoology 600, Smithsonian Institution, Washington.

Huelsenbeck J.P. 2000. MrBayes: Bayesian Inference of Phylogeny. NCBI, New York.

Huelsenbeck J.P. & Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755. http://dx.doi.org/10.1093/bioinformatics/btg180

Hurvich C.M. & Tsai C.L. 1989. Regression and time series model selection in small samples. Biometrika 76: 297–307.

Kelley K. & Lai K. 2011. MBESS 3.0.4 (or higher): [computer software and manual]. Available from http://www.cran.r-project.org/ [accessed 30 May 2016]

Liu H.P., Hershler R. & Clift K. 2003. Mitochondrial DNA sequences reveal extensive cryptic diversity within a western American springsnail. Molecular Ecology 12: 2771–2782. http://dx.doi.org/10.1046/j.1365-294X.2003.01949.x

R Development Core Team. 2011. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.

Radoman P. 1955. Recherches morphologiques et systematiques sur les Hydrobiides du Lac d’Ohrid. Posebna Izd. Srpska Biol Dr 1: 1–106.

Radoman P. 1983. Hydrobioidea a Superfamily of Prosobranchia (Gastropoda): Systematics. Serbian Academy of Sciences and Arts, Belgrade.

Rambaut A. & Drummond A. 2009. Tracer v. 1.5. Available from http://tree.bio.ed.ac.uk/software/tracer/ [accessed 30 May 2016]

Ramos M.A., Arconada B., Moreno D. & Rolán E. 2000. A new genus and a new species of Hydrobiid snail (Mollusca: Gastropoda: Hydrobiidae) from eastern Spain. Malacologia 42: 75–101. http://biodiversitylibrary.org/page/12937820

Schreiber K., Hauffe T., Albrecht C. & Wilke T. 2012. The role of barriers and gradients in differentiation processes of pyrgulinid microgastropods of Lake Ohrid. Hydrobiologia 682: 61–73. http://dx.doi.org/10.​1007/​s10750-011-0864-4

Shadin V.I. 1952. Mollusks of fresh and brackish waters of the USSR. Academy of Sciciences of the U.S.S.R., Moscow.

Strong E.E., Gargominy O., Ponder W.F. & Bouchet P. 2008. Global diversity of gastropods (Gastropoda; Mollusca) in freshwater. In: Balian E.V., Lévêque C., Segers H., Martens K. (eds) Freshwater Animal Diversity Assessment. Developments in Hydrobiology 595 (1): 149–166. http://dx.doi.org/10.1007/s10750-007-9012-6

Sugiura N. 1978. Further analysis of the data by Akaike’s information criterion and the finite corrections. Communications in Statistics − Theory and Methods A 7: 13–26. http://dx.doi.org/10.1080/03610927808827599

Swofford D.L. 2002. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland, Massachusetts.

Szarowska M. 2006. Molecular phylogeny, systematics and morphological character evolution in the Balkan Rissooidea (Caenogastropoda). Folia Malacologica 14: 99–168. http://dx.doi.org/10.12657/folmal.014.014

Szarowska M., Grzmil P. & Falniowski A. 2009. Pseudamnicola Paulucci, 1878 (Gastropoda: Hydro-biidae) in the Balkans. Folia Malacologica 14: 179–190. http://dx.doi.org/10.12657/folmal.014.016

Tamura K. & Nei M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10: 512–526.

Wilke T. 2003. Salenthydrobia gen. nov. (Rissooidea: Hydrobiidae): a potential relict of the Messinian salinity crisis. Zoological Journal of the Linnean Society 137: 319–336. http://dx.doi.org/10.1046/j.1096-3642.2003.00049.x

Wilke T. & Davis G.M. 2000. Infraspecific mitochondrial sequence diversity in Hydrobia ulvae and Hydrobia ventrosa (Hydrobiidae: Rissooidea: Gastropoda): Do their different life histories affect biogeographic patterns and gene flow? Biological Journal of the Linnean Society 70: 89–105. http://dx.doi.org/10.1111/j.1095-8312.2000.tb00202.x

Wilke T., Albrecht C., Anistratenko V.V., Sahin S.K. & Yıldırım M.Z. 2007. Testing biogeographical hypotheses in space and time: faunal relationships of the putative ancient Lake Eğirdir in Asia Minor. Journal of Biogeography 34: 1807–1821. http://dx.doi.org/10.1111/j.1365-2699.2007.01727.x

Wilke T., Davis G.M., Falniowski A., Giusti F., Bodon M. & Szarowska M. 2001. Molecular systematics of Hydrobiidae (Mollusca: Gastropoda: Rissooidea): testing monophyly and phylogenetic relationships. Proceedings of the Academy of Natural Sciences of Philadelphia 151: 1–21. http://dx.doi.org/10.1635/0097-3157(2001)151[0001:MSOHMG]2.0.CO;2

Wilke T., Davis G.M., Qiu D.C. & Spear R.C. 2006. Extreme mitochondrial sequence diversity in the intermediate schistosomiasis host Oncomelania hupensis robertsoni: another case of ancestral polymorphism? Malacologia 48: 143–157. Available from http://biodiversitylibrary.org/page/13115586 [accessed 30 May 2016]

Wilke T., Haase M., Hershler R., Liu H.P., Misof B. & Ponder W. 2013. Pushing short DNA fragments to the limit: Phylogenetic relationships of ‘hydrobioid’ gastropods (Caenogastropoda: Rissooidea). Molecular Phylogenetics and Evolution 66: 715–736. http://dx.doi.org/10.1016/j.ympev.2012.10.025

Wilke T., Pfenninger M. & Davis G.M. 2002. Anatomical variation in cryptic mudsnail species: Statistical discrimination and evolutionary significance. Proceedings of the National Academy of Sciences of Philadelphia 152: 45–66.

Wilke T., Rolán E. & Davis G.M. 2000. The mudsnail genus Hydrobia s.s. in the northern Atlantic and western Mediterranean: a phylogenetic hypothesis. Marine Biology 137: 827–833. http://dx.doi.org/10.1007/s002270000407

Yıldırım M.Z., Koca S.B. & Kebapçi Ü. 2006. Supplement to the Prosobranchia (Mollusca: Gastropoda) fauna of fresh and brackish waters of Turkey. Turkish Journal of Zoology 30: 197–204.

How to Cite
Delicado, D., Pešić, V., & Glöer, P. (2016). Unraveling a new lineage of Hydrobiidae genera (Caenogastropoda: Truncatelloidea) from the Ponto-Caspian region. European Journal of Taxonomy, (208). https://doi.org/10.5852/ejt.2016.208