Radiation in Bythinella Moquin-Tandon, 1856 (Mollusca: Gastropoda: Rissooidea) in the Balkans

Andrzej Falniowski, e-mail: andrzej.falniowski@uj.edu.pl

Department of Malacology, Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Cracow, Poland

Magdalena Szarowska

Department of Malacology, Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Cracow, Poland

Peter Glöer

Department of Biology, University of Montenegro, Cetinjski put b.b, 81000 Podgorica, Montenegro

Vladimir Pešić

Department of Ecology and Environmental Conservation, University of Plovdiv, Tzar Assen 24, BG-4000 Plovdiv, Bulgaria

Dilian Georgiev

Department of Botany and Zoology, Masaryk University, Kotlářská 2, CZ-611 37 Brno, Czech Republic

Michal Horsák

Department of Ecology and Environmental Protection, Lucian Blaga University, 31 Oituz St., 550337 Sibiu, Romania

Ioan Sirbu

Department of Ecology and Environmental Protection, Lucian Blaga University, 31 Oituz St., 550337 Sibiu, Romania

61 sequences of cytochrome oxidase subunit 1 (COI), 570 bp long, from Central Europe (8), Slovenia (2), and from the Balkans (51: 6 from, Romania, 15 from Greece, 15 from Bulgaria, 6 from Serbia, and 9 from Montenegro), 33 of them new, together with 61 sequences of the ribosomal 18S, 450 bp long, all ofthem new, were analysed to infer the pattern of radiation of Bythinella in the Balkans. Thirty two nominal taxa of Bythinella (22 nominal species: B. austriaca, B. calimanica, B. charpentieri, B. compressa, B. dacica, B. dispersa, B.grossui, B. hansboetersi, B. luteola, B. micherdzinskii, B. molcsanyi, B. nonveilleri, B. pannonica, B. pesterica, B.radomani, B. rhodopensis, B. robiciana, B. schmidti, B. slaveyae, B. srednogorica, B. taraensis and B. viseuiana; one nominal subspecies: B. austriaca ehrmanni; and nine Greek species not yet described) were included, represented mostly by paratypes or at least topotypes, collected at 31 Balkan localities. The phylogeny, inferred on the combined data set with the ML approach, showed two large clades, although they were weakly supported. One of them comprised the Romanian and Montenegro populations, and one Serbian population, the other (less genetically diversified) consisted of one Serbian and all the Bulgarian/Greek populations. The origin of those two clades was dated, with the external data, to be more than 4.341±0753 MYA old, thus its origin was assigned to isolation by the Dacic Basin (part of Paratethys). All the Bulgarian populations presumably belong to one species, which may be assigned to the recent recolonisation of this territory from the south.

Key words
Rissooidea; Balkan Peninsula; DNA; phylogeny; taxonomy; speciation

Akaike H. 1974. A new look at the statistical model identification. IEEE Transactions of Automatic Control 19: 716–723.  

Benke M., Brändle M., Albrecht C., Wilke T. 2009. Pleistocene phylogeography and phylogenetic concordance in cold-adapted spring snails (Bythinella spp.). Molec. Ecol. 18: 890–903.

Bichain J.-M., Gaubert P., Samadi S., Boisselier-Dubayle M.-C. 2007a. A gleam in the dark: Phylogenetic species delimitation in the confusing spring-snail genus Bythinella Moquin-Tandon, 1856 (Gastropoda: Rissooidea: Amnicolidae). Mol. Phylogenet. Evol. 45: 927–941.

Bichain J.-M., Boisselier-Dubayle M.-C., Bouchet P., Samadi S. 2007b. Species delimitation in the genus Bythinella (Mollusca: Caenogastropoda: Rissooidea): a first attempt combining molecular and morphometrical data. Malacologia 49: 293–311.

Davis G. M. 1992. Evolution of prosobranch snails transmitting Asian Schistosoma: coevolution with Schistosoma: a review. Prog. Clin. Parasitol. 3: 145–204.

Esu D., Gianolla D. 2009. The malacological record from the Plio-Pleistocene Leffe Basin (Bergamo, Northern Italy). Quatern. Int. 204: 11–19. 

Falniowski A. 1980. Bythinella micherdzinskii n. sp. – new species from the family Bythinellidae s. Radoman (Gastropoda, Prosobranchia). Bull. Acad. Pol. Sci., Ser. sci. biol. Cl. 2, 28: 225–230.

Falniowski A. 1987. Hydrobioidea of Poland (Prosobranchia: Gastropoda). Folia Malacol. 1: 1–122.

Falniowski A. 1992. Genus Bythinella Moquin-Tandon, 1855, in Poland (Gastropoda, Prosobranchia, Hydrobiidae. In: Gittenberger E., Goud J. (eds). Proc. 9th Int. Malac. Congr. Edinburgh, 31 August–6 September 1986. Unitas Malacologica, Leiden: 135–138.

Falniowski A. 2003. Metody numeryczne w taksonomii. Wydawnictwo Uniwersytetu Jagiellońskiego, Kraków.

Falniowski A., Horsak M., Szarowska M. 2009a. Bythinella hansboetersi Glöer et Pešić, 2006 (Gastropoda: Rissooidea) in Bulgaria: its morphology, molecular distinctness, and phylogeography. Folia Malacol. 17: 11–20.

Falniowski A., Szarowska M. 2011. Radiation and phylogeography in a spring snail Bythinella (Mollusca: Gastropoda: Rissooidea) in continental Greece. Ann. Zool. Fennici 48: 67–90.

Falniowski A., Szarowska M., Sirbu I. 2009b. Bythinella Moquin-Tandon, 1856 (Gastropoda: Rissooidea: Bythinellidae) in Romania: species richness in a glacial refugium. J. Nat. Hist. 43: 2955–2973. 

Falniowski A., Szarowska M., Sirbu I. 2009c. Bythinella Moquin-Tandon, 1856 (Gastropoda: Rissooidea: Bythinellidae) in Romania: its morphology with description of four new species. Folia Malacol. 17: 21–36.

Falniowski A., Wilke T. 2001. The genus Marstoniopsis (Gastropoda: Rissooidea): intra- and intergeneric phylogenetic relationships. J. Moll. Stud. 67: 483–488.

Farris J. S., Källersjö M., Kluge A. G., Bult C. 1995. Testing significance of incongruence. Cladistics 10: 315–319. 

Felsenstein J. 1981. Evolutionary trees from DNA sequences: a maximum-likelihood approach. J. Molec. Evol. 17: 368–376. 

Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791. 

Folmer O., Black M., Hoeh W., Lutz R. A., Vrijenhoek R. C. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3: 294–299.

Giusti F., Pezzoli E. 1977. Primo contributo alla revisione del genere Bythinella in Italia. Natura Bresciana, Annurario del Museo Civico di Storia Naturale di Brescia 14: 3–80.

Glöer P. 2002. Die Süsswassergastropoden Nord- und Mitteleuropas, Bestimmungsschlüssel, Lebensweise, Verbreitung. Die Tierwelt Deutschlands, 73. Teil. ConchBooks, Hackenheim.

Glöer P. 2008. Three new hydrobioid species from Serbia (Mollusca, Gastropoda, Hydrobiidae). In: Pavićević D., M. Perreau (eds). Advances in the studies of the subterranean and epigean fauna of the Balkan Peninsula. Volume dedicated to the memory of Guido Nonvellier. Monograph 22, Institute for Nature Conservation of Serbia, pp. 349–356.

Glöer P., Georgiev D. 2009. New Rissooidea from Bulgaria (Gastropoda: Rissooidea). Mollusca 27: 123–136.

Glöer P., Pešić V. 2006. Bythinella hansboetersi n. sp., a new species from Bulgaria. Heldia 6: 11–15.

Glöer P., Pešić V. 2010. The freshwater snails of the genus Bythinella Moquin-Tandon (Gastropoda: Rissooidea: Hydrobiidae) from Montenegro. Arch. Biol. Sci., Belgrade 62: 441–447.

Haase M., Wilke T., Mildner P. 2007. Identifying species of Bythinella (Caenogastropoda: Rissooidea): A plea for an integrative approach. Zootaxa 1563: 1–16.

Hall T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95–98.

Hewitt G. M. 1989. The subdivision of species by hybrid zones. In: Otte D., Endler J. A. (eds). Speciation and its consequences. Sinauer Associates Inc. Publishers, Sunderland, Massachusetts, pp. 85–110.

Hewitt G. M. 1996. Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linn. Soc. 58: 247–276.

Hewitt G. M. 2000. The genetic legacy of the Quaternary ice ages. Nature 405: 907–913. 

Hillis D. M., Mable B. K., Larson A., Davis S. K., Zimmer E. A. 1996. Nucleic acids IV: Sequencing and cloning. In: Hillis D. M., Moritz L., Mable B. K. (eds). Molecular Systematics. Second Edition. Sinauer Associates Inc. Publishers, Sunderland, Massachusetts, pp. 321–381.

Jungbluth J. H., Boeters H. D. 1977. Zur Artabgrenzung bei Bythinella dunkeri und bavarica (Prosobranchia). Malacologia 16: 143–147.

Kimura M. 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111–120. 

Maddison D. R., Maddison W. P. 2002. MACCLADE. Ver. 4.05. [Computer software and manual]. Sinauer Associates Inc. Publishers, Sunderland, Massachusetts.

Nei M., Kumar S. 2000. Molecular evolution and phylogenetics. Oxford University Press, Oxford.

Palumbi S. R. 1996. Nucleic Acids II: The Polymerase Chain Reaction. In: Hillis D. M, Moritz C., Mable B. K. (eds). Molecular Systematics. Second Edition. Sinauer Associates Inc., Sunderland, Massachusetts, pp. 205–247.

Petit R. J., Aguinagalde I., de Beaulieu J.-L., Bittkau C., Brewer S., Cheddadi R., Ennos R., Fineschi S., Grivet D., Lascoux M., Mohanty A., Müller-Starck G., Demesure-Musch B., Palmé A., Martín J. P., Rendell S., Vendramin G. 2003. Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300: 1563–1565. 

Popescu S.-M., Dalesme F., Jouannic G., Escarguel G., Head M., Melinte-Dobrinescu M.-C., Süto-Szentai M., Bakrac K., Clauzon G., Suc J. P. 2009. Galeacysta etrusca complex: dinoflagellate cyst marker of Paratethyan influxes to the Mediterranean Sea before and after the peak of the Messinian Salinity Crisis. Palynology 33: 105–134.

Popov S. V., Rögl F., Rozanov A. Y., Steininger F. F., Shcherba I. G., Kovac M. 2004. Lithological-paleogeographic maps of the Paratethys. 10 maps Late Eocene to Pliocene. Courier Forschungsinstitut Senckenberg 250: 1–46.

Popov S. V., Shcherba I. G., Ilyina L. B., Nevesskaya L. A., Paramonova N. P., Khondkarian S. O., Magyar I. 2006. Late Miocene to Pliocene palaeogeography of the Paratethys and its relation to the Mediterranean. Palaeogeogr. Palaeoclimatol. Palaeoecol. 238: 91–106.

Posada D. 2003. Selecting models of evolution. In: Salemi M., Vandamme A.- M. (eds). The phylogenetic handbook. A practical approach to DNA and protein phylogeny. Cambridge University Press, Cambridge, pp. 256–282.

Posada D., Buckley T. R. 2004. Model selection and model averaging in phylogenetics: Advantages of Akaike Information Criterion and Bayesian approaches over likelihood ratio tests. Syst. Biol. 53: 793–808.

Posada D., Crandall K. A. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818. 

Radoman P. 1976. Speciation within the family Bythinellidae on the Balkans and Asia Minor. Z. Zool. System. Evol. 14: 130–152. 

Radoman P. 1983. Hydrobioidea a superfamily of Prosobranchia (Gastropoda). I; Systematics. Monographs, Department of Sciences, Serbian Academy of Sciences and Arts 547(57): 1–256.

Radoman P. 1985. Hydrobioidea, a superfamily of prosobranchia (Gastropoda). II: Origin, zoogeography, evolution in the Balkans and Asia Minor. Monographs, Faculty of Science, Department of Biology, Institute of Zoology Beograd 1: 1–173.

Schmitt T. 2007. Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Front. Zool. 4: 11. 

Sober E. 2002. Instrumentalism, parsimony, and the Akaike framework. Philos. Sci. 69: 112–123. 

Swofford D. L. 2002. PAUP*- Phylogenetic analysis using parsimony (* and other methods). Ver. 4. [Computer software and manual]. Sinauer Associates Inc., Sunderland, Massachusetts.

Swofford D. L., Olsen G. J., Waddell P. J., Hillis D. M. 1996. Phylogenetic inference. In: Hillis D. M., Moritz C.,  Mable B. K. (eds). Molecular Systematics Second ed. Sinauer Associates Inc., Sunderland, Massachusetts, pp. 407–514.

Szarowska M., Wilke T. 2004. Sadleriana pannonica (Frauenfeld, 1865): a lithoglyphid, hydrobiid or amnicolid taxon? J. Moll. Stud. 70: 49–57. 

Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24: 4876–4882. 

Vogel J. C., Rumsey F. J., Schneller J. J., Barrett J. A., Gibby M. 1999. Where are the glacial refugia in Europe? Evidence from pteridophytes. Biol. J. Linn. Soc. 66: 23–37. 

Wilke T., Davis G. M., Falniowski A., Giusti F., Bodon M., Szarowska M. 2001. Molecular systematics of Hydrobiidae (Gastropoda: Rissooidea): testing monophyly and phylogenetic relationships. Proc. Acad. Nat. Sci. Philad. 151: 1–21. 

Xia X. 2000. Data analysis in molecular biology and evolution. Kluwer Academic Publishers. Boston/Dordrecht/ London.

Xia X., Xie Z., Salemi M., Chen L., Wang Y. 2003. An index of substitution saturation and its application. Mol. Phylogenet. Evol. 26: 1–7.

Zagorchev I. 2007. Late Cenozoic development of the Strouma and Mesta fluviolacustrine systems, SW Bulgaria and northern Greece. Quaternary Sci. Rev. 26: 2783–2800. 

Folia Malacologica (2012) 20: 1-10
First published on-line: 2012-03-05 00:00:00
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