Abstract
We review competing taxonomic classifications and hypotheses for the phylogeny of emydine turtles. The formerly recognized genus Clemmys sensu lato clearly is paraphyletic. Two of its former species, now Glyptemys insculpta and G. muhlenbergii, constitute a well-supported basal clade within the Emydinae. However, the phylogenetic position of the other two species traditionally placed in Clemmys remains controversial. Mitochondrial data suggest a clade embracing Actinemys (formerly Clemmys) marmorata, Emydoidea and Emys and as its sister either another clade (Clemmys guttata + Terrapene) or Terrapene alone. In contrast, nuclear genomic data yield conflicting results, depending on which genes are used. Either Clemmys guttata is revealed as sister to ((Emydoidea + Emys) + Actinemys) + Terrapene or Clemmys guttata is sister to Actinemys marmorata and these two species together are the sister group of (Emydoidea + Emys); Terrapene appears then as sister to (Actinemys marmorata + Clemmys guttata) + (Emydoidea + Emys). The contradictory branching patterns depending from the selected loci are suggestive of lineage sorting problems. Ignoring the unclear phylogenetic position of Actinemys marmorata, one recently proposed classification scheme placed Actinemys marmorata, Emydoidea blandingii, Emys orbicularis, and Emys trinacris in one genus (Emys), while another classification scheme treats Actinemys, Emydoidea, and Emys as distinct genera. The inclusion of Actinemys in the same taxon as Emydoidea + Emys is unacceptable under a phylogenetic classification framework because there is evidence for the non-monophyly of this clade. Moreover, Actinemys, Emydoidea, and Emys are morphologically highly distinct. Their morphological divergence exceeds by far the differences that typically occur among species of the same genus, so that a continued usage of the distinct genera Actinemys, Emydoidea and Emys is recommended.References
Agassiz, L. (1857) Contributions to the Natural History of the United States of America, Volumes I & II. Little, Brown and Company, Boston, Volume I: pp. i–li + 1–452, Volume II: pp. 451–643, XVII pls.
Bickham, J.W., Lamb, T., Minx, P. & Patton, J.C. (1996) Molecular systematics of the genus Clemmys and the intergeneric relationships of emydid turtles. Herpetologica, 52, 89–97.
Böhme, M.U., Fritz, U., Kotenko, T., Džukić, G., Ljubisavljević, K., Tzankov, N. & Berendonk, T.U. (2007) Phylogeography and cryptic variation within the Lacerta viridis complex (Lacertidae, Reptilia). Zoologica Scripta, 36, 119–131.
Boulenger, G.A. (1889) Catalogue of the Chelonians, Rhynchocephalians, and Crocodiles in the British Museum (Natural History). British Museum (Natural History), London, x + 311 pp., 6 pls.
Bramble, D.M. (1974) Emydid shell kinesis: biomechanics and evolution. Copeia, 1974, 707–727.
Burke, R.L., Leuteritz, T.E. & Wolf, A.J. (1996) Phylogenetic relationships of emydine turtles. Herpetologica, 52, 572–584.
Colliard, C., Sicilia, A. Turrisi, G.F., Arculeo, M., Perrin, N. & Stöck, M. (2010) Strong reproductive barriers in a narrow hybrid zone of West-Mediterranean green toads (Bufo viridis subgroup) with Plio-Pleistocene divergence. BMC Evolutionary Biology, 10, 232.
Duméril, A.M.C. (1806) Zoologie analytique, ou méthode naturelle de classification des animaux, rendue plus facile a l’aide de tableaux synoptiques. Allais, Paris, xxxii + 344 + (1) pp.
Ernst, C.H. (2001) An overview of the North American turtle genus Clemmys Ritgen, 1828. Chelonian Conservation and Biology, 4, 211–216.
Ernst, C.H., Altenburg, R.G.M. & Barbour, R.W. (2000) Turtles of the World. World Biodiversity Database, Version 1.2. Biodiversity Center of ETI, Amsterdam, CD-ROM.
Ernst, C.H. & Barbour, R.W. (1972) Turtles of the United States. University Press of Kentucky, Lexington, Kentucky, x + 347 pp., 24 pls.
Ernst, C.H. & Barbour, R.W. (1989) Turtles of the World. Smithsonian Institution Press, Washington, D.C., xii + 313 pp., 16 pls.
Ernst, C.H. & Lovich, J.E. (2009) Turtles of the United States and Canada. Second Edition. The Johns Hopkins University Press, Baltimore, Maryland, xii + 827 pp.
Feldman, C.R. & Parham, J.F. (2002) Molecular phylogenetics of emydine turtles: Taxonomic revision and the evolution of shell kinesis. Molecular Phylogenetics and Evolution, 22, 388–398.
Fritz, U. (2003) Die Europäische Sumpfschildkröte. Laurenti Verlag, Bielefeld, 224 pp.
Fritz, U., Ayaz, D., Hundsdörfer, A.K., Kotenko, T., Guicking, D., Wink, M., Tok, C.V., Çiçek, K. & Buschbom, J. (2009) Mitochondrial diversity of European pond turtles (Emys orbicularis) in Anatolia and the Ponto-Caspian Region: Multiple old refuges, hotspot of extant diversification and critically endangered endemics. Organisms, Diversity & Evolution, 9, 100–114.
Fritz, U., Fattizzo, T., Guicking, D., Tripepi, S., Pennisi, M.G., Lenk, P., Joger, U. & Wink, M. (2005) A new cryptic species of pond turtle from southern Italy, the hottest spot in the range of the genus Emys (Reptilia, Testudines, Emydidae). Zoologica Scripta, 34, 351–371.
Fritz, U., Guicking, D., Kami, H., Arakelyan, M., Auer, M., Ayaz, D., Ayres-Fernández, C., Bakiev, A.G., Celani, A., Džukić, G., Fahd, S., Havaš, P., Joger, U., Khabibullin, V.F., Mazanaeva, L.F., Široký, P., Tripepi, S., Valdeón-Vélez, A., Velo-Antón, G. & Wink, M. (2007) Mitochondrial phylogeography of European pond turtles (Emys orbicularis, Emys trinacris) – an update. Amphibia-Reptilia, 28, 418–426.
Fritz, U. & Havaš, P. (2007) Checklist of chelonians of the world. Vertebrate Zoology, 57, 149–368.
Gaffney, E.S. & Meylan, P.A. (1988) A phylogeny of turtles. In: Benton, M.J. (ed.), The Phylogeny and Classification of the Tetrapods. Vol. 1, Amphibians, Reptiles, Birds. Clarendon Press/Systematics Association, Oxford, UK, pp. 157–219.
Gvoždík, V., Moravec, J., Klütsch, C. & Kotlík, P. (2010) Phylogeography of the Middle Eastern tree frogs (Hyla, Hylidae, Amphibia) as inferred from nuclear and mitochondrial DNA variation, with a description of a new species. Molecular Phylogenetics and Evolution, 55, 1146–1166.
Holland, D.C. (1994) The Western Pond Turtle: Habitat and History. Final Report, U.S. Department of Energy, Bonneville Power Administration. Project 92-068, Contribution DE-BI79-92B62137, 302 pp.
Holman, J.A. & Fritz, U. (2001) A new emydine species from the Medial Miocene (Barstovian) of Nebraska, USA with a new generic arrangement for the species of Clemmys sensu McDowell (1964). Zoologische Abhandlungen, 51, 321–343.
ICZN [International Commission on Zoological Nomenclature] (1999) International Code of Zoological Nomenclature. Fourth Edition. International Trust for Zoological Nomenclature, London, XXIX + 306 pp.
Joger, U., Fritz, U., Guicking, D., Kalyabina-Hauf, S., Nagy, Z.T. & Wink, M. (2007) Phylogeography of western Palaearctic reptiles – Spatial and temporal speciation patterns. Zoologischer Anzeiger, 246, 293–313.
Lenk, P., Fritz, U., Joger, U. & Wink, M. (1999) Mitochondrial phylogeography of the European pond turtle, Emys orbicularis (Linnaeus 1758). Molecular Ecology, 8, 1911–1922.
Loveridge, A. & Williams, E.E. (1957) Revision of the African tortoises and turtles of the suborder Cryptodira. Bulletin of the Museum of Comparative Zoology, 115, 163–557, 18 pls.
Lovich, J.E., Laemmerzahl, A.F., Ernst, C.H. & McBreen, J.F. (1991) Relationships among turtles of the genus Clemmys (Reptilia, Testudines, Emydidae) as suggested by plastron scute morphology. Zoologica Scripta, 20, 425–429.
McDowell, S.B. (1964) Partition of the genus Clemmys and related problems in the taxonomy of the aquatic Testudinidae. Proceedings of the Zoological Society London, 143, 239–279.
Pedall, I., Fritz, U., Stuckas, H., Valdeón, A. & Wink, M. (2011) Gene flow across secondary contact zones of the Emys orbicularis complex in the Western Mediterranean and evidence for extinction and re-introduction of pond turtles on Corsica and Sardinia (Testudines: Emydidae). Journal of Zoological Systematics and Evolutionary Research, 49, 44–57.
Rhodin, A.G.J., van Dijk, P.P., Iverson, J.B. & Shaffer, H.B. (2010) Turtles of the world, 2010 update: Annotated checklist of taxonomy, synonymy, distribution, and conservation status. Chelonian Research Monographs, 5, 000.85–000.164.
Rykena, S. (1991) Kreuzungsexperimente zur Prüfung der Artgrenzen im Genus Lacerta sensu stricto. Mitteilungen des Zoologischen Museums Berlin, 67, 55–68.
Seidel, M.E. & Smith, H.M. (1986) Chrysemys, Pseudemys, Trachemys (Testudines: Emydidae): Did Agassiz have it right? Herpetologica, 42, 242–248.
Siebenrock, F. (1909) Synopsis der rezenten Schildkröten, mit Berücksichtigung der in historischer Zeit ausgestorbenen Arten. Zoologisches Jahrbuch für Systematik, Supplement 10, 427–618.
Spinks, P.Q. & Shaffer, H.B. (2005) Range-wide molecular analysis of the western pond turtle (Emys marmorata): cryptic variation, isolation by distance, and their conservation implications. Molecular Ecology, 14, 2047–2064.
Spinks, P.Q. & Shaffer, H.B. (2009) Conflicting mitochondrial and nuclear phylogenies for the widely disjunct Emys (Testudines: Emydidae) species complex, and what they tell us about biogeography and hybridization. Systematic Biology, 58, 1–20.
Spinks, P.Q., Thomson, R.C. & Shaffer, H.B. (2009) Nuclear gene phylogeography reveals the historical legacy of an ancient inland sea on lineages of the western pond turtle, Emys marmorata in California. Molecular Ecology, 19, 542–556.
Stephens, P.R. & Wiens, J.J. (2003) Ecological diversification and phylogeny of emydid turtles. Biological Journal of the Linnean Society, 79, 577–610.
Stöck, M., Dubey, S., Klütsch, C., Litvinchuk, S.N., Scheidt, U. & Perrin, N. (2008) Mitochondrial and nuclear phylogeny of circum-Mediterranean tree frogs from the Hyla arborea group. Molecular Phylogenetics and Evolution, 49, 1019–1024.
Stöck, M., Moritz, C., Hickerson, M., Frynta, D., Dujsebayeva, T., Eremchenko, V., Macey, J.R., Papenfuss, T.J. & Wake, D.B. (2006) Evolution of mitochondrial relationships and biogeography of Palearctic green toads (Bufo viridis subgroup) with insights in their genomic plasticity. Molecular Phylogenetics and Evolution, 41, 663–689.
Strauch, A. (1862) Chelonologische Studien, mit besonderer Beziehung auf die Schildkrötensammlung der Kaiserlichen Akademie der Wissenschaften zu St.-Petersburg. Mémoires de l’Académie impériale de St.-Pétersbourg, VIIe Série, 5(7), 1–196, 1 pl.
Vörös, J. & Arntzen, J.W. (2010) Weak population structuring in the Danube crested newt, Triturus dobrogicus, inferred from allozymes. Amphibia-Reptilia, 31, 339–346.
Wagler, J.G. (1830) Natürliches System der Amphibien. J.G. Cotta, München, Stuttgart, and Tübingen, vi + 354 pp., 1 pl., 1 folding table; atlas, 4 pp., 7 pls.
Wallis, G.P. & Arntzen, J.W. (1989) Mitochondrial-DNA variation in the crested newt superspecies: limited cytoplasmic gene flow among species. Evolution, 43, 88–104.
Wermuth, H. & Mertens, R. (1961) Schildkröten, Krokodile, Brückenechsen. VEB G. Fischer, Jena, xxvii + 422 pp.
Wermuth, H. & Mertens, R. (1977) Testudines, Crocodylia, Rhynchocephalia. Das Tierreich, 100, i–xxvii + 1–174.
Wiens, J.J., Kuczynski, C.A. & Stephens, P.R. (2010) Discordant mitochondrial and nuclear gene phylogenies in emydid turtles: implications for speciation and conservation. Biological Journal of the Linnean Society, 99, 445–461.