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The Phylogeny of Crested Newts (Triturus Cristatus Superspecies)

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The Phylogeny of Crested Newts (Triturus Cristatus Superspecies) Contributions to Zoology, 76 (4) 261-278 (2007) The phylogeny of crested newts (Triturus cristatus superspecies): nuclear and mitochondrial genetic characters suggest a hard polytomy, in line with the paleogeography of the centre of origin J.W. Arntzen1, G. Espregueira Themudo1,2, B. Wielstra1,3 1 National Museum of Natural History, P. O. Box 9517, 2300 RA Leiden, The Netherlands, [email protected] 2 CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Campus Agrário de Vairão, 4485-661 Vairão, Portugal, [email protected] 3 Institute of Biology Leiden, Leiden University, P.O. Box 9516, 2300 RA Leiden, The Netherlands, wielstra@natu- ralis.nl Key words: allozymes, historical biogeography, mitochondrial DNA-sequences, Triturus macedonicus, Triturus marmoratus, vicariance Abstract tionary lineage and we propose to elevate its taxonomic status to that of a species, i.e., from Triturus c. macedonicus (Karaman, Newts of the genus Triturus (Amphibia, Caudata, Salamandri- 1922) to Triturus macedonicus (Karaman, 1922). dae) are distributed across Europe and adjacent Asia. In spite of its prominence as a model system for evolutionary research, the phylogeny of Triturus has remained incompletely solved. Our Contents aim was to rectify this situation, to which we employed nuclear encoded proteins (40 loci) and mitochondrial DNA-sequence Introduction .................................................................................... 261 data (mtDNA, 642 bp of the ND4 gene). We sampled up to four Materials and methods ................................................................. 263 populations per species covering large parts of their ranges. Al- Sampling strategy ................................................................... 263 lozyme and mtDNA data were analyzed separately with parsi- Allozyme data .......................................................................... 263 mony, distance, likelihood and Bayesian methods of phyloge- Mitochondrial DNA-sequence data .................................... 268 netic inference. Existing knowledge on taxonomic relationships Phylogenetic analysis ............................................................. 268 was confi rmed, including the monophyly of the genus and the Results ............................................................................................. 269 groups of crested newts (four species) and marbled newts (two Allozymes ................................................................................. 269 species). The genetic coherence of species and subspecies was Mitochondrial DNA-sequences ........................................... 270 also confi rmed, but not always with high statistical support (de- Discussion ...................................................................................... 272 pending on taxon, characters under consideration, and method Genetic coherence of species and subspecies ................... 272 of inference). In spite of our efforts we did not obtain suffi cient Phylogeny ................................................................................. 272 phylogenetic signal to prefer one out of twelve potential topolo- Historical biogeography ........................................................ 273 gies representing crested newts relationships. We hypothesize Taxonomic considerations .................................................... 275 that the lack of phylogenetic resolution refl ects a hard polytomy Acknowledgements ...................................................................... 276 and represents the (near)-simultaneous origin of crested newt References ...................................................................................... 276 species. Using a calibration point of 24 Ma (million years before Appendix I ...................................................................................... 278 present) for the most recent common ancestor of Triturus-spe- Appendix II .................................................................................... 278 cies, the crested newt radiation event is dated at 7-6 Ma (sce- nario 1) or at 11-10 Ma (scenario 2), depending on the applica- tion of an allozyme versus mtDNA molecular clock. The fi rst biogeographical scenario involves the spread of crested newts Introduction from the central Balkans into four compass directions. This sce- nario cannot be brought into line with potential vicariance events The newt genus Triturus Rafi nesque, 1815 (Amphibia, for south-eastern Europe. The second scenario involves the Caudata, Salamandridae) is a model group for various more or less simultaneous origin of four species of crested newts lines of evolutionary research, on e.g. locomotion through large-scale vicariance events and is supported by the (Gvozdik and van Damme, 2006), cranial ontogeny paleogeographical reconstruction for the region at the end of the Middle Miocene. The subspecies Triturus carnifex macedonicus (Ivanović et al., 2007), reproductive behaviour (Stein- carries in one large area the mtDNA that is typical for the neigh- fartz et al., 2007) and sexual size dimorphism (A. bouring species T. karelinii, which is attributed to introgression Ivanović, K. Sotiropoulos, M. Furtula, G. Džukić and and a recent range shift. It is nevertheless a long distinct evolu- M.L. Kalezić, submitted). Considering the effi cient use 262 J.W. Arntzen et al. – Phylogeny of crested newts of the ‘comparative method’ that aims to account for (Laurenti, 1768), that is distributed over central, west- non-independence among characters due to shared evo- ern and northern Europe and eastwards deep into Rus- lutionary histories (Harvey and Pagel, 1991), it would sia, T. carnifex (Laurenti, 1768), that occurs on the Ap- seem important that the phylogenetic relationships penine Peninsula and part of the Balkans, T. dobrogi- within the group are well resolved. Despite considera- cus (Kiritzescu, 1903), that is confi ned to the Pannon- ble efforts, starting with the osteological study of Bolkay ian and Dobrogean lowlands, and T. karelinii (Strauch, (1928), an unambiguous phylogenetic resolution for 1870), with a range from the southern Balkans to the Triturus has not been obtained (Arntzen, 2003). Caspian Sea. Triturus carnifex has two allopatric sub- The genus Triturus encompasses six species of so- species, the nominotypical subspecies in the western called ‘large bodied’ newts that are organized in two part and T. c. macedonicus (Karaman, 1922) in the east- groups: the marbled newts with two species and the ern part of the species range, separated by the Adriatic crested newts with four species. Marbled newts are Sea and the area approximately coinciding with Bos- characterized by a dorsal green colouration and a fairly nia-Herzegovina. uniform light grey or black underside. Triturus mar- Given their contiguous parapatric ranges with limit- moratus (Latreille, 1800) occurs in central and south- ed hybridization (Wallis and Arntzen, 1989), the four ern France and the northern part of the Iberian Penin- species of crested newt are conveniently referred to as a sula and T. pygmaeus (Wolterstorff, 1905) is confi ned superspecies (or ‘Artenkreis’) sensu Rensch (1929). to the south-western and southern parts of the Iberian Molecular phylogenetic studies corroborate the mono- Peninsula. Crested newts are characterized by an or- phyly of Triturus and the sistergroup relationship of ange and black spotted ventral colouration and a dark crested and marbled newts (e.g. Zajc and Arntzen, 1999; backside and occupy most other parts of Europe and Steinfartz et al., 2007). Approximate geographical dis- adjacent Asia. Four species are recognized: T. cristatus tributions of Triturus species are shown in Figure 1. Fig. 1. Approximate geographical distribution of Triturus species, represented by the following colours: orange - T. carnifex, red - T. crista- tus, blue - T. dobrogicus, yellow - T. karelinii, dark green - T. marmoratus, light green - T. pygmaeus. Numbers indicate the populations sampled in this study as listed in Appendix I. The concave polygon in the Balkans represents the area where karelinii-type mtDNA was observed in T. carnifex macedonicus (Arntzen and Wallis, 1999 and present study). Note the zone of sympatry between T. cristatus and T. marmoratus in western France. Contributions to Zoology, 76 (4) – 2007 263 The monophyly of the genus Triturus is strongly fall within the species for which they are recognized. supported by a number of synapomorphic character The aforementioned ‘NRBV-constraint’ equals to tree states (Arntzen, 2003), including a remarkable genetic number 10. In the present study, we set out to elucidate condition that kills off all embryos that are homomor- the phylogenetic relationships of the genus Triturus phic for either the long or the short copy of chromo- and in particular the Triturus cristatus superspecies. some-1, the so-called ‘chromosome-1 syndrome’ (Rid- For this purpose, we employ the independent datasets ley, 1993). The small- and medium-sized newt species of nuclear encoded protein data and mtDNA-sequence (alpestris, vittatus, vulgaris and allies), traditionally data. included in Triturus have recently been placed in gen- era of their own (García-París et al., 2004; Steinfartz et al., 2007). Material and methods Adult crested newts can be organized in a morpho- logical series from a stocky built with well-developed Sampling strategy appendages in T. karelinii, to a slender built with short appendages in T. dobrogicus, with
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