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Phylogenetic Relationships of the European Newts (Genus Triturus ) Tested With Contributions to Zoology, 68 (2) 73-81 (1999) SPB Academic Publishing bv, The Hague Phylogenetic relationships of the European newts (genus Triturus ) tested with mitochondrial DNA sequence data I. Zajc ¹ & J.W. Arntzen² Department of Zoology, Leicester University, Leicester LEI 7RH, United Kingdom Present addresses: 'National Institute ofBiology, Vecna pot 111, P.O. Box 141, 1001 Ljubljana, Slovenia department of Zoology and Anthropology, Faculty of Sciences, University of Porto, CECA/ICETA/UP. Campus Agrdrio de Vairdo, 4480 Vila do Conde, Portugal Keywords : 12S rRNA, ATPase, mitochondrial DNA, newt, phylogeny, Triturus Abstract Introduction Phylogenies are a cornerstone to the study of evo- European newts (genus Triturus) are widely studied, but their lution: without them we are unable to reconstruct phylogeny is not yet unambiguously resolved. Fragments of and understand and mitochondrial DNA experiencing different rates of evolution pattern process of evolution- and to (the ATPase 12S rRNA were in order To robust genes) sequenced ary change. obtain a phylogenetic hy- test a phylogenetic hypothesis derived from biochemical and pothesis requires the gathering of multiple inde- behavioral data. Well-supported branches of the existing and data pendent complementary sets, because usu- phylogeny gainedsupport in our study. The monophyletic origin ally no single data set is sufficiently powerful to ofthe hypothesized T. boscai — T. italicus clade remained am- resolve older and more biguous, whereas strong support was gainedfor the sister-taxon simultaneously recent of of relationship T. vulgaris and T. montandoni. The position cladogenetic events. T. sister the T. vittatus as a taxon to marmoratus species group The genus Triturus (European newts) has been was also supported. The phylogenetic position of T. alpestris the subject of extensive phylogenetic analysis with could not be clarified. With an in-group taxon sampling den- various data sets [osteological 1928; ser than in previous molecular phylogenetic studies and under (Bolkay, a selection of from Rafmski and Pecio, 1989), the priori species the genera Cynops, Neurer- immunological (Busack gus and Paramesotriton as out-groups, the monophyly ofTriturus et al., 1988), morphological (Giacoma and Balletto, was It cannot be excluded, however, that strongly supported. 1988), biochemical (Rafmski and Arntzen, 1987), the presumed out-group actually belongs to the in-group, render- behavioral and (Arntzen Sparreboom, 1989), cy- ing Triturus paraphyletic as was concluded from recently pub- et al., and is con- lished 12S 16S rRNA data. togenetic (Macgregor 1990)], and sequence sidered by some to be the phylogenetically best in the studied genus world (Halliday and Arano, 1991). Despite these concerted efforts, its phylog- Contents eny is not fully resolved and several competing with hypotheses are available, none of them un- ambiguous overall support. We take the study by Abstract 73 Arntzen and Sparreboom (1989) as the basis of Introduction 73 our work because the phylogeny they present is Materials and methods 74 based on two independent and complementary data Results 75 sets. Moreover, their resolves the ear- Discussion 78 hypothesis lier well the later events in Triturus Acknowledgements 80 as as the ra- References 80 diation and is robust under the jack-knife test. 74 I. Zajc & J. W. Arntzen — Phytogeny of European newts some behavioral synapomorphies; 5) the mono- phyly of Triturus, traditionally taken for granted, has been put in doubt by molecular data (Titus and Larson, 1995). We tested the phylogenetic hypothesis of Triturus with a newly generated set of independent data. Two fragments of the mitochondrial (mt)DNA molecule experiencing different evolutionary rates were studied. The slowly evolving 12S rRNA gene (Kocher et ah, 1989; Hickson et al., 1996) was partially sequenced to test some of the supposedly earlier events of the Triturus radiation, while the fast evolving ATPase gene (Kumar, 1996) was partially sequenced to test the branching order some related among supposedly closely species in the T. vulgaris species group. Sequence data for b for the based on available cytochrome produced ambiguous phyloge- Fig. I. Phylogeny genus Triturus of biochemical and behavioral characters. Numbers refer to specific netic results, perhaps due to the comparison non- addressed in the text. taxa taken questions as Out-group are homologous sequences (Caccone et al., 1997; cf. from and Paramesotriton. the genera Cynops, Neurergus, Zhang & Hewitt, 1996) and were discarded. Nine or twelve Triturus species are currently Materials and methods recognized, depending on the criteria used for spe- cies recognition. Here we refer to twelve species, Two specimens were selected from each of nine with four of them (Triturus cristatus, T. carnifex, Triturus species, if possible from different locali- T. karelinii and T. dobrovicus) grouped together ties. As out-groups to the genus, representatives in the T. cristatus superspecies (Wallis and Arntzen, of the salamandrid genera Cynops, Neurergus and 1989). The ‘big’- and ‘medium-sized’ newts (T. Paramesotriton were selected, following Arntzen T. T. T. Triturus cristatus, marmoratus, vittatus and alpestris) and Sparreboom (1989). boscai was taken are organized in the subgenus Triturus and the as out-group to the T. vulgaris species group. Speci- ‘small-bodied’ newts (T. boscai, T. helveticus, T. mens for which DNA was extracted were sampled italicus, T. montandoniand T. vulgaris) are placed as follows: T. alpestris from Mayenne, France and in the subgenus Palaeotriton. The detailed con\ Pola de Sierra, Spain (subspecies cyreni)\ T. boscai figuration is given in Fig. 1, alongside with the from Toledo, Spain; T. cristatus from Limanowa, For T. from nomenclature that we adopt. the following Poland and Sinaia, Romania; helveticus sections of the phylogenetic tree the support is Ambleteuse, France and Canterbury, U. K.; T. itali- limited or contradictory: 1) the sister-taxon status cus from Conversano, Italy; T. marmoratus from of T. vulgaris and T. montandoni is supported by El Berrueco near Madrid, Spain and Rochechouart, allozymc data only; 2) the monophyly of T. boscai France; T. montandoni from Ustrzyki, Poland; T. and T. italicus hinges on the interpretation given vittatus from an unknown locality in Israel and to behavioral characters; 3) the status of T. vittatus from Adapazari, Turkey (subspecies ophryticus) as the sister taxon of the T. marmoratus species and T. vulgaris from Ambleteuse, France. Out- be called group may into question on the basis of group taxa Cynops ensicauda, Neurergus strauchii its overall to Paramesotriton from similarity some small-bodied spe- and sp. were obtained the T. the for trade cies, vulgaris in particular; 4) support pet with no reliable locality information. the position of T. alpestris in the subgenus Triturus Total DNA was extracted from approximately is weak due the relatively to non-independence of 50 mg of frozen or ethanol-preserved tissue (liver, Contributions to Zoology, 68 (2) - 1999 75 heart or tail muscle) following standard protocols mesotriton, Pleurodeles, Salamandra, Salaman- (Sambrook et ah, 1989). For PCR-amplification drina, Taricha and Tylototriton. of the 12S rRNA region the forward (L2475) and Phylogenetic reconstruction was performed under reverse (H2897) ‘universal’ primers were used the principle of parsimony, using the PAUP 3.1.1 with the ’branch-and- (Kocher et ah, 1989). The forward and reverse software (Swofford, 1991) ATPase primers L9858 (s'-CTCCTCCTTAATGA- bound’ search option (the ‘heuristic search’ method TATGCCACA-3') and H 10307 (3'-TTCACCCCA- was used in the bootstrap runs). Two a priori se- in ACTACCCAACTATC-s') were designed our lected strategies were followed. First, a uniform laboratory by G. Rowe. Double stranded DNA am- transition - transversion ratio and uniform posi- plifications were performed using standard PGR tional ratio was used, i.e., ‘no weighting’. Sec- protocols (Erlich, 1989) with negative controls to ond, different weights were assigned to transitions test rRNA for contamination. The 12S fragment versus transversions inversely proportional to the was amplified under stringent conditions (anneal- frequency of different substitutions among in-group ing temperature 65°C, extension time 25 seconds, taxa as traced from the tree obtained with the un- up to 28 cycles), while the ATPase primers re- weighted approach, with 24 as the base number. quired milder conditions (annealing temperature Gap derived character-state changes were given 45-50°C, extension time of 60 seconds, minimum the same weight as transversions, also on an apriori of basis. Positional 30 cycles). The amplified products were sepa- weighting factors for the first, sec- rated and the third codon determined on 1.5% low melting point agarose gels, cut ond, positions were out of the gel and purified by successive phenol, for the protein coding DNA fragment (ATPase) phenol-chloroform and chloroform-isoamylalcohol in a similar way. Bootstrap scores (Felsenstein, extractions, followed by ethanol precipitation. Both 1985; Hillis and Bull, 1993) were determined over 5000 obtain strands were directly sequenced using the dideoxy replications to an impression of the chain-termination method (Sanger et ah, 1977). strength of support from the data for the phyloge- with Clustal-V netic maximum Multiple sequences were aligned tree showing parsimony. Temple- software (Higgins and Sharp, 1988) with manual
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