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Molecular Phylogenetic Analysis of Relationships of the Tropical Salamander Genera Oedipina and Nototriton, with Descriptions of a New Genus and Three New Species

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Molecular Phylogenetic Analysis of Relationships of the Tropical Salamander Genera Oedipina and Nototriton, with Descriptions of a New Genus and Three New Species Copeia, 2000(1), pp. 42±70 Molecular Phylogenetic Analysis of Relationships of the Tropical Salamander Genera Oedipina and Nototriton, with Descriptions of a New Genus and Three New Species MARIO GARCIÂA-PARIÂSANDDAVID B. WAKE Sequences of two mitochondrial genes (385 base pairs of cytochrome b and ap- proximately 520 base pairs of 16S DNA) were gathered for 26 taxa of the Middle American plethodontid salamander genera Nototriton and Oedipina and from three outgroup members of the tribe Bolitoglossini. Phylogenetic analyses of these data reveal well-supported cladistic structure and demonstrate the paraphyly of the moss salamanders of the genus Nototriton, which includes two well-de®ned clades. One clade, the sister taxon of Oedipina, corresponding to the Costa Rican and Honduran species of the picadoi, richardi, and barbouri groups, retains the name Nototriton.A new name is required for the second clade, the sister taxon of Oedipina plus Noto- triton (sensu stricto). This clade, which we name Cryptotriton, is well supported mor- phologically and includes the species of the nasalis and adelos groups. A new species of Nototriton from Monteverde, Costa Rica, is described as Nototriton gamezi. Species of Oedipina fall into two clades that we treat as subgenera. Oedipina (sensu stricto) includes the longer-bodied, generally more slender and darker colored species and is the more speciose clade. Oedopinola includes the shorter-bodied, generally more robust and lighter-colored species. Two new species of the latter clade are described, Oedipina maritima from the lowlands of northwestern PanamaÂ, and Oedipina savagei, from uplands of southwestern Costa Rica. HE evolutionary radiation of bolitoglossine of the genus Nototriton were used as outgroups, T salamanders in tropical America resulted following the phylogenetic hypotheses of Wake in an enormous diversi®cation of morphology and Elias, 1983). Two major clades were found. and ecology, ranging from large, robust terres- The ®rst includes the species O. alleni and O. trial forms (e.g., Pseudoeurycea bellii) to diminu- parvipes, which corresponds to the short-bodied tive moss dwelling forms (e.g., Nototriton abscon- and often white-headed species of the O. parvi- dens). One of the most strikingly derived mor- pes group, for which the name Oedopinola phologies within the bolitoglossines is displayed (which we treat here as a subgenus) is available by the genus Oedipina, which comprises 18 cur- (Hilton, 1949). A second group includes the re- rently recognized species distributed from Chia- maining species (subgenus Oedipina), all elon- pas and the YucataÂn Peninsula in MeÂxico to gated, black or brown attenuate forms compris- northwestern Ecuador. Oedipina is a well-sup- ing the uniformis group of Brame (1968). The ported monophyletic group (Wake and Elias, electrophoretic evidence (large Nei genetic dis- 1983), characterized as being the only tropical tances, ranging from 0.37 to 2.67 among spe- bolitoglossine salamanders in which body elon- cies) suggests that most species of Oedipina have gation is a consequence of an increase in the had a long independent evolutionary history. number of vertebrae. All bolitoglossine sala- Most of the species of Oedipina studied show a manders with the exception of Oedipina have 14 large number of autapomorphic alleles. trunk vertebrae, whereas Oedipina has from 18 Phylogenetic relationships within the super- to 23 (Wake, 1966; Brame, 1968). Members of genus Bolitoglossa remain largely unresolved, but Oedipina typically are fossorial, and consequent- Nototriton and Oedipina appear to be sister taxa ly they are rarely seen. They range from sea lev- (Wake and Elias, 1983). Oedipina and Nototriton el (throughout their range) to elevations in ex- share a strongly heteromorphic X/Y sex chro- cess of 2200 m in Costa Rica. The status and mosome system (Kezer et al., 1989; Sessions and phylogenetic relationships of many of the spe- Kezer, 1991), also present in Thorius and Den- cies in the genus were clari®ed by Good and drotriton (Sessions and Kezer, 1991), as well as Wake (1997) based on analysis of an extensive several osteological synapomorphies (Wake and allozyme dataset. Their analysis resulted in a Elias, 1983). Nototriton includes diminutive, slen- general phylogenetic hypothesis for relation- der animals which share with Oedipina the pres- ships among the species of Oedipina (members ence of a long tail that considerably exceeds q 2000 by the American Society of Ichthyologists and Herpetologists GARCIÂA-PARIÂS AND WAKEÐNEW TROPICAL SALAMANDERS 43 their snout±vent length and some osteological from small amounts of frozen tissue or protein features (reviewed later in this paper). The spe- extracts using NaCl following a protocol modi- cies of Nototriton typically inhabit hanging moss ®ed from Miller et al. (1988). mats, epiphytic bromeliads, or surface litter and Sequences of the ®rst portion (385 base are distributed in two disjunct regions: (1) the pairs) of the cyt b gene and of the large (16S) geologically ancient core region of nuclear Mid- ribosomal subunit gene (rDNA) were obtained. dle America along the mountains of the Oaxa- Those regions of mtDNA were selected to re- can-Chiapan-Guatemalan-Honduran corridor; cover a maximum of phylogenetic information and (2) the Cordillera Central and northern at all phylogenetic depths. We expect that cyt b Talamancan region of Costa Rica. Good and evolves more rapidly than 16S; thus, it is ex- Wake (1993) revised the Costa Rican species of pected to be more useful in determining rela- the genus. The genus has been suspected to be tionships of terminal taxa, whereas 16S should paraphyletic (following Wake and Elias, 1983), be more useful for resolving basal relationships and relationships among the picadoi, richardi, (Mindell and Honeycutt, 1990; Hillis and Dix- nasalis and adelos species groups (Papenfuss and on, 1991; Tan and Wake, 1995). Wake, 1987) remain unresolved. Nei's genetic Fragments extending from the third position distances among Costa Rican species range be- of codon 7 through codon 135 of the Xenopus tween 0.14 and 1.18, and phylogenetic analysis cyt b gene (Roe et al., 1985), and approximately of the allozyme data supports recognition of a 520 bp of the 16S rDNA gene corresponding to picadoi group (with four species) and a richardi positions 2510±3059 in the human mitochon- group (with two species) for the Costa Rican drial genome (Anderson et al., 1981), were am- segment of the genus (Good and Wake, 1993). pli®ed via the polymerase chain reaction (PCR; All Honduran, Guatemalan, and Chiapan spe- Saiki et al., 1988) using the primers cyt b-2 (Ko- cies (only four were known to Papenfuss and cher et al., 1989) and MVZ15 (Moritz et al., Wake, 1987) were included in the nasalis group. 1992) for cyt b, and 16Sar-L and 16Sbr-H (Pal- In this paper, we generate new phylogenetic umbi et al., 1991) for 16S. PCR reactions con- hypotheses for Nototriton and Oedipina based on sisted of 38 cycles with a denaturing tempera- partial DNA sequences from two mitochondrial ture of 92 C (1 min), annealing at 48±50 C (1 genes, the cytochrome b (cyt b) encoding gene min) and extension at 72 C (1 min) in a Techne and 16S rDNA. We examine the data for the two PHC-1 thermocycler. PCR reactions were run in genes separately and analyze congruence a total volume of 25 ml, using 0.6 units of Taq among hypotheses generated from the two mi- polymerase (Cetus) in tubes containing 0.5 tochodrial datasets. A combined mitochondrial pmol of each primer, 0.75 mM dNTPs, and 1.5 hypothesis is used to test previous allozyme and mM MgCl2 in a pH 8.4 buffer with 50 mM KCL morphological hypotheses. We show that Noto- and 10 mM Tris HCl (®nal concentrations). triton as presently constituted is paraphyletic, Both heavy and light primers were used for PCR and we place some northern species of the cur- ampli®cations and sequencing. rent genus in a new genus. Phylogenetic analysis Double-stranded templates were cleaned us- reveals several new candidate populations for ing MicroSpin S-300 HR columns (Pharmacia species status, and three species are described Biotech). Four ml of double-strand product as new. were used as the template for cycle sequencing reactions in 10 ml total volume with the Perkin y MATERIALS AND METHODS Elmer Ready Reaction Kit to incorporate dye- labeled dideoxy terminators. Thermal cycling Isolation, ampli®cation, and sequencing of DNA.Ð was performed using standard conditions. Cycle A total of 78 specimens representing most of sequencing products were puri®ed using etha- the known geographic range of Oedipina and nol precipitation and separated by electropho- Nototriton were included in the DNA study. resis on a 6% polyacrylamide gel using an ABI These represent 17 taxa (two described herein) 377 DNA sequencer (Applied Biosystems). of Oedipina and 12 taxa (one described herein) of Nototriton. Many of these were used in the Sequence alignment and phylogenetic analysis.ÐPar- allozymic studies of Good and Wake (1993, tial sequences of cyt b were read from both 1997). We have determined that the taxon iden- strands and aligned to each other by eye in the ti®ed as O. ignea by Good and Wake (1997) is program Sequence Navigatory (vers. 1.0.1, Ap- more appropriately assigned to O. stenopodia. plied Biosystems). The resulting partial 16S se- Localities of origin, museum collection num- quences were checked and aligned using CLUS- bers and GenBank accession numbers are given TAL in the program Sequence Navigatory in Appendix 1. Genomic DNA was extracted (vers. 1.0.1, Applied Biosystems). Computer- 44 COPEIA, 2000, NO. 1 generated alignments were re®ned by eye and of two tropical bolitoglossine genera, Bolitoglossa by comparing them to published secondary cerroensis and Dendrotriton rabbi, were used as se- structure models for 16S (Guttel and Fox, 1988; quential outgroups.
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