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The Phylogeny of Poison Dart Frogs (Amphibia: Anura: Dendrobatidae) Taran Grant Submitted in Partial Fulfillment of the Require

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The Phylogeny of Poison Dart Frogs (Amphibia: Anura: Dendrobatidae) Taran Grant Submitted in Partial Fulfillment of the Require The Phylogeny of Poison Dart Frogs (Amphibia: Anura: Dendrobatidae) Taran Grant Submitted in partial fulfillment of the Requirements for the degree of Doctor of Philosophy in the Graduate School of Arts and Sciences COLUMBIA UNIVERSITY 2005 © 2005 Taran Grant All Rights Reserved Nomenclatural Disclaimer The taxonomic changes presented herein, including new taxa, combinations, and synonymy, are disclaimed as nomenclatural acts and are not available, in accordance with Article 8.3 of the International Code of Zoological Nomenclature. ABSTRACT The Phylogeny of Poison Dart Frogs (Amphibia: Anura: Dendrobatidae) Taran Grant This study was designed to test current knowledge of dendrobatid diversification by performing a total evidence analysis. Evidence included DNA sequences from five mitochondrial and six nuclear loci and 175 phenotypic character transformations of morphology, behavior, and alkaloid profiles. The data set consisted of 412 terminals: 365 terminals of 152 ingroup species and 47 outgroup terminals. Direct optimization parsimony analysis resulted in a single optimal solution. Dendrobatids were recovered as monophyletic, and their sister group consists of Crossodactylus, Hylodes, and Megaelosia. Monophyly was corroborated for Mannophryne and Phyllobates. Aromobates nocturnus and Colostethus saltuensis were found to be nested within Nephelobates and Minyobates to be paraphyletic and nested within Dendrobates. Colostethus was shown to be rampantly nonmonophyletic. A morphologically and behaviorally diverse clade of median lingual process- possessing species was discovered. This study confirmed reports of multiple origins of alkaloid sequestration, and optimization of alkaloid characters allowed detailed explanations and predictions to be advanced. Multiple origins of phytotelm-breeding, larval oophagy, and endotrophy were discovered. Available evidence indicated that dorsal tadpole transport—a dendrobatid synapomorphy—is primitively carried out by male nurse frogs, with three origins of female transport and five origins of biparental transport. A novel approach to heuristic total evidence analysis of DNA partitions was developed. All examined partitions contributed to the individuation of clades across vastly different hierarchic levels, each partition differed in the frequency of transformations at different levels, and the relative amount of evidence contributed by each partition varied across hierarchic levels. Table of Contents Chapter 1: Introduction 1 Chapter 2: History of Dendrobatid Systematics 10 Chapter 3: Phylogenetic Placement of Dendrobatidae and 62 Outgroup Sampling Chapter 4: Materials and Methods 70 Chapter 5: Phenotypic Characters 112 Chapter 6: Results 252 Chapter 7: A Monophyletic Taxonomy 315 Chapter 8: Character Evolution 365 Chapter 9: Summary and Future Directions 403 Literature Cited 413 Appendix 1: Prior Phylogenetic Hypotheses 448 Appendix 2: Chronology of Dendrobatid Family-Group Names 461 Appendix 3: Chronology of Available Genus-Group Names 462 Proposed or Currently in Dendrobatidae Appendix 4: Chronology of Available Species Names Proposed 463 or Currently in Dendrobatidae, with Original, Current, and Proposed Generic Placement Appendix 5: Tissue and Sequence Data 474 Appendix 6: Numbers and References for Sequences Obtained 479 from Genbank i Appendix 7: Specimens Examined 485 Appendix 8: Phenotypic Character Matrix 494 List of Tables Table 4.1. PCR primers used in this study. 93 Table 4.2. Summary of DNA sequence data. 98 Table 4.3. Summary of tree searching methods combined in overall 104 search strategy. Table 6.1. Percent uncorrected pairwise distances between cytochrome 256 b sequences of tepuyensis and BPN3. Table 6.2. Percent uncorrected pairwise distances between cytochrome 258 b sequences of degranvillei from Guiana, praderioi, and the undescribed species ROM1. Table 6.3. Percent uncorrected pairwise distances between cytochrome 259 b sequences of beebei and roraima. Table 6.4. Percent uncorrected pairwise distances between cytochrome 261 b sequences of stepheni baeobatrachus, and undescribed species BPN1 and BPN2. Table 6.5. Percent uncorrected pairwise distances between cytochrome 265 b sequences of syntopic specimens of undulatus. Table 6.6. Percent uncorrected pairwise distances between cytochrome 266 b sequences of talamanae and Magdalena species. Table 6.7. Percent uncorrected pairwise distances between cytochrome 269 ii b sequences of brunneus. Table 6.8. Uncorrected pairwise distances between cytochrome b 269 sequences of RioFormoso2. Table 6.9. Percent uncorrected pairwise distances between cytochrome 272 b sequences of femoralis and zaparo. Table 6.10. Percent uncorrected pairwise distances between cytochrome 274 b sequences of syntopic specimens of caeruleoactylus. Table 6.11. Percent uncorrected pairwise distances between cytochrome 276 b sequences of RioItuxi. Table 6.12. Percent uncorrected pairwise distances between cytochrome 277 b sequences of an undescribed brunneus-like species from Santarem and Curva Una localities in Brazil. Table 6.13. Percent uncorrected pairwise distances between cytochrome 278 b sequences of RioFormoso3. Table 6.14. Percent uncorrected pairwise distances between cytochrome 279 b sequences of conspicuus and a undescribed species form Cuyabeno, Ecuador. Table 6.15. Percent uncorrected pairwise distances between cytochrome 281 b sequences of trilineatus and related undescribed species. Table 6.16. Percent uncorrected pairwise distances between cytochrome 285 b sequences of flotator, nubicola, and punctiventris. Table 6.17. Percent uncorrected pairwise distances between cytochrome 287 b sequences of fraterdanieli. iii Table 6.18. Percent uncorrected pairwise distances between cytochrome 289 b sequences of imbricolus, inguinalis, and two distant localities of panamensis. Table 6.19. Percent uncorrected pairwise distances between cytochrome 290 b sequences of trivittatus. Table 6.20. Percent uncorrected pairwise distances between cytochrome 293 b sequences of hahneli. Table 6.21. Percent uncorrected pairwise distances between cytochrome 296 b sequences of pulcherrimus and sylvaticus. Table 6.22. Percent uncorrected pairwise distances between cytochrome 298 b sequences of Ibagué species. Table 6.23. Percent uncorrected pairwise distances between cytochrome 299 b sequences of idiomelus. Table 6.24. Percent uncorrected pairwise distances between cytochrome 302 b sequences of aurotaenia, bicolor, lugubris, terribilis, and vittatus. Table 6.25. Percent uncorrected pairwise distances between cytochrome 304 b sequences of claudiae, fulguritus, and minutus. Table 6.26. Percent uncorrected pairwise distances between cytochrome 305 b sequences of nominal ventrimaculatus. Table 6.27. Percent uncorrected pairwise distances between cytochrome 306 b sequences of castaneoticus, galactonotus, and quinquevittatus. Table 6.28. Percent uncorrected pairwise distances between cytochrome 308 b sequences of histrionicus, Dendrobates lehmanni, and Dendrobates iv sylvaticus. Table 6.29. Percent uncorrected pairwise distances between cytochrome 309 b sequences of arboreus, pumilio, speciosus, and vicentei. Table 6.30. Percent uncorrected pairwise distances between cytochrome 311 b sequences of azureus and tinctorius. Table 6.31. Percent uncorrected pairwise distances between cytochrome 311 b sequences of auratus and truncatus. List of Figures Figure 2.1. Accumulation of dendrobatid species 1797–2004. 10 Figure 3.1. Phylogenetic placement of Dendrobatidae according 66 to Frost et al. (2005). Figure 4.1. Examples of variation in dendrobatid maxillary teeth. 88 Figure 4.2. Posterior view of several species of dendrobatids, 90 showing cloacal variation. Figure 5.1. Character 0, dorsal skin texture. 113 Figure 5.2. Character 3, distal subarticular tubercle of finger IV. 116 Figure 5.3. Character 4, length of finger IV. 118 Figure 5.4. Characters 7–10 and 31–35, schematic illustration of 121 the four states observed in the expansion of digital discs. Figure 5.5. Characters 11−18, finger fringes. 124 Figure 5.6. Character 19, metacarpal ridge. 126 Figure 5.7. Character 21, morphology of swollen third finger in males. 129 v Figure 5.8. Character 22, male nuptial pad (undulatus, AMNH 159134). 130 Figure 5.9. Character 26, thenar tubercle. 132 Figure 5.10. Character 29, morphology of tarsal keel. 135 Figure 5.11. Character 30, tarsal fringe. 136 Figure 5.12. Character 46, metatarsal fold. 141 Figure 5.13. Character 49, pale paracloacal mark. 143 Figure 5.14. Character 50, dorsal thigh color pattern. 144 Figure 5.15. Character 51, discrete pale proximoventral calf spot. 145 Figure 5.16. Character 52, dorsolateral stripe A. 148 Figure 5.17. Character 53, dorsolateral stripe B. 149 Figure 5.18. Character 54, ventrolateral stripe. 150 Figure 5.19. Character 56, oblique lateral stripe length. 152 Figure 5.20. Character 57, oblique lateral stripe structure. 153 Figure 5.21. Character 58, markings on gular-chest region, 154 state 1 (present). Figure 5.22. Character 59, dermal collar, state 1 (present) in trinitatis. 155 Figure 5.23. Extensive subdermal melanosis of the collar region. 157 Figure 5.24. Character 60, dark lower lip line. 158 Figure 5.25. Character 61, male throat color. 161 Figure 5.26. Character 62, female throat color. 162 Figure 5.27. Character 63, male abdomen color. 164 Figure 5.28. Character 64, female abdomen color. 166 Figure 5.29. Character 65, iris coloration. 169 vi Figure 5.30. Character 66, large intestine color. 170 Figure 5.31. Character 67, adult testis
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