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Phylogenetic Systematics of Dart-Poison Frogs and Their Relatives (Amphibia: Athesphatanura: Dendrobatidae)

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Phylogenetic Systematics of Dart-Poison Frogs and Their Relatives (Amphibia: Athesphatanura: Dendrobatidae) PHYLOGENETIC SYSTEMATICS OF DART-POISON FROGS AND THEIR RELATIVES (AMPHIBIA: ATHESPHATANURA: DENDROBATIDAE) TARAN GRANT,1,2 DARREL R. FROST,1 JANALEE P. CALDWELL,3 RON GAGLIARDO,4 CE´ LIO F. B. HADDAD,5 PHILIPPE J. R. KOK,6 D. BRUCE MEANS,7 BRICE P. NOONAN,8 WALTER E. SCHARGEL,9 AND WARD C. WHEELER10 1Division of Vertebrate Zoology (Herpetology), American Museum of Natural History (TG: [email protected]; DRF: [email protected]). 2Department of Ecology, Evolution, and Environmental Biology, Columbia University, New York, NY 10027. 3Sam Noble Oklahoma Museum of Natural History and Department of Zoology, University of Oklahoma, Norman, OK 73072 ([email protected]). 4Curator of Tropical Collections, The Dorothy C. Fuqua Conservatory, Atlanta Botanical Garden, 1345 Piedmont Avenue, Atlanta, GA 30309 ([email protected]). 5Departamento de Zoologia, I.B., Universidade Estadual Paulista (UNESP), Caixa Postal 199, 13.506-900 Rio Claro, SP, Brazil ([email protected]). 6Vertebrates Department (Herpetology), Royal Belgian Institute of Natural Sciences, Rue Vautier 29, B-1000 Brussels, Belgium ([email protected]). 7Coastal Plains Institute and Land Conservancy, 1313 Milton Street, Tallahassee, FL 32303; and Department of Biological Sciences, Florida State University, Tallahassee, FL 32306 ([email protected]). 8Brigham Young University, Department of Integrative Biology, Provo, UT 84602 ([email protected]). 9Department of Biology, The University of Texas at Arlington, TX 76019 ([email protected]). 10Division of Invertebrate Zoology, American Museum of Natural History([email protected]). BULLETIN OF THE AMERICAN MUSEUM OF NATURAL HISTORY CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024 Number 299, 262 pp., 79 figures, 37 tables, 8 appendices Issued August 15, 2006 Copyright E American Museum of Natural History 2006 ISSN 0003-0090 Frontispiece. Adelphobates castaneoticus (Caldwell and Myers, 1990), the type species of Adelphobates n.gen., named for Charles W. Myers and John W. Daly in recognition of the enormity of their contribution to the scientific knowledge of dart-poison frogs. CONTENTS Abstract ....................................................... 6 Introduction . ...................................................... 6 History of Dendrobatid Systematics. .................................... 9 Part I: 1797–1926, Early History . ................................... 10 Part II: 1926–Present, Relationships among Dendrobatids . 13 Part III: 1926–Present, Relationships Between Dendrobatidae and Other Frogs . 30 Summary of Historical Review. 37 Phylogenetic Placement of Dendrobatids and Outgroup Sampling . 39 Theoretical Background ............................................ 39 Empirical Background. 39 Outgroup Sampling................................................ 43 Materials and Methods. 44 Conventions and Abbreviations ....................................... 44 General Analytical Approach: Theoretical Considerations . 45 Choice of Phylogenetic Method . 45 Sources of Evidence. 46 Nucleotide Homology and the Treatment of Indels ....................... 47 Total Evidence . 48 General Analytical Approach: Implementation . 49 Taxon Sampling . 49 Phenotypic Character Sampling . ................................... 49 Genotypic Character Sampling . ................................... 53 Laboratory Protocols. ............................................ 55 Molecular Sequence Formatting . 56 Total Evidence Analysis. 56 Heuristic Character Optimization . 58 Heuristic Tree Searching .......................................... 58 Heuristic Data Exploration ........................................ 60 Species Identification . 60 Phenotypic Characters ............................................... 62 Results........................................................ 117 General Results . 117 Dendrobatid Monophyly and Outgroup Relationships . 118 Relationships among Dendrobatids . .................................. 120 Summary of Relationships among Dendrobatids . 145 A Monophyletic Taxonomy. .......................................... 146 Preliminary Considerations . 146 The Higher-Level Taxonomy of Athesphatanura Frost et al., 2006 . 150 Centrolenidae Taylor, 1951 . 151 Cruciabatrachia new taxon ...................................... 151 Leptodactylidae Werner, 1896 (1838) ............................. 151 Chthonobatrachia Frost et al., 2006. 152 Ceratophryidae Tschudi, 1838 . 152 Batrachylinae Gallardo, 1965 ............................... 152 Ceratophryinae Tschudi, 1838 .............................. 152 Telmatobiinae Fitzinger, 1843 . 153 Hesticobatrachia Frost et al., 2006 ............................. 153 Cycloramphidae Bonaparte, 1850 ............................ 153 Calamitophrynia new taxon ................................ 154 Leiuperidae Bonaparte, 1850 ............................. 154 Agastorophrynia Frost et al., 2006 . 154 4 2006 GRANT ET AL.: PHYLOGENETICS OF DART-POISON FROGS 5 Bufonidae Gray, 1825 . 154 Nobleobatia new taxon ................................ 155 Hylodidae Gu¨nther, 1858 . 156 Dendrobatoidea Cope, 1865 . 156 The Taxonomy Dendrobatoidea Cope, 1865. 157 Aromobatidae new family .......................................... 157 Anomaloglossinae new subfamily ................................... 158 Anomaloglossus new genus ...................................... 158 Rheobates new genus .......................................... 159 Aromobatinae new subfamily ...................................... 160 Aromobates Myers, Paolillo, and Daly, 1991 . 160 Mannophryne La Marca, 1991 . 161 Subfamily: Allobatinae new subfamily ................................ 161 Allobates Zimmermann and Zimmermann, 1988. 162 Dendrobatidae Cope, 1865 ......................................... 163 Colostethinae Cope, 1867 ........................................ 163 Ameerega Bauer, 1986 ......................................... 163 Colostethus Cope, 1867 . 165 Epipedobates Myers, 1987. 166 Silverstoneia new genus......................................... 167 Hyloxalinae new subfamily ........................................ 168 Hyloxalus Jime´nez de la Espada, 1871 ‘‘1870’’ . 168 Dendrobatinae Cope, 1865. 169 Phyllobates Dume´ril and Bibron, 1841.............................. 170 Minyobates Myers, 1987. 170 Ranitomeya Bauer, 1988........................................ 171 Adelphobates new genus ........................................ 172 Oophaga Bauer, 1994. 172 Dendrobates Wagler, 1830 . 173 Incertae Sedis and Nomina Dubia . 173 Discussion: Character Evolution . 174 Adult Habitat Selection. 175 Reproductive Amplexus. ........................................... 176 Sex of Nurse Frogs . 176 Larval Habitat and Diet ........................................... 177 Summary and Conclusions ........................................... 179 Acknowledgments . 182 References . 184 Appendix 1: Chronology of Available Species Names Proposed or Currently in Dendrobatoidea, with Original, Current, and Proposed Generic Placement. 204 Appendix 2: Chronology of Available Dendrobatoid Genus-Group Names . 210 Appendix 3: Chronology of Dendrobatoid Family-Group Names . 211 Appendix 4: Numbers and References for Sequences Obtained from Genbank. 211 Appendix 5: Tissue and Sequence Data . 214 Appendix 6: Specimens Examined ...................................... 241 Appendix 7: Phenotypic Data . 247 Appendix 8: Diagnostic DNA Sequence Transformations for Named Clades . 252 ABSTRACT The known diversity of dart-poison frog species has grown from 70 in the 1960s to 247 at present, with no sign that the discovery of new species will wane in the foreseeable future. Although this growth in knowledge of the diversity of this group has been accompanied by detailed investigations of many aspects of the biology of dendrobatids, their phylogenetic relationships remain poorly understood. This study was designed to test hypotheses of dendrobatid diversification by combining new and prior genotypic and phenotypic evidence in a total evidence analysis. DNA sequences were sampled for five mitochondrial and six nuclear loci (approximately 6,100 base pairs [bp]; x¯53,740 bp per terminal; total dataset composed of approximately 1.55 million bp), and 174 phenotypic characters were scored from adult and larval morphology, alkaloid profiles, and behavior. These data were combined with relevant published DNA sequences. Ingroup sampling targeted several previously unsampled species, including Aromobates nocturnus, which was hypothesized previously to be the sister of all other dendrobatids. Undescribed and problematic species were sampled from multiple localities when possible. The final dataset consisted of 414 terminals: 367 ingroup terminals of 156 species and 47 outgroup terminals of 46 species. Direct optimization parsimony analysis of the equally weighted evidence resulted in 25,872 optimal trees. Forty nodes collapse in the strict consensus, with all conflict restricted to conspecific terminals. Dendrobatids were recovered as monophyletic, and their sister group consisted of Crossodactylus, Hylodes, and Megaelosia, recognized herein as Hylodidae. Among outgroup taxa, Centrolenidae was found to be the sister group of all athesphatanurans except Hylidae, Leptodactyidae was polyphyletic, Thoropa was nested within Cycloramphidae, and Ceratophryinae was paraphyletic with respect to Telmatobiinae. Among dendrobatids, the monophyly and content of Mannophryne and Phyllobates were corroborated. Aromobates nocturnus and Colostethus saltuensis were found to be nested within
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