TY - JOUR
T1 - Phylogenetic relationships of glassfrogs (Centrolenidae) based on mitochondrial and nuclear genes
AU - Guayasamin, Juan M.
AU - Castroviejo-Fisher, Santiago
AU - Ayarzagüena, José
AU - Trueb, Linda
AU - Vilà, Carles
N1 - Funding Information:
We are grateful to many individuals and institutions who provided the specimens, permits, and tissues necessary for this study (for abbreviations see Appendix A )—Luis A. Coloma, Martín R. Bustamante, Italo Tapia, Néstor Acosta, Diego Almeida-Reinoso (QCAZ), Celsi Señaris, Gilson Rivas, Carlos Lasso (MHNLS), Marco Rada (Conservation International-Colombia), William E. Duellman, John E. Simmons (KU), John D. Lynch (ICN), Roy W. McDiarmid, James A. Poindexter, Ron Heyer, Addison Wynn (USNM), Julián Faivovich, Taran Grant, Linda S. Ford (AMNH), Maureen A. Donnelly (Florida International University, USA), S. Blair Hedges (Penn State University, USA), James Hanken, José Rosado (MCZ), Brice P. Noonan (Brigham Young University, Provo, USA), Roberto Ibáñez (Universidad de Panamá), Margarita Medina, Karen Siu Ting, César Aguilar (MHNSM), Karl-Heinz Jungfer (Geobotanisches Institut, Switzerland), Gerardo Chavéz, Federico Bolaños (UCR), Kirsten E. Nicholson (Washington University in St. Louis, USA), Diego F. Cisneros-Heredia (USFQ), Edgar Lehr (MTD), Jonathan A. Campbell, Paul C. Ustach (UTA), Alan Resetar (FMNH), Paul Gutiérrez (MHUA), Ignacio De la Riva, José Manuel Padial (MNCN), Juan Carlos Chaparro (MHNC), César Barrio-Amorós (Fundación Andígena, Venezuela), Raffael Ernst, Ardiel Quintana (SMNS), Gunther Köehler (SMF), Rodrigo Aguayo (CBG), Andrew J. Crawford (Smithsonian Research Tropical Institute, Panama), Enrique La Marca (ULABG), Robert-Jan den Tex (Uppsala University, Sweden), Koos van Egmond (RMNH), Barry Clarke (BM), and Michel Blanc. For assistance during fieldwork, we thank Elisa Bonaccorso, Martín R. Bustamante, Cesar Barrio-Amorós, Lizi Ernst, Handel Guayasamin, Justo González, Emira Sánchez, Antonio Bonaccorso, Juan F. Freile, José Ruiz, José María Castroviejo, Rafael Antelo, Daniel González, Enrique Ávila, Ignacio De la Riva, José Manuel Padial, Jaime Bosch, Juan Carlos Chaparro, Márcos Natera and Gilson Rivas. The work of SCF in Venezuela would have not been possible without the continuous help of Rafael Antelo. Special thanks to Julián Faivovich for providing sequences of Hyalinobatrachium eurygnathum. Research permits in Ecuador were issued by the Ministerio del Ambiente (#033-IC-FAU-DNBAPVS/MA) and in Peru by authorization 008-2005 of INRENA-IFFS-DCB. This study is included in the “Contrato Marco de Acceso a Recursos Genéticos N° 0001, 11 Enero 2007” subscribed between Fundación La Salle de Ciencias Naturales and the Ministerio del Ambiente, Venezuela. John J. Wiens provided us with primers and PCR protocols prior to their publication. J.M.G. thanks John D. Lynch, Marco Rada, and Angela Suárez for their hospitality during specimen examination in Colombia. Luis F. García provided workspace and supplies during J.M.G.’s molecular work in Colombia. Michael Alfaro, Hugo Alamillo, and Barb Banbury facilitated access to the computer cluster at Washington State University for some of the final analyses. We are indebted to Jeet Sukumaran for his input, time, and patience, especially when dealing with the runs in the KUNHM computational cluster. This work was supported by grants from the National Science Foundation (Doctoral Dissertation Improvement Grant DEB–0608011: LT, JMG; EF–0334928: LT), the American Philosophical Society through the Lewis and Clark Fund for Exploration and Field Research (JMG), Panorama Society Grant and Harris Scholarship Award of the University of Kansas Natural History Museum (JMG), Estación Biológica El Frío (SCF, CV, and JA), Asociación Amigos de Doñana and its director J. Castroviejo Bolíbar (SCF, CV, and JA), Stiftelsen Sven och Lilly Lawskis (SCF), Helge Ax:son Johnsons Stiftelse Foundation (SCF), Synthesis Project (European Union) ES-TAF-2827 and NL-TAF-4090 (SCF), Sederholms’ stipend (SCF), The Royal Swedish Academy of Science (SCF), and the Swedish Research Council (CV and SCF). The manuscript was greatly improved by discussions and comments from several people, including Elisa Bonaccorso, Rafe Brown, William E. Duellman, Edward O. Wiley, Kevin de Queiroz, Andrew T. Peterson, Charles Linkem, Omar Torres-Carvajal, Jeet Sukumaran, Jennifer A. Leonard, Ignacio De la Riva, José Manuel Padial, Allan Larson, and three anonymous reviewers. Very special thanks go to Elisa Bonaccorso for her help, patience, and input during this and other projects of her negrito (=JMG).
PY - 2008/8
Y1 - 2008/8
N2 - Glassfrogs (family Centrolenidae) represent an exceptionally diverse group among Neotropical anurans, but their evolutionary relationships never have been assessed from a molecular perspective. Mitochondrial and nuclear markers were used to develop a novel hypothesis of centrolenid phylogeny. Ingroup sampling included 100 terminals, with 78 (53%) of the named species in the family, representing most of the phenotypic diversity described for the group. Thirty-five species representing taxa traditionally associated with glassfrogs were used as outgroups. Gene sampling consisted of complete or partial sequences of three mitochondrial (12S, 16S, ND1) and three nuclear markers (c-myc exon 2, RAG1, POMC) for a total of ∼4362 bp. Phylogenies were estimated using maximum parsimony, maximum likelihood, and Bayesian analyses for individual genes and combined datasets. The separate analysis of mitochondrial and nuclear datasets allowed us to clarify the relationships within glassfrogs; also, we corroborate the sister-group relationship between Allophryne ruthveni and glassfrogs. The new phylogeny differs significantly from all previous morphology-based hypotheses of relationships, and shows that hypotheses based on few traits are likely to misrepresent evolutionary history. Traits previously hypothesized as unambiguous synapomorphies are shown to be homoplastic, and all genera in the current taxonomy (Centrolene, Cochranella, Hyalinobatrachium, Nymphargus) are found to be poly- or paraphyletic. The new topology implies a South American origin of glassfrogs and reveals allopatric speciation as the most important speciation mechanism. The phylogeny profoundly affects the traditional interpretations of glassfrog taxonomy, character evolution, and biogeography-topics that now require more extensive evaluation in future studies.
AB - Glassfrogs (family Centrolenidae) represent an exceptionally diverse group among Neotropical anurans, but their evolutionary relationships never have been assessed from a molecular perspective. Mitochondrial and nuclear markers were used to develop a novel hypothesis of centrolenid phylogeny. Ingroup sampling included 100 terminals, with 78 (53%) of the named species in the family, representing most of the phenotypic diversity described for the group. Thirty-five species representing taxa traditionally associated with glassfrogs were used as outgroups. Gene sampling consisted of complete or partial sequences of three mitochondrial (12S, 16S, ND1) and three nuclear markers (c-myc exon 2, RAG1, POMC) for a total of ∼4362 bp. Phylogenies were estimated using maximum parsimony, maximum likelihood, and Bayesian analyses for individual genes and combined datasets. The separate analysis of mitochondrial and nuclear datasets allowed us to clarify the relationships within glassfrogs; also, we corroborate the sister-group relationship between Allophryne ruthveni and glassfrogs. The new phylogeny differs significantly from all previous morphology-based hypotheses of relationships, and shows that hypotheses based on few traits are likely to misrepresent evolutionary history. Traits previously hypothesized as unambiguous synapomorphies are shown to be homoplastic, and all genera in the current taxonomy (Centrolene, Cochranella, Hyalinobatrachium, Nymphargus) are found to be poly- or paraphyletic. The new topology implies a South American origin of glassfrogs and reveals allopatric speciation as the most important speciation mechanism. The phylogeny profoundly affects the traditional interpretations of glassfrog taxonomy, character evolution, and biogeography-topics that now require more extensive evaluation in future studies.
KW - Anura
KW - Biogeography
KW - Centrolenidae
KW - Evolution
KW - Homoplasy
KW - Monophyly
KW - Neotropics
KW - Phylogeny
KW - Speciation
UR - http://www.scopus.com/inward/record.url?scp=47749083474&partnerID=8YFLogxK
U2 - 10.1016/j.ympev.2008.04.012
DO - 10.1016/j.ympev.2008.04.012
M3 - Artículo
C2 - 18515151
AN - SCOPUS:47749083474
SN - 1055-7903
VL - 48
SP - 574
EP - 595
JO - Molecular Phylogenetics and Evolution
JF - Molecular Phylogenetics and Evolution
IS - 2
ER -