Abstract
Three frogs of a new species found in cloud forests on two nearby mountains in Guyana were included in a molecular phylogeny of 17 nuclear and mitochondrial genes (10,739 aligned sites) that revealed that their closest relative is Terrarana (Brachycephalidae, Craugastoridae, Eleutherodactylidae, and Strabomantidae) and their next-closest relative is Hemiphractidae (marsupial frogs). We place these frogs in a new family, genus, and species which is strongly supported as the basal clade within Terrarana: Ceuthomantidae n. fam., Ceuthomantis smaragdinus n. gen, n. sp. Morphological evidence supports the placement of two other species from the Guiana Highlands, Pristimantis aracamuni (BarrioAmorós & Molina) and P. cavernibardus (Myers & Donnelly), in the new family and genus. This close phylogenetic relationship of terraranans and marsupial frogs, nearly all of which have direct development, supports an hypothesis that direct development evolved early in the evolution of this huge clade (~1000 species), for which we propose the unranked taxonomic epithet Orthobatrachia.References
Alberch, P. & Gale, E.A. (1985) A developmental analysis of an evolutionary trend: digital reduction in amphibians. Evolution, 39, 8–23.
AmphibiaWeb. (2009) AmphibiaWeb: information on amphibian biology and conservation (http://amphibiaweb.org/), accessed: 14 June 2009. University of California, Berkeley, California
Ayarzagüena, J. (1985 “1983”) Una nueva especie de Dischidodactylus Lynch (Amphibia, Leptodactylidae) en la cumbre del Tepui Marahuaca, Territorio Federal Amazonas – Venezuela. Memorias Sociedad de Ciencias Naturales La Salle, 43, 215–220.
Báez, A.M. (2000) Tertiary anurans from South America. In: Heatwole, H. & Carrol, R.L. (Eds.) Amphibian biology, Volume 4: Paleontology. Surrey Beatty & Sons, Chipping Norton, Australia, pp. 1388–1401.
Báez, A.M. & Nicoli, L. (2004) Bufonid toads from the late Oligocene beds of Salla, Bolivia. Journal of Vertebrate Paleontology, 24, 73–79.
Barrio-Amorós, C.L. & Brewer-Cariás, C. (2008) Herpetological results of the 2002 expedition to Sarisariñama, a tepui in Venezuela Guayana, with the description of five new species. Zootaxa, 1942, 3–68.
Barrio-Amorós, C.L. & Molina, C.R. (2006) A new Eleutherodactylus (Anura, Brachycephalidae) from the Venezuelan Guayana, and redescription of Eleutherodactylus vilarsi (Melin). Zootaxa, 1302, 1–20.
Biju, S.D. & Bossuyt, F. (2003) New frog family from India reveals an ancient biogeographical link with the Seychelles. Nature, 425, 711–714.
Blackburn, D.C. (2008) Biogeography and evolution of body size and life history of African frogs: phylogeny of squeakers (Arthroleptis) and long-fingered frogs (Cardioglossa) estimated from mitochondrial data. Molecular Phylogenetics and Evolution, 49, 802–826.
Bossuyt, F. & Milinkovitch, M.C. (2000) Convergent adaptive radiations in Madagascan and Asian ranid frogs reveal covariation between larval and adult traits. Proceedings of the National Academy of Sciences of the United States of America, 97, 6585–6590.
Callery, E.M., Fang, H., & Elinson, R.P. (2001) Frogs without polliwogs: evolution of anuran direct development. Bioessays, 23, 233–241.
Caramaschi, U. & Pombal, J.P., Jr. (2001) Barycholos savagei: a junior synonym of Paludicola ternetzi, with notes on development. Journal of Herpetology, 35, 357–360.
Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17, 540–552.
Catenazzi, A. (2006) Phrynopus cophites. Reproduction. Herpetological Review, 37, 206.
Crawford, A.J. & Smith, E.N. (2005) Cenozoic biogeography and evolution in direct-developing frogs of Central America (Leptodactylidae: Eleutherodactylus) as inferred from a phylogenetic analysis of nuclear and mitochondrial genes. Molecular Phylogenetics and Evolution, 35, 536–555.
Darst, C.R. & Cannatella, D.C. (2004) Novel relationships among hyloid frogs inferred from 12S and 16S mitochondrial DNA sequences. Molecular Phylogenetics and Evolution, 31, 462–475.
De la Riva, I. (2007) Bolivian frogs of the genus Phrynopus, with the description of twelve new species (Anura: Brachycephalidae). Herpetological Monographs, 21, 241–277.
De la Riva, I. & Lynch, J.D. (1997) New species of Eleutherodactylus from Boliva (Amphibia: Leptodactylidae). Copeia, 1997, 151–157.
Doyle, A.C. (1912) The Lost World. Hodder & Stoughten, London, 192 pp.
Dubois, A. (2009) Miscellanea nomenclatorica batrachologica 20. Class-series nomina are nouns in the nominative plural. Alytes, 26, 167–175.
Duellman, W.E. (2007) Amphibian life histories: their utilization in phylogeny and classification. In: Heatwole, H. & Tyler, M. (Eds.) Amphibian Biology, Vol. 7 Systematics. Surrey Beatty & Sons, Chipping Norton, NSW, Australia, pp. 2843–2892.
Duellman, W.E. & Hillis, D.M. (1987) Marsupial frogs (Anura, Hylidae, Gastrotheca) of the Ecuadorian Andes: resolution of taxonomic problems and phylogenetic relationships. Herpetologica, 43, 141–173.
Duellman, W.E. & Pramuk, J.B. (1999) Frogs of the genus Eleutherodactylus (Anura: Leptodactylidae) in the Andes of northern Peru. Scientific Papers Natural History Museum University of Kansas, 13, 1–78.
Duellman, W.E. & Trueb, L. (1986) Biology of Amphibians. McGraw-Hill, New York, 670 pp.
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.
Fabrezi, M. & Alberch, P. (1996) The carpal elements of anurans. Herpetologica, 52, 188–204.
Faivovich, J., Haddad, C.F.B., Garcia, P.C.A., Frost, D.R., Campbell, J.A. & Wheeler, W.C. (2005) Systematic review of the frog family Hylidae, with special reference to Hylinae: phylogenetic analysis and taxonomic revision. Bulletin of the American Museum of Natural History, 294, 1–228.
Frost, D.R., Grant, T., Faivovich, J., Bain, R.H., Haas, A., Haddad, C.F.B., De Sa, R.O., Channing, A., Wilkinson, M., Donnellan, S.C., Raxworthy, C.J., Campbell, J.A., Blotto, B.L., Moler, P., Drewes, R.C., Nussbaum, R.A., Lynch, J.D., Green, D.M. & Wheeler, W.C. (2006) The amphibian tree of life. Bulletin of the American Museum of Natural History, 297, 1–371.
Frost, D.R. (2009) Amphibian species of the World: an online reference. Version 5.3 (http://research.amnh.org/herpetology/amphibia/index.php/), accessed 14 May 2009. American Museum of Natural History, New York.
Gluesenkamp, A.G. & Acosta, N. (2001) Sexual dimorphism in Osornophryne guacamayo with notes on natural history and reproduction in the species. Journal of Herpetology, 35, 148–151.
Grant, T., Frost, D.R., Caldwell, J.P., Gagliardo, R., Haddad, C.F.B., Kok, P.J.R., Means, D.B., Noonan, B.P., Schargel, W.E. & Wheeler, W.C. (2006) Phylogenetic systematics of dart-poison frogs and their relatives (Amphibia: Athesphatanura: Dendrobatidae). Bulletin of the American Museum of Natural History, 299, 1–262.
Guayasamin, J.M., Castroviejo-Fisher, S., Ayarzagüena, J., Trueb, L., & Vilà, C. (2008) Phylogenetics of glassfrogs (Centrolenidae) based on mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution, 48, 574–595.
Guayasamin, J.M., Castroviejo-Fisher, S., Trueb, L., Ayarzagüena, J., Rada, M., & Vilà, C. (2009) Phylogenetic systematics of glassfrogs (Amphibia: Centrolenidae) and their sister taxon Allophryne ruthveni. Zootaxa, 2002, 1–97.
Hanken J., Jennings, D.H., & Olsson, L. (1997) Mechanistic basis of life-history evolution in anuran amphibians: direct development. American Zoologist, 37, 160–171.
Heath, T.A., Hedtke, S.M. & Hillis, D.M. (2008) Taxon sampling and the accuracy of phylogenetic analyses. Journal of Systematics and Evolution, 46, 239–257.
Heatwole, H. (1962) Contributions to the natural history of Eleutherodactylus cornutus maussi. Stahlia, 2, 1–7.
Hedges, S.B. (1989) Evolution and biogeography of West Indian frogs of the genus Eleutherodactylus: slow-evolving loci and the major groups. In C.A. Woods (Ed.), Biogeography of the West Indies: past present and future. Sandhill Crane Press, Gainesville, Florida, pp. 305–370.
Hedges, S.B. (1996) The origin of West Indian amphibians and reptiles. In Powell, R. & Henderson, R.W. (Eds.), Contributions to West Indian herpetology: a tribute to Albert Schwartz. Society for the Study of Amphibians and Reptiles, Ithaca, New York, pp. 95-128.
Hedges, S. B. (2003) The coelacanth of frogs. Nature, 425, 669–670.
Hedges, S.B., Duellman, W.E., & Heinicke, M.P. (2008) New World direct-developing frogs (Anura: Terrarana): Molecular phylogeny, classification, biogeography, and conservation. Zootaxa, 1737, 1–182.
Hedges, S.B., Hass, C.A., & Maxson, L.R. (1992) Caribbean biogeography: molecular evidence for dispersal in West Indian terrestrial vertebrates. Proceedings of the National Academy of Sciences (USA), 89, 1909–1913.
Heinicke, M.P., Duellman, W.E. & Hedges, S.B. (2007) Major Caribbean and Central American frog faunas originated by oceanic dispersal. Proceedings of the National Academy of Sciences (USA), 104, 10092–10097.
Hödl, W. (1990) Reproductive diversity in Amazonian lowland frogs. Fortschritte der Zoologie, 38, 41–60.
Huber, O., Gharbarran, G., & Funk, V. (1995) Vegetation map of Guyana. Center for the Study of Biological Diversity, University of Guyana, Georgetown, Guyana.
Huelsenbeck, J.P., and Ronquist, F. (2001) Mr. Bayes: Bayesian inference of phylogenetic tree. Bioinformatics Applications Note, 17, 754–755.
Iturralde-Vinent, M.A. & MacPhee, R.D.E. (1996) Age and paleogeographical origin of Dominican amber. Science, 273, 1850–1852.
Izecksohn, E., Jim, J., De Albuquerque, T.S., & De Mendonça, W.F. (1971) Observaçãos sôbre o desenvolvimento e os hábitos de Myersiella subnigra (Miranda-Ribeiro). Arquivos do Museu Nacional Rio de Janeiro, 54, 69–73.
Janečka, J.E., Miller, W., Pringle, T.H., Wiens, F., Zitzmann, A., Helgen, K.M., Springer, M.S., Murphy, W.J. (2007) Molecular and genomic data identify the closest living relative of primates. Science, 318, 792–794.
Li, Z.X. & Powell, C.M. (2001) An outline of the palaeogeographic evolution of the Australasian region since the beginning of the Neoproterozoic. Earth-Science Reviews, 53, 237–277.
Lutz, B. (1958) Anfíbios novos e raros das Serras Costeiras do Brasil. Memórias do Instituto Oswaldo Cruz, 56, 373–405.
Lynch, J.D. (1971) Evolutionary relationships, osteology, and zoogeography of leptodactyloid frogs. Miscellaneous Publications of the University of Kansas, Museum of Natural History, 53, 1–238.
Lynch, J.D. (1973) The transition from archaic to advanced frogs. In J.L. Vial (Ed.), Evolutionary biology of the anurans: contemporary research on major problems. University of Missouri Press, Columbia, pp. 133–182.
Lynch, J.D. (1979) A new genus for Elosia duidensis Rivero (Amphibia, Leptodactylidae) from southern Venezuela. American Museum Novitates, 2680, 1–8.
Lynch, J.D. (1986) The definition of the Middle American clade of Eleutherodactylus based in jaw musculature (Amphibia: Leptodactylidae). Herpetologica, 42, 248–258.
Lynch, J.D. & Duellman, W.E. (1997) Frogs of the genus Eleutherodactylus in western Ecuador. University of Kansas Special Publication, 23, 1–236.
Lynn, W.G. & Lutz, B. (1946) The development of Eleutherodactylus guentheri Stdnr. 1864. Boletim do Museu Nacional Rio de Janeiro, Nova Serie, Zoologia, 71, 1–46.
MacCulloch, R.D. & Lathrop, A. (2005) Hylid frogs from Mount Ayanganna, Guyana: new species, redescriptions, and distributional records. Phyllomedusa, 4, 17–37.
MacCulloch, R.D., Lathrop, A., & Khan, S.Z. (2006) Exceptional diversity of Stefania (Cryptobatrachidae) II: Six species from Mount Wokomung, Guyana. Phyllomedusa, 5, 31–41.
Mayr, E. & Phelps, Jr., W.H. (1967) The origin of the bird fauna of the south Venezuelan highlands. Bulletin of the American Museum of Natural History, 136, 269–328.
McDiarmid, R.W. & Donnelly, M.A. (2005) The herpetofauna of the Guayana Highlands: amphibians and reptiles of the Lost World. In: Donnelly, M.A., Crother, B.I., Guyer, C., Wake, M.H. & White, M.E. (Eds.) Ecology and evolution in the tropics; a herpetological perspective. University of Chicago Press, Chicago, pp. 461–560.
McDiarmid, R.W. & Gorzula, S. (1989) Aspects of the reproductive ecology and behavior of the tepui toads, genus Oreophrynella (Anura: Bufonidae). Copeia, 1989, 445–451.
Meegaskumbura, M., Bossuyt, F., Pethiyagoda, R., Manamendra-Arachchi, K., Bahir, M., Milinkovitch, M.C. & Schneider, C.J. (2002) Sri Lanka: An amphibian hot spot. Science, 298, 379–379.
Myers, C.W. & Donnelly, M.A. (1997) A tepui herpetofauna on a granitic mountain (Tamacuari) in the borderland between Venezuela and Brazil: report from the Phipps Tapirapecó Expedition. American Museum Novitates, 3213, 1–71.
Myers, C.W. & Donnelly, M.A. (2008) The summit herpetofauna of Auyantepui, Venezuela: report from the Robert G. Goelet American Museum-Terramar Expedition. Bulletin of the American Museum of Natural History, 308, 1–147.
Ovaska, K. & Rand, A.S. (2001) Courtship and reproductive behavior of the frog Eleutherodactylus diastema (Anura: Leptodactylidae) in Gamboa, Panama. Journal of Herpetology, 35, 44–50.
Pikacha, P., Morrison, C. & Richards, S. (2008) Frogs of the Solomon Islands. Institute of Applied Sciences, University of the South Pacific, Suva, Fiji, 68 pp.
Poinar, G.O. & Cannatella, D.C. (1987) An Upper Eocene frog from the Dominican Republic and its implication for Caribbean biogeography. Science, 237, 1215–1216.
Pombal, J.P., Jr., Sazima, I. & Haddad, C.F.B. (1994) Breeding behavior of the pumpkin toadlet, Brachycephalus ephippium (Brachycephalidae). Journal of Herpetology, 28, 516–519.
Posada, D. & Crandall, K.A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics, 14, 817–818.
Rambaut, A. & Drummond, A. (2005) Tracer version 1.3. (http://tree.bio.ed.ac.uk/software/tracer/). University of Oxford, Oxford
Roelants, K. & Bossuyt, F. (2005) Archaeobatrachian paraphyly and Pangaean diversification of crown-group frogs. Systematic Biology, 54, 111–26.
Roelants, K., Gower, D.J., Wilkinson, M., Loader, S.P., Biju, S.D., Guillaume, K., Moriau, L. & Bossuyt, F. (2007) Global patterns of diversification in the history of modern amphibians. Proceedings of the National Academy of Sciences of the United States of America, 104, 887–892.
Rokas, A., Carroll, S.B. (2006) Bushes in the tree of life. PLOS Biology, 4, e352.
Sanchiz, F.B. (1998) Vertebrates from the Early Miocene lignite deposits of the opencast mine Oberdorf (western Styrian Basin, Austria). 2. Amphibia. Annalen des Naturhistorischen Museums in Wien, 99, 13–29.
Sanmartin, I. & Ronquist, F. (2004) Southern Hemisphere biogeography inferred by event-based models: Plant versus animal patterns. Systematic Biology, 53, 216–243.
Schwartz, A. & Henderson, R.W. (1991) Amphibians and Reptiles of the West Indies: Descriptions, Distributions, and Natural History. University Press of Florida, Gainesville, 720 pp.
Señaris, J.D. & MacCulloch, R. (2005) Amphibians. In: Hollowell, T. & Reynolds, R (Eds.) Checklist of the terrestrial vertebrates of the Guiana Shield. Bulletin of the Biological Society of Washington, 13, 8–23.
Shubin, N. & Alberch, P. (1986) A morphogenetic approach on the origin and basic organization of the tetrapod limb. In: Hecht, M., Wallace, B. & Prance, G. (Eds.) Evolutionary Biology. Plenum Press, New York, USA, pp. 319–387.
Springer, M.S., Westerman, M., Kavanagh, J.R., Burk, A., Woodburne, M.O., Kao, D.J. & Krajewski, C. (1998) The origin of the Australasian marsupial fauna and the phylogenetic affinities of the enigmatic monito del monte and marsupial mole. Proceedings of the Royal Society of London Series B-Biological Sciences, 265, 2381–2386.
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.
Steyermark, J.A. (1986) Speciation and endemism in the flora of the Venezuelan tepuis. In: Vuilleumier, F. & Monasterío, M. (Eds.) High Altitude Tropical Biogeography, Oxford University Press, New York, USA, pp. 317–373.
Stocsits, R.R. (2009) RNAsalsa. Web resource available at: http://www.zfmk.de/web/Forschung/Abteilungen/AG_Wgele/Software/index.en.html. Museumsmeile Bonn, Bonn, Germany.
Tamura, K., Dudley, J., Nei, M., Kumar, S. (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596–1599.
Thibaudeau, G. & Altig, R. (1999) Endotrophic Anurans: Development and Evolution. In: McDiarmid, R.W. & Altig, R. (Eds.) Tadpoles: The Biology of Anuran Larvae. University of Chicago Press, Chicago, USA, pp. 170–188.
Thorne, J.L. & Kishino, H. (2002) Divergence time and evolutionary rate estimation with multilocus data. Systematic Biology, 51, 689–702.
Trueb, L. (1977) Osteology and anuran systematics: Intrapopulational variation in Hyla lanciformis. Sysytematic Zoology, 26, 165–184.
Trueb, L. (1993) Patterns of cranial diversity among the Lissamphibia. In: J. Hanken, J. & Hall, B.K. The skull. Volume 2. Patterns of structural and systematic diversity. University of Chicago Press, Chicago. pp. 255–343.
Valett, B.B. & Jameson, D.L. (1961) The embryology of Eleutherodactylus augusti latrans. Copeia, 1961, 103–109.
Wake, M.H. (1978) The reproductive biology of Eleutherodactylus jasperi (Amphibia, Anura, Leptodactylidae), with comments on the evolution of live-bearing systems. Journal of Herpetology, 12, 121–133.
Wassersug, R.J. & Duellman, W.E. (1984) Oral structures and their development in egg-brooding hylid frog embryos and larvae: evolutionary and ecological implications. Journal of Morphology, 182, 1–37.
Wells, K.D. (2007) The ecology and behavior of amphibians. University of Chicago Press, Chicago, 1148 pp.
Wiens, J.J., Fetzner, J.W., Parkinson, C.L. & Reeder, T.W. (2005) Hylid frog phylogeny and sampling strategies for speciose clades. Systematic Biology, 54, 719–748.
Wiens, J.J., Kuczynski, C.A., Duellman, W.E. & Reeder, T.W. (2007) Loss and re-evolution of complex life cycles in marsupial frogs: Does ancestral trait reconstruction mislead? Evolution, 61, 1886–1899.
Wiens, J.J., Kuczynski, C.A., Smith, S.A., Mulchay, D.G., Sites, J.W., Jr., Townsend, T.M. & Reeder, T.W. (2008) Branch lengths, support, and congruence: testing the phylogenomic approach with 20 nuclear loci in snakes. Systematic Biology, 57, 420–431.
Woodburne, M.O. & Case, J.A. (1996) Dispersal, vicariance, and the late Cretaceous to early Tertiary land mammal biogeography from South America to Australia. Journal of Mammalian Evolution, 3, 121–161.
Xia, X. & Xie, Z. (2001) DAMBE: Software package for data analysis in molecular biology and evolution. Journal of Heredity, 92, 371–373.
Yang, Z. & Yoder, A.D. (2003) Comparison of likelihood and Bayesian methods for estimating divergence times using multiple gene Loci and calibration points, with application to a radiation of cute-looking mouse lemur species. Systematic Biology, 52, 705–716.