The Phylogenetic Relationships of the Charismatic Poster Frogs, Phyllomedusinae (Anura, Hylidae)

Cladistics Cladistics 26 (2010) 227–261 10.1111/j.1096-0031.2009.00287.x The phylogenetic relationships of the charismatic poster frogs, Phyllomedusinae (Anura, Hylidae) Julia´ n Faivovicha,*, Ce´ lio F. B. Haddadb,De´ lio Baeˆ tac, Karl-Heinz Jungferd, Guilherme F. R. A´ lvarese, Reuber A. Branda˜ oe, Christopher Sheilf, Lucas S. Barrientosg,Ce´ sar L. Barrio-Amoro´ sh, Carlos A. G. Cruzc and Ward C. Wheeleri aDivisioń Herpetologıá, Museo Argentino de Ciencias Naturales-CONICET, Angel Gallardo 470, C1405DJR, Buenos Aires, Argentina; Departamento de Zoologia, I.B., Universidade Estadual Paulista, Rio Claro, CEP 13506-900, Saõ Paulo, Brazil; and Herpetology, Division of Vertebrate Zoology, American Museum of Natural History, New York, USA; bDepartamento de Zoologia, I.B., Universidade Estadual Paulista, Rio Claro, CEP 13506-900, Saõ Paulo, Brazil; cSetor de Herpetologia, Departamento de Vertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, s ⁄ n°,Saõ Cristo´vaõ, CEP 20940-040, Rio de Janeiro, RJ, Brazil; dPanoramastr. 14, 74405 Gaildorf, Germany; eLaborato´rio de Fauna e Unidades de Conservaçaõ, Departamento de Engenharia Florestal, Universidade de Brası´lia, Brası´lia-DF, CEP 70910-900, Brazil; fDepartment of Biology, Dolan Center for Science & Technology, John Carroll University, 20700 North Park Boulevard, University Heights, OH 44118, USA; gInstituto de Ciencias Naturales, Universidad Nacional de Colombia, calle 53, 2° edificio Bogota´, Colombia; hFundacioń Andı´genA, Apartado Postal 210, 5101-A Me´rida, Venezuela; iDivision of Invertebrate Zoology, American Museum of Natural History, Central Park West at 79th St, New York, NY 10024, USA Accepted 8 August 2009 Abstract The leaf or monkey frogs of the hylid subfamily Phyllomedusinae are a unique group of charismatic anurans. We present a molecular phylogenetic analysis that includes 45 of the 60 species of phyllomedusines using up to 12 genes and intervening tRNAs. The aims were to gain a better understanding of the phylogenetic position of Phrynomedusa, test the monophyly and explore the relationships among several putative lineages (Hylomantis, the H. buckleyi Group, Phasmahyla, the four species groups of Phyllomedusa, and the species of Phyllomedusa that remain unassigned to any group), and to examine the implications of our phylogeny for the evolution of several characters in phyllomedusines. The analyses resulted in a well-supported phylogenetic hypothesis that provides a historical framework for a discussion of the evolution of characters associated with reproductive biology, gliding behaviour, the physiology of waterproofing, and bioactive peptides. Implications include an earlier origin for eggless capsules than for leaf-folding behaviour during amplexus, two independent origins of gliding, and an earlier origin of reduction in evaporative water loss than uricotelism, which is a result that originally was predicted on the basis of physiology alone. Furthermore, our results support the prediction that bioactive peptides from different peptide families are to be expected in all species of Phyllomedusinae. Hylomantis (as recently redefined) is shown to be paraphyletic and the synonymy of Agalychnis is revised to remedy this problem by including both Hylomantis and Pachymedusa. Ó The Willi Hennig Society 2009. Commonly known as leaf frogs, monkey frogs, and these frogs. However, the bioprospecting storm over red-eyed tree frogs, phyllomedusines are possibly the these beautiful frogs had not until recently been most charismatic treefrogs with which the general public accompanied by an equivalent increase in our knowl- is familiar. In addition, several species of this subfamily edge of their phylogenetic relationships. have become popular in biochemical research over the The first comprehensive hypothesis of relationships past three decades due to the diversity of bioactive of Phyllomedusinae was that of Funkhouser (1957), peptides that are stored in granular glands in the skin of who presented a precladistic narrative ‘‘phylogenetic arrangement’’ that included most species known at that *Corresponding author: time, and it was based mostly on perceived degrees of E-mail address: [email protected] specialization of the foot (here reproduced as Fig. 1), a Ó The Willi Hennig Society 2009 228 J. Faivovich et al. / Cladistics 26 (2010) 227–261 condensed version of which was also presented by Lutz which Faivovich et al. (2005) had no exemplars (1968). A more recent hypothesis of the phylogenetic (Fig. 2d). However, for these two species Wiens et al. relationships of Phyllomedusinae (Faivovich et al., (2005, 2006) and Moen and Wiens (2008) were only able 2005) was presented in the broader context of relation- to include about 830 bp of the12S mitochondrial gene, ships within Hylidae. This study was based on the in comparison with the up to 8000 bp from several loci analysis of partial or complete sequences of four available for some species in their analyses. Considering mitochondrial and five nuclear genes for up to 5100 bp the weakly supported results they obtained, the position per species, and a dataset built from BurtonÕs (2004) of Phrynomedusa can still be considered to be poorly collection of observations on hylid foot musculature (the established. relevant section of their hypothesis is here reproduced as The results of these phylogenetic analyses are difficult Fig. 2a). Furthermore, Faivovich et al. (2005) reviewed to compare because they resulted from different analy- the available morphological evidence for the monophyly tical methods and character weighting, particularly with of Phyllomedusinae. Wiens et al. (2005) presented a regard to how nucleotide homologies and inser- separate phylogenetic analysis of hylids (the relevant tion ⁄deletion events were considered during tree section of their hypothesis is here reproduced as Fig. 2b) searches. Even though these analyses imply different using fewer exemplars that included data from mor- relationships, they agree in several aspects. phology for two phyllomedusines and several gene 1. Polyphyly of Agalychnis. The former Agalychnis fragments (3367 bp from five gene fragments for four calcarifer (and presumably also A. craspedopus) was exemplars of Phyllomedusinae and 830 bp for ten other inferred to be the sister taxon of all remaining Phyllo- exemplars from the 12S ribosomal mitochondrial gene). medusinae, and a new generic name (Cruziohyla) was Later, Wiens et al. (2006) combined most sequences introduced (Faivovich et al., 2005). However, the lack of generated by Faivovich et al. (2005) with those of Wiens any exemplar of Phrynomedusa in the analysis of et al. (2005) and presented a new phylogenetic hypoth- Faivovich et al. (2005), with which both C. calcarifer esis as supplementary data without substantial discus- and C. craspedopus share two character states of uncer- sion (the relevant section of their hypothesis is tain polarity (oral disc with complete marginal papila- reproduced as Fig. 2c). Moen and Wiens (2008) pre- tion, and bicoloured iris), left uncertainty in the analysis sented a reanalysis of the Phyllomedusinae available to as to whether Cruziohyla is the sister taxon of all Wiens et al. (2006) using Bayesian methods—the results Phyllomedusinae, or if it is actually the sister taxon to of this latter study were presented as supplementary Phrynomedusa. A solution to this question could not be data and without discussion (here reproduced as hypothesized based on the taxonomic distribution of Fig. 2d). More recently, Gomez-Mestre et al. (2008) known morphological character states because Phyllo- presented a phylogenetic hypothesis for the genus medusinae is the sister taxon of the large Australo- Agalychnis on the basis of several mitochondrial and papuan subfamily Pelodryadinae (Faivovich et al., 2005; nuclear genes (here reproduced as Fig. 2e). Wiens et al., 2005, 2006). The internal relationships of Taxon sampling of Phyllomedusinae included by Pelodryadinae remain to be studied and both character Faivovich et al. (2005) comprised at least one exemplar states that would support a sister-group relationship of of all but a single recognized genus within the subfamily Cruziohyla and Phrynomedusa do occur in some species of and three of the four species groups of Phyllomedusa. Pelodryadinae; therefore, the polarity of these character Overall this sampling was adequate to test the mono- states could not be deduced at that time. In the results of phyly of the subfamily and to gain a general perspective Wiens et al. (2006), Phrynomedusa was obtained as the on the internal topology of the group. However, from sister taxon of all Phyllomedusinae, whereas Cruziohyla the inception of that study, it was evident that the taxon was recovered asthe sister group ofPhasmahyla, with both sampling was insufficient to address certain phylogenetic nodes having less than 50% bootstrap support. problems within the subfamily. These problems ranged 2. Polyphyly of Phyllomedusa. Duellman (1968, 1969), from the position of Phrynomedusa (no exemplars of this Cannatella (1980), and Jungfer and Weygoldt (1994) genus were available), to the monophyly of Hylomantis have suggested the polyphyly of Phyllomedusa and, (only a single exemplar was available), to the individual corroborating this, the single available exemplar of the monophyly of each of the species groups of Phyllome- former P. buckleyi Group (P. lemur) was found to be dusa (only one exemplar was available for each of the only distantly

Load more