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A Molecular Phylogeny Recovers Strabomantis Aramunha Cassimiro, Verdade and Rodrigues, 2008 and Haddadus Binotatus (Spix, 1824) (Anura: Terrarana) As Sister Taxa

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A Molecular Phylogeny Recovers Strabomantis Aramunha Cassimiro, Verdade and Rodrigues, 2008 and Haddadus Binotatus (Spix, 1824) (Anura: Terrarana) As Sister Taxa Zootaxa 3741 (4): 569–582 ISSN 1175-5326 (print edition) www.mapress.com/zootaxa/ Article ZOOTAXA Copyright © 2013 Magnolia Press ISSN 1175-5334 (online edition) http://dx.doi.org/10.11646/zootaxa.3741.4.7 http://zoobank.org/urn:lsid:zoobank.org:pub:74D5A225-9727-48BE-B273-64E8D84FF19C A molecular phylogeny recovers Strabomantis aramunha Cassimiro, Verdade and Rodrigues, 2008 and Haddadus binotatus (Spix, 1824) (Anura: Terrarana) as sister taxa RENATA C. AMARO1,7, IVAN NUNES2, CLARISSA CANEDO2,, MARCELO F. NAPOLI3, FLORA A. JUNCÁ4, VANESSA K. VERDADE5, CÉLIO F.B. HADDAD6 & MIGUEL T. RODRIGUES1 1Universidade de São Paulo, Instituto de Biociências, Departamento de Zoologia, Caixa Postal 11.461, 05422-970 São Paulo, São Paulo, Brazil 2Universidade Federal do Rio de Janeiro, Museu Nacional, Departamento de Vertebrados, 20940-040 Rio de Janeiro, Rio de Janeiro, Brazil 3Universidade Federal da Bahia, Museu de Zoologia, Instituto de Biologia, Departamento de Zoologia, 40170-115, Salvador, Bahia, Brazil 4Universidade Estadual de Feira de Santana, Departamento de Ciências Biológicas, 44036-900 Feira de Santana, Bahia, Brazil 5Universidade Federal do ABC, Centro de Ciências Naturais e Humanas, Avenida dos Estados, n5001, 09210-971 Santo André, São Paulo, Brazil 6Universidade Estadual Paulista ‘‘Júlio de Mesquita Filho’’, Instituto de Biociências, Departamento de Zoologia, 13506-900 Rio Claro, São Paulo, Brazil 7Corresponding author. E-mail: [email protected] Abstract The taxonomic and biogeographic affinities of Strabomantis aramunha from the Campos Rupestres of Brazil are intrigu- ing. A unique skull morphology of females suggest affinities with the broad-headed eleutherodactylines of Northwestern South America in the genus Strabomantis. Male and juvenile morphology nonetheless suggest S. aramunha could be re- lated to members of the recently described genus Haddadus from eastern Brazil. We assess the affinities of S. aramunha using molecular phylogenetic analyses of mitochondrial (12S, tRNAval, 16S, cyt b) and nuclear sequences (RAG-1and rhodopsin). Bayesian inference, likelihood, and parsimony analysis recover a highly supported clade with S. aramunha and H. binotatus as sister taxa. Accordingly, we transfer S. aramunha to Haddadus, and provide a new generic definition of the later. The distribution of species in Haddadus (highlands of the Espinhaço mountain Range and coastal eastern Bra- zil) is now concordant with the general pattern observed for other species in the area. Key words: Haddadus aramunha, molecular data, new combination, nomenclature, phylogeny Introduction Molecular phylogenetic studies have resulted in several taxonomic changes at the family and generic levels within Terrarana (an unranked name for direct developing frogs created by Hedges et al. 2008) during the last ten years (see Darst & Cannatella 2004; Crawford & Smith 2005; Frost et al. 2006; Heinicke et al. 2007, 2009; Hedges et al. 2008; Padial et al. 2009; Canedo & Haddad 2012). In this context, frogs formerly placed in the highly speciose paraphyletic genus Eleutherodactylus were partitioned in several other genera (e.g., Frost et al. 2006; Hedges et al. 2008; Padial et al. 2009). The recent results presented by Canedo & Haddad (2012) indicated the non-monophyly of yet some other genera in the current taxonomy (e.g. Ischnocnema sensu Hedges et al. 2008). Despite progress in our understanding of the phylogenetic relationships of Terraranas and the consequent improvement in their taxonomy, several relationships inferred by Frost et al. (2006), Hedges et al. (2008), Padial et al. (2009), Pyron & Wiens (2011), and Canedo & Haddad (2012) are poorly supported, many species have not yet been sampled, and other lack substantial amounts of evidence. These limitations suggest that additional work is still much needed. Accepted by J. Padial: 29 Oct. 2013; published: 29 Nov. 2013 569 The naming and description of the terraranan frog Strabomantis aramunha by Cassimiro et al. (2008) is contemporary with Hedges et al. (2008). The species was described on the basis of four adults and three juvenile specimens from Serra do Sincorá (13°04'07"S, 41°20'09"W, 998 m a.s.l.), northern Espinhaço mountain range, Mucugê Municipality, Bahia State, Brazil. This species occurs in the highly endemic rock meadows environment referred to as “Campos Rupestres” (for the description of Brazilian Campos Rupestres, see Heyer 1999). The disjunctive distribution of S. aramunha with respect to the remaining western and northwestern South American species of Strabomantis was considered enigmatic (Cassimiro et al. 2008). Nonetheless, its generic allocation was justified by the observation of a combination of characters of females of S. aramunha that, following Lynch (1997), would ally this species with members of the former Eleutherodactylus sulcatus species group (now Strabomantis biporcatus species series; Hedges et al. 2008): large size, broad head, posterior pars fascialis of maxillae deepened, V3 ramus of trigeminus nerve superficial to the m. levator posterior mandibulae subexternus (“S” condition of Lynch 1986). Alternatively, according to Cassimiro et al. (2008), males of S. aramunha are also similar to Haddadus binotatus Spix. Placing S. aramunha within the genus Haddadus, however, would require a new generic definition of the later to correct that of Hedges et al. (2008). Since the morphological evidence can be considered ambiguous, herein we provide novel evidence based on molecular analysis of mitochondrial and nuclear sequences for Strabomantis, Haddadus, and other Neobatrachia (mainly Terrarana), in order to clarify the position of S. aramunha. Material and methods Molecular study design. The phylogenetic analyses relied on two different datasets, one gene-rich dataset including mitochondrial and nuclear DNA for 51 taxa, and species-rich dataset including only mitochondrial DNA for 322 taxa. The gene-rich dataset includes 2,082 bp (508 bp of 12S, 591 bp of 16S, 223 bp of cyt b, 442 bp of RAG-1 and 318 bp of Rhodopsin) and 51 terminals. This dataset includes sequences of four paratypes of Strabomantis aramunha and representatives of diverse Neobatrachia families and major groups of Terrarana sampled by Heinicke et al. (2009). The species-rich dataset includes 1,602 bp of aligned DNA sequences from mitochondrial genes (890 bp of 12S, 85 bp of tRNAVal, 627 bp of 16S) for 322 terminals (Appendix 1 and 2). The ingroup comprised 312 terminals, including sequences for two specimens of Strabomantis aramunha, for seven other species of Strabomantis, eight specimens of Haddadus binotatus, and 295 other terminals within Terrarana. Outgroup selection followed Frost et al. (2006), and includes ten terminals from seven anuran genera: six hyloids, Agalychnis callidryas (Cope), Epipedobates boulengeri (Barbour), E. tricolor (Boulenger), Flectonotus fitzgeraldi (Parker), Flectonotus sp., Litoria caerulea (White), Rhinella arenarum (Hensel), R. margaritifera (Laurenti), Uperoleia laevigata Keferstein), and the ranoid Lithobates catesbeianus (Shaw); the last one was used to root the tree. The second species of the genus Haddadus, H. plicifer (Boulenger), is a poorly characterized species for which we could not access tissue samples for molecular analyses. Molecular data gathering. We extracted genomic DNA from ethanol-preserved tissues following protocol from Feztner (1990). The Polymerase Chain Reaction (PCR) were directly purified with Exonuclease I and Shrimp Alkaline Phosphatase (USB or Fermentas). Automated sequencing was carried out using BigDye Terminator v3.1 Cycle Sequencing kit (Applied Biosystems), followed by analysis on ABI Prism 310, 3700 or 3170 Genetic Analyzer Sequencers (Applied Biosystems) according to the manufacturer’s instructions. In the second aproach, we extracted genomic DNA from ethanol-preserved tissues using the DNeasy tissue extraction kit (Qiagen Inc.). We performed Polymerase Chain Reaction (PCR) for the amplification of the selected fragments using PCR Master Mix (2X) Fermentas (0.05 u/µl Taq DNA Polymerase, reaction buffer, 4 mM MgCl2, 0.4 mM of each dNTP) and specific primers (Table 1). Standard reaction conditions were an initial hold for 2 min at 94ºC; 35 cycles of 94ºC for 30s, 50ºC for 30s, and 72ºC for 2 min, followed by a final hold of 72ºC for 7 min, and terminating the reaction at 4ºC. PCR products were visualized in 1% agarose gels. Part of purification and sequencing were done by Macrogen Inc. (sequencing conducted under BigDyeTM terminator cycling conditions; reacted products purified using ethanol precipitation and runs performed in Automatic Sequencer 3730XL). Chromatograms were fully inspected, embedded primer sequences were deleted, and forward and reverse strands were compared before assembling consensus sequences with CodonCode Aligner 3.5 (Codon Code Corporation). GenBank accession numbers for sequences generated in this study are available on Appendix 1 and 2, as well those data downloaded 570 · Zootaxa 3741 (4) © 2013 Magnolia Press AMARO ET AL. from GenBank. In some cases we joined sequences from different individuals of the same species to construct a single composite terminal (applied only to GenBank sequences from non-Strabomantis or non-Haddadus terminals). Sequences were aligned in MEGA 5.0 (Molecular Evolutionary Genetics Analysis; Tamura et al., 2011) using Muscle (Multiple Sequence Comparison by Log-Expectation; Edgar 2004a; Edgar 2004b), and were subsequently adjusted by hand for some of the highly variable regions of the 12S and 16S
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