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Phylogeny of Frogs from the Genus Physalaemus (Anura, Leptodactylidae) Inferred from Mitochondrial and Nuclear Gene Sequences Q ⇑ Luciana B

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Phylogeny of Frogs from the Genus Physalaemus (Anura, Leptodactylidae) Inferred from Mitochondrial and Nuclear Gene Sequences Q ⇑ Luciana B Molecular Phylogenetics and Evolution 92 (2015) 204–216 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Phylogeny of frogs from the genus Physalaemus (Anura, Leptodactylidae) inferred from mitochondrial and nuclear gene sequences q ⇑ Luciana B. Lourenço a, , Cíntia P. Targueta a, Diego Baldo b, Juliana Nascimento a, Paulo C.A. Garcia c, Gilda V. Andrade d, Célio F.B. Haddad e, Shirlei M. Recco-Pimentel a a Departamento de Biologia Estrutural e Funcional, Instituto de Biologia, Universidade Estadual de Campinas, 13083-863 Campinas, São Paulo, Brazil b Laboratorio de Genética Evolutiva, Instituto de Biología Subtropical (CONICET-UNaM), Facultad de Ciencias Exactas Químicas y Naturales, Universidad Nacional de Misiones, Félix de Azara 1552, CPA N3300LQF, Posadas, Misiones, Argentina c Laboratório de Herpetologia, Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, Pampulha, 31270-901 Belo Horizonte, Minas Gerais, Brazil d Departamento de Biologia, Centro de Ciências Biológicas e da Saúde, Universidade Federal do Maranhão-UFMA, 65080-040 São Luís, Maranhão, Brazil e Departamento de Zoologia, Instituto de Biociências, Universidade Estadual Paulista, C.P. 199, 13506-900 Rio Claro, São Paulo, Brazil article info abstract Article history: Although some species groups have been recognized in the leiuperine genus Physalaemus,no Received 8 December 2014 phylogenetic analysis has previously been performed. Here, we provide a phylogenetic study based on Revised 16 June 2015 mitochondrial and nuclear DNA sequences from 41 of the 46 species of Physalaemus. We employed the Accepted 17 June 2015 parsimony criterion using the software TNT and POY and the Bayesian criterion using the software Available online 2 July 2015 MrBayes. Two major clades were recovered inside the monophyletic Physalaemus: (i) the highly sup- ported Physalaemus signifer Clade, which included P. nattereri and the species previously placed in the Keywords: P. deimaticus and P. signifer Groups; and (ii) the Physalaemus cuvieri Clade, which included the remaining Phylogeny species of Physalaemus. Five species groups were recognized in the P. cuvieri Clade: the P. biligonigerus Systematics Anura Group, the P. cuvieri Group, the P. henselii Group, the P. gracilis Group and the P. olfersii Group. The Physalaemus P. gracilis Species Group was the same as that previously proposed by Nascimento et al. (2005). The P. henselii Group includes P. fernandezae and P. henselii, and was the sister group of a clade that comprised the remaining species of the P. cuvieri Clade. The P. olfersii Group included P. olfersii, P. soaresi, P. maximus, P. feioi and P. lateristriga. The P. biligonigerus Species Group was composed of P. biligonigerus, P. marmoratus, P. santafecinus and P. riograndensis. The P. cuvieri Group inferred here differed from that recognized by Nascimento et al. (2005) only by the inclusion of P. albifrons and the exclusion of P. cicada. The paraphyly of P. cuvieri with respect to P. ephippifer was inferred in all the analyses. Distinct genetic lineages were recognized among individuals currently identified as P. cuvieri and they were congruent with cytogenetic differences reported previously, supporting the hypothesis of occurrence of formally unnamed species. Ó 2015 Elsevier Inc. All rights reserved. 1. Introduction Pyron and Wiens (2011) recognized the leptodactylid subfamily Leiuperinae to comprise the genera Edalorhina, Engystomops, Physalaemus is one of the largest genera in Leptodactylidae, but Eupemphix [raised as a junior synonym of Physalaemus by its intergeneric and internal relationships remain unclear. Over the Faivovich et al. (2012)], Physalaemus, Pleurodema (including last decade, the taxonomy of leptodactylid anurans has changed as Somuncuria) and Pseudopaludicola. Fouquet et al. (2013),inan a result of a number of phylogenetic analyses (Frost et al., 2006; extensive analysis of Leptodactylidae, also recovered a mono- Grant et al., 2006; Pyron and Wiens, 2011; Faivovich et al., 2012; phyletic Leiuperinae, whereas Faivovich et al. (2012), in a study Fouquet et al., 2013; de Sá et al., 2014), and according to the latest designed to analyze the internal relationships in Pleurodema, did studies Physalaemus is included in the subfamily Leiuperinae. not recover Pseudopaludicola as belonging to the clade that includes all the remaining leiuperines. Although Pleurodema has been repeatedly recovered as the sister group of a clade composed q This paper was edited by the Associate Editor A. Larson. of Edalorhina, Engystomops and Physalaemus (Frost et al., 2006; ⇑ Corresponding author. E-mail address: [email protected] (L.B. Lourenço). Grant et al., 2006; Lourenço et al., 2008; Pyron and Wiens, 2011; http://dx.doi.org/10.1016/j.ympev.2015.06.011 1055-7903/Ó 2015 Elsevier Inc. All rights reserved. L.B. Lourenço et al. / Molecular Phylogenetics and Evolution 92 (2015) 204–216 205 Faivovich et al., 2012; Fouquet et al., 2013), it is not clear which is the P. biligonigerus Group and the P. signifer Group. Based on a phe- the sister group of Physalaemus. netic analysis of morphometric data, external morphology, color The internal phylogenetic relationships of Physalaemus are even patterns and osteological characters, Nascimento et al. (2005) less well studied than its intergeneric cladistic proximity. reviewed the proposal of Lynch (1970) and in addition to resurrect- Currently, 46 named species of Physalaemus are known (listed in ing the genera Engystomops and Eupemphix, rearranged the Frost, 2014), but even in the most comprehensive phylogenetic Physalaemus species into seven groups (P. albifrons, P. cuvieri, P. analyses of leiuperines conducted to date, only a few species of deimaticus, P. gracilis, P. henselii, P. olfersii and P. signifer Species Physalaemus were included [in addition to P. nattereri, Pyron and Group). However, the monophyly of each of these species groups Wiens (2011), Fouquet et al. (2013) and de Sá et al. (2014) analyzed has not been tested, and recent studies have noted the lack of eight species of Physalaemus, whereas Faivovich et al. (2012) ana- known synapomorphies for two of them, i.e., the P. henselii lyzed only five]. (Tomatis et al., 2009) and the P. albifrons (Vittorazzi et al., 2014) Tárano and Ryan (2002), in a study of the advertisement call of Groups. Physalaemus enesefae (currently a junior synonym of Physalaemus The need for phylogenetic analysis of Physalaemus is evident not fischeri), presented in the introduction of their paper a preliminary only from a taxonomic point of view but also because such analysis phylogenetic inference of Physalaemus relationships performed by will enable accurate evolutionary studies of several character sys- D. Cannatella, M. Holder, D. Hillis, A. S. Rand and M. J. Ryan. This tems, including chromosomal data. Cytogenetic data are available inference included ten species of Physalaemus in addition to ‘‘P. for 29 of the 46 species of Physalaemus (Beçak, 1968; Beçak et al., enesefae’’ and, according to Tárano and Ryan (2002), it was based 1970; Denaro, 1972; de Lucca et al., 1974; Silva et al., 1999, on morphological characters, allozymes and mitochondrial DNA 2000; Amaral et al., 2000; Lourenço et al., 2006; Ananias et al., sequences, but no further information about the phylogenetic 2007; Quinderé et al., 2009; Tomatis et al., 2009; Milani et al., methods used was provided. Tárano and Ryan (2002) noted two 2010; Nascimento et al., 2010; Provete et al., 2012; Vittorazzi monophyletic groups in that cladogram, one of them composed et al., 2014), and this set of data has already been explored by of the species currently assigned to Engystomops and the other Tomatis et al. (2009) and Vittorazzi et al. (2014) in an attempt to composed of the species of Physalaemus (Fig. 1), but the authors evaluate the arrangement of the P. henselii and P. albifrons did not discuss the internal relationships of those groups. Groups as proposed by Nascimento et al. (2005). Despite the noto- Despite the absence of a study specially designed to evaluate rious interspecific variation in the location of nucleolus organizer the phylogenetic relationships in Physalaemus, morphological regions (NORs) in Physalaemus, the steps of karyotypic evolution groups of species have been recognized. Lynch (1970), who consid- in this genus and the recognition of chromosomal synapomorphies ered Engystomops a synonym of Physalaemus, recognized four spe- for species groups remain largely unknown (see comments in cies groups in Physalaemus: the P. pustulosus Group (including Tomatis et al., 2009 and Vittorazzi et al., 2014). One critical limita- species currently in the genus Engystomops), the P. cuvieri Group, tion to the cytogenetic studies of Physalaemus has been the scarcity Fig. 1. Phylogenetic relationships of Physalaemus species presented by Tárano and Ryan (2002), based on unpublished analysis performed by D. Cannatella, M. Holder, D. Hillis, A.S. Rand and M.J. Ryan. 206 L.B. Lourenço et al. / Molecular Phylogenetics and Evolution 92 (2015) 204–216 of chromosomal markers, which prevents a reliable recognition of PCR amplification of a segment of the nuclear gene RAG-1, the pri- interspecific chromosome homeology, especially with regards to mers RAG-1F and RAG-1R (Faivovich et al., 2005) were used. The the smallest of the 22 chromosomes of the diploid complement PCR products were purified with
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