Title
Evolution in the Genus Rhinella: A Total Evidence Phylogenetic Analysis of Neotropical True Toads (Anura: Bufonidae)
Date Issued
31 March 2021
Access level
open access
Resource Type
journal article
Author(s)
Pereyra M.O.
Blotto B.L.
Baldo D.
Ron S.R.
Elias-Costa A.J.
Iglesias P.P.
Maria M.T.
Ospina-Sarria J.J.
Maciel N.M.
Rada M.
Kolenc F.
Borteiro C.
Rivera-Correa M.
Rojas-Runjaic F.J.M.
Moravec J.
De La Riva I.
Wheeler W.C.
Castroviejo-Fisher S.
Grant T.
Haddad C.F.B.
Faivovich J.
Publisher(s)
American Museum of Natural History Library
Abstract
True toads of the genus Rhinella are among the most common and diverse group of Neotropical anurans. These toads are widely distributed throughout South America, inhabiting a great diversity of environments and ecoregions. Currently, however, the genus is defined solely on the basis of molecular characters, and it lacks a proper diagnosis. Although some phenetic species groups have traditionally been recognized within Rhinella, the monophyly of some of them have been rejected in previous phylogenetic analyses, and many species remain unassigned to these poorly defined groups. Additionally, the identity and taxonomy of several species are problematic and hinder the specific recognition and description of undescribed taxa. In this work, we first perform phylogenetic analyses of separate mitochondrial and nuclear datasets to test the possible occurrence of hybridization and/or genetic introgression in the genus. The comparative analysis of both datasets revealed unidirectional mitochondrial introgressions of an unknown parental species into R. horribilis ("ghost introgression") and of R. dorbignyi into R. bernardoi; therefore, the mitochondrial and nuclear datasets of these species were considered separately in subsequent analyses. We performed total-evidence phylogenetic analyses that included revised molecular (four mitochondrial and five nuclear genes) and phenotypic (90 characters) datasets for 83 nominal species of Rhinella, plus several undescribed and problematic species and multiple outgroups. Results demonstrate that Rhinella was nonmonophyletic due to the position of R. ceratophrys, which was recovered as the sister taxon of Rhaebo nasicus with strong support. Among our outgroups, the strongly supported Anaxyrus + Incilius is the sister clade of all other species of Rhinella. Once R. ceratophrys is excluded, the genus Rhinella is monophyletic, well supported, and composed of two major clades. One of these is moderately supported and includes species of the former R. spinulosa Group (including R. gallardoi); the monophyletic R. granulosa, R. crucifer, and R. marina Groups; and a clade composed of the mitochondrial sequences of R. horribilis. The other major clade is strongly supported and composed of all the species from the non-monophyletic R. veraguensis and R. margaritifera Groups, the former R. acrolopha Group, and R. sternosignata. Consistent with these results, we define eight species groups of Rhinella that are mostly diagnosed by phenotypic synapomorphies in addition to a combination of morphological character states. Rhinella sternosignata is the only species that remains unassigned to any group. We also synonymize nine species, treat three former subspecies as full species, and suggest that 15 lineages represent putative undescribed species. Lastly, we discuss the apparently frequent occurrence of hybridization, deep mitochondrial divergence, and "ghost introgression"; the incomplete phenotypic evidence (including putative character systems that could be used for future phylogenetic analyses); and the validity of the known fossil record of Rhinella as a source of calibration points for divergence dating analyses.
Start page
1
End page
156
Volume
447
Issue
1
Language
English
OCDE Knowledge area
Zoología, Ornitología, Entomología, ciencias biológicas del comportamiento
Scopus EID
2-s2.0-85103597581
Source
Bulletin of the American Museum of Natural History
ISSN of the container
00030090
Sponsor(s)
We sincerely thank José M. Padial (Bronx Community College, New York); Thelia M. Céspedes Alejabo (CINBIOTYC, Peru); Guarino Colli and Helga Wiederhecker (Coleção Herpetológica da Universidade de Brasília, Brazil); Jimena Grosso (Fundación Miguel Lillo, Argentina); Juan M. Daza (Grupo Herpetológico de Antioquia, Colombia); Diego A. Barrasso and Leonardo Cotichelli (Insti-tuto de Diversidad y Evolución Austral, Centro Nacional Patagónico, Argentina); Albertina P. Lima (Instituto Nacional de Pesquisas da Amazônia, Brazil); Antoine Fouquet (Laboratoire Evolution & Diversité Biologique, Université Toulouse, France); Juan M. Boeris, Andrés E. Brunetti, Dario E. Car-dozo, and Juan M. Ferro (Laboratorio de Genética Evolutiva, Instituto de Biología Subtropical, Argentina); Sebastián Barrionuevo, Nadia G. Cervino, Laura Nicoli, and Santiago J. Nenda (Museo Argentino de Ciencias Naturales, Argentina); César Agui-lar (Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Lima, Perú); Bea-triz Álvarez Dorda and Isabel Rey Fraile (Museo Nacional de Ciencias Naturales, Spain); personnel of the herpetological collection of Museo de Biodi-versidad (MUBI, Perú); Andrés Pansonato and Tiago Pezzuti (Universidade Federal de Minas Gerais, Brazil); Francisco Brusquetti, Ariadne Fares Sabbag, and Mariana Lyra (Universidad Estadual Paulista, Brazil); and Pedro H. Dias, Juliana Jordão, Julia S. Parreiras, Paulo D.P. Pinheiro, and Miguel Rodrigues (Universidade de São Paulo, Brazil) for sharing with us specimens, tissue samples and/or DNA sequences. For access to collections and specimen loans we thank Ariane Silva and Fernanda Werneck (Instituto Nacional de Pesquisas da Ama-zonia, Brazil); Rafe Brown, Richard Glor, Linda Trueb, and Luke Welton (Kansas University, Lawrence); Marta Calvo (Museo Nacional de Ciencias Naturales, Spain); Aline Staskowian Benetti (Museu de Zoologia da Universidade de São Paulo, Brazil); Carol Spencer and Natasha Stepanova (Museum of Vertebrate Zoology, Berkeley, California); and Eric Smith (University of Texas at Arlington). Pedro H. Dias; Ana Duport Bru, M. Laura Ponssa, and M. Florencia Vera Candioti (Fundación Miguel Lillo, Argentina); and Marinus S. Hoogmoed (Museu Paraense Emilio Goeldi, Brazil), contributed with valuable information on taxonomy or morphology of several specimens. Michael Jowers (Porto University) helped us to clarify the identity of some sequences of R. beebei and R. humboldti. M. Jimena Gómez Fernández, M. Daniela Pereyra, and Araceli Seiffe (Museo Argentino de Ciencias Naturales, Argentina) provided technical laboratory assistance. Several colleagues kindly shared with us photographs and/or data of species of Rhinella: César L. Barrio-Amorós (R. sternosignata), Michelle Castellanos (R. sclerocephala), Andrés Cecconi (R. diptycha), Pedro H. Dias (R . acutirostris), José Gerardo Espinoza (Rhinella sp. 14), Peter Janzen (R. crucifer), Konstantin D. Milto (type material of R . margaritifera), Arturo Muñoz (R . quechua), Roberto L.M. Novaes (R. icterica), Mirco Solé (R. hoogmoedi), Mauro Texeira Jr. (R. ornata), Rodrigo Tinoco (R . ocellata), Vicente Valdés Guzman (R . atacamensis), and Mario Yañez-Muñoz (R. cf. roqueana). David Blackburn, contributors, and the staff of Morphosource (Duke Library Digital Repository) very kindly made available μCT images of relevant species. TNT was provided free by the Willi Hennig Society. We thank Consejo Nacional de Investigaciones Científicas y Técnicas (CONI-CET), ANPCyT, Fundação de Amparo à Pesquisa do Estado de São Paulo for financial support: PIP 11220110100889; PICT 2013-0404, 2015-0813, 2015-0820, 2015-2381, 2017-2437, and 2018-3349; and grants #2012/10000-5, #2013/20423-3, #2013/50741-7, #2014/03585-2, #2015/11237-7, #2016/25070-0, and #2018/15425-0 from São Paulo Research Foundation (FAPESP). M.R. was supported by a PNPD post-doctoral fellowship from the Brazilian Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES grant 2016.1.263.41.6). J.M. thanks Ministry of Culture of the Czech Republic (grant DKRVO 2021/6.VI.c National Museum Prague, 00023272). S.C.F. was supported by CNPq (grant 312744/ 2017-0) and the PrInt program of Coordenação de Aperfeiçoa-mento de Pessoal de Nivel Superior, CAPES, Brazil (grant 88887.508359/2020-00). T.G. was supported by research fellowships from the Brazilian Con-selho Nacional de Desenvolvimento Científico e Tecnológico (CNPq grant 306823/2017-9). C.F.B.H. thanks CNPq for a research fellowship (grant 306623/2018-8). The Centro de Estudos de Insetos Sociais, I.B., UNESP, Rio Claro allowed access to its molecular laboratory facilities for the production of some sequences used in this study. Field and laboratory work in Ecuador were funded by Secretaría Nacional de Educación Superior, Ciencia, Tec-nología e Innovación del Ecuador SENESCYT (Arca de Noé initiative; S.R.R. and Omar Torres principal investigators) and grants from Pontificia Universidad Católica del Ecuador, Dirección General Académica. B.L.B. acknowledges Esteban O. Lavilla for his support during initial studies on the R. spinulosa Group. We greatly appreciate the critical reviews of the manuscript by Aaron Bauer and Joseph Mendelson.
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