Species diversity and biogeography of an ancient frog clade from the Guiana Shield (Anura: Microhylidae: Adelastes, Otophryne, Synapturanus) exhibiting spectacular phenotypic diversification

Author:

Fouquet Antoine1,Leblanc Killian1,Framit Marlene1,Réjaud Alexandre1,Rodrigues Miguel T2,Castroviejo-Fisher Santiago3,Peloso Pedro L V4ORCID,Prates Ivan5,Manzi Sophie1,Suescun Uxue1,Baroni Sabrina2,Moraes Leandro J C L6,Recoder Renato2ORCID,de Souza Sergio Marques2,Dal Vecchio Francisco2,Camacho Agustín2,Ghellere José Mario3,Rojas-Runjaic Fernando J M37,Gagliardi-Urrutia Giussepe38,de Carvalho Vinícius Tadeu9,Gordo Marcelo10,Menin Marcelo10,Kok Philippe J R11,Hrbek Tomas12,Werneck Fernanda P6,Crawford Andrew J13,Ron Santiago R14ORCID,Mueses-Cisneros Jonh Jairo15,Rojas Zamora Rommel Roberto10,Pavan Dante16,Ivo Simões Pedro17,Ernst Raffael18,Fabre Anne-Claire1920

Affiliation:

1. Laboratoire Evolution et Diversité Biologique, UMR 5174, CNRS, IRD, Université Paul Sabatier, Bâtiment 4R1 31062 cedex 9, 118 Route de Narbonne, Toulouse, France

2. Universidade de São Paulo Instituto de Biociências, Departamento de Zoologia, São Paulo, SP, Brazil

3. Pontifícia Universidade Católica do Rio Grande do Sul, Laboratório de Sistemática de Vertebrados/Programa de Pós-Graduação em Ecologia e Evolução da Biodiversidade, Escola de Ciências da Saúde e da Vida, Porto Alegre, RS, Brazil

4. Universidade Federal do Pará, Instituto de Ciências Biológicas, R. Augusto Corrêa, 1, Guamá, Belém, Pará, Brazil

5. Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, USA

6. Instituto Nacional de Pesquisas da Amazônia, Coordenação de Biodiversidade, Avenida André Araújo 2936, Manaus, AM, Brazil

7. Fundación La Salle de Ciencias Naturales, Museo de Historia Natural La Salle, Sección de Herpetología, Caracas, Venezuela

8. Peruvian Center for Biodiversity and Conservation (PCB&C), Iquitos, Peru

9. Programa de Pós-Graduação em Diversidade Biológica e Recursos Naturais, Universidade Regional do Cariri, Rua Cel. Antônio Luiz, 1161, 63.105-000, Crato CE, Brazil

10. Departamento de Biologia, Instituto de Ciências Biológicas, Universidade Federal do Amazonas, Manaus, AM, Brazil

11. Department of Ecology and Vertebrate Zoology, Faculty of Biology and Environmental Protection, University of Łódź, 12/16 Banacha Str., Łódź, Poland

12. Departamento de Genética, Instituto de Ciências Biológicas, Universidade Federal do Amazonas, Manaus, AM, Brazil

13. Department of Biological Sciences, Universidad de los Andes, Bogotá, Colombia

14. Museo de Zoología, Escuela de Biología, Pontificia Universidad Católica del Ecuador, Quito, Ecuador

15. Corporación para el Desarrollo Sostenible del Sur de la Amazonia-CORPOAMAZONIA, Mocoa, Putumayo, Colombia

16. Ecosfera Consultoria e Pesquisa em Meio Ambiente LTDA. Rodovia BR-259 s/n, Fazenda Bela Vista, Itapina, ES, Brazil

17. Departamento de Zoologia, Universidade Federal de Pernambuco, Av. Professor Moraes Rego, S/N, Cidade Universitária, 50760-420, Recife, PE, Brazil

18. Museum of Zoology, Senckenberg Natural History Collections Dresden, Dresden, Germany

19. The Natural History Museum, London, UK

20. Palaeontological Institute and Museum, University of Zurich, Zurich, Switzerland

Abstract

Abstract The outstanding biodiversity of the Guiana Shield has raised many questions about its origins and evolution. Frogs of the genera Adelastes, Otophryne and Synapturanus form an ancient lineage distributed mostly across this region. These genera display strikingly disparate morphologies and life-history traits. Notably, Synapturanus is conspicuously adapted to fossoriality and is the only genus within this group to have dispersed further into Amazonia. Moreover, morphological differences among Synapturanus species suggest different degrees of fossoriality that might be linked to their biogeographical history. Through integrative analysis of genetic, morphometric and acoustic data, we delimited 25 species in this clade, representing a fourfold increase. We found that the entire clade started to diversify ~55 Mya and Synapturanus ~30 Mya. Members of this genus probably dispersed three times out of the Guiana Shield both before and after the Pebas system, a wetland ecosystem occupying most of Western Amazonia during the Miocene. Using a three-dimensional osteological dataset, we characterized a high morphological disparity across the three genera. Within Synapturanus, we further characterized distinct phenotypes that emerged concomitantly with dispersals during the Miocene and possibly represent adaptations to different habitats, such as soils with different physical properties.

Funder

Agence Nationale de la Recherche

French Foundation for Research on Biodiversity

Brazilian Fundação de Amparo à Pesquisa do Estado do Amazonas

Conselho Nacional de Desenvolvimento Científico e Tecnológico

Fundação de Amparo à Pesquisa do Estado de São Paulo

Fonds voor Wetenschappelijk Onderzoek

Deutsche Forschungsgemeinschaft

Universidad de los Andes

Publisher

Oxford University Press (OUP)

Subject

Ecology, Evolution, Behavior and Systematics

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