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      The poverty of adult morphology: Bioacoustics, genetics, and internal tadpole morphology reveal a new species of glassfrog (Anura: Centrolenidae: Ikakogi) from the Sierra Nevada de Santa Marta, Colombia

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          Abstract

          Ikakogi is a behaviorally and morphologically intriguing genus of glassfrog. Using tadpole morphology, vocalizations, and DNA, a new species is described from the Sierra Nevada de Santa Marta (SNSM), an isolated mountain range in northern Colombia. The new taxon is the second known species of the genus Ikakogi and is morphologically identical to I. tayrona (except for some larval characters) but differs by its genetic distance (14.8% in mitochondrial encoded cytochrome b MT-CYB; ca. 371 bp) and by the dominant frequency of its advertisement call (2928–3273 Hz in contrast to 2650–2870 Hz in I. tayrona). They also differ in the number of lateral buccal floor papillae, and the position of the buccal roof arena papillae. Additionally, the new species is differentiated from all other species of Centrolenidae by the following traits: tympanum visible, vomerine teeth absent, humeral spines present in adult males, bones in life white with pale green in epiphyses, minute punctuations present on green skin dorsum, and flanks with lateral row of small, enameled dots that extend from below eye to just posterior to arm insertion. We describe the external and internal larval morphology of the new species and we redescribe the larval morphology of Ikakogi tayrona on the basis of field collected specimens representing several stages of development from early to late metamorphosis. We discuss the relevance of larval morphology for the taxonomy and systematics of Ikakogi and other centrolenid genera. Finally, we document intraspecific larval variation in meristic characters and ontogenetic changes in eye size, coloration, and labial tooth-rows formulas, and compare tadpoles of related species. Ikakogi tayrona has been proposed as the sister taxon of all other Centrolenidae; our observations and new species description offers insights about the ancestral character-states of adults, egg clutches, and larval features in this lineage of frogs.

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          The Ecology and Behavior of Amphibians

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            A simplified table for staging anuran embryos and larvae with notes on identification

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              Phylogenetic analyses reveal unexpected patterns in the evolution of reproductive modes in frogs.

              Understanding phenotypic diversity requires not only identification of selective factors that favor origins of derived states, but also factors that favor retention of primitive states. Anurans (frogs and toads) exhibit a remarkable diversity of reproductive modes that is unique among terrestrial vertebrates. Here, we analyze the evolution of these modes, using comparative methods on a phylogeny and matched life-history database of 720 species, including most families and modes. As expected, modes with terrestrial eggs and aquatic larvae often precede direct development (terrestrial egg, no tadpole stage), but surprisingly, direct development evolves directly from aquatic breeding nearly as often. Modes with primitive exotrophic larvae (feeding outside the egg) frequently give rise to direct developers, whereas those with nonfeeding larvae (endotrophic) do not. Similarly, modes with eggs and larvae placed in locations protected from aquatic predators evolve frequently but rarely give rise to direct developers. Thus, frogs frequently bypass many seemingly intermediate stages in the evolution of direct development. We also find significant associations between terrestrial reproduction and reduced clutch size, larger egg size, reduced adult size, parental care, and occurrence in wetter and warmer regions. These associations may help explain the widespread retention of aquatic eggs and larvae, and the overall diversity of anuran reproductive modes. © 2012 The Author(s). Evolution© 2012 The Society for the Study of Evolution.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: Project administrationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Formal analysisRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: Writing – original draftRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: Visualization
                Role: ConceptualizationRole: InvestigationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                8 May 2019
                2019
                : 14
                : 5
                : e0215349
                Affiliations
                [1 ] Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil
                [2 ] Grupo de Investigación en Biodiversidad y Ecología Aplicada (GIBEA), Facultad de Ciencias Básicas, Universidad del Magdalena, Santa Marta, Colombia
                [3 ] Grupo Herpetológico Universidad del Magdalena, Santa Marta, Colombia
                [4 ] Grupo Biomics, Departmento de Ciencias Biológicas, Universidad de los Andes, Bogotá, Colombia
                [5 ] Grupo de Morfología y Ecología Evolutiva, Universidad Nacional de Colombia, Sede Bogotá, Colombia
                [6 ] Grupo de investigación en Evolución, Ecología y Conservación EECO, Programa de Biología, Facultad de Ciencias Básicas y Tecnologías, Universidad del Quindío, Armenia, Colombia
                Universitat Trier, GERMANY
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-9359-6461
                Article
                PONE-D-18-31601
                10.1371/journal.pone.0215349
                6506205
                31067224
                08bd60f3-873f-4133-ae55-889cf4ae3674
                © 2019 Rada et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 1 November 2018
                : 29 March 2019
                Page count
                Figures: 24, Tables: 7, Pages: 46
                Funding
                Funded by: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (BR)
                Award ID: 001
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100002322, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior;
                Award ID: PEC-PG
                Award Recipient :
                Funded by: Fundación Centro de Estudios Interdiciplinarios Básicos y Aplicados
                Award ID: CEIBA 2016
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001807, Fundação de Amparo à Pesquisa do Estado de São Paulo;
                Award ID: 2008/50928-1, 2012/10000-5 and 2013/20420–4
                Award Recipient :
                Scholarship grant support was provided by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES financeiro code 001, PEC-PG) and PNPD programs (Proc. 2016.1.263.41.6) to MR and the Fundación Centro de Estudios Interdiciplinarios Básicos y Aplicados (CEIBA 2016) to MA-C. Fieldwork and others facilities was supported by a grant of Fundação de Amparo à Pesquisa do Estado de São Paulo, FAPESP (Proc. Proc. 2008/50928-1, 2012/10000-5 and 2013/20420–4). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Tadpoles
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Larvae
                Biology and Life Sciences
                Anatomy
                Biological Tissue
                Connective Tissue
                Cartilage
                Medicine and Health Sciences
                Anatomy
                Biological Tissue
                Connective Tissue
                Cartilage
                Biology and Life Sciences
                Physiology
                Reproductive Physiology
                Oviposition
                Clutches
                Medicine and Health Sciences
                Physiology
                Reproductive Physiology
                Oviposition
                Clutches
                Biology and Life Sciences
                Anatomy
                Digestive System
                Teeth
                Medicine and Health Sciences
                Anatomy
                Digestive System
                Teeth
                Biology and Life Sciences
                Anatomy
                Head
                Jaw
                Teeth
                Medicine and Health Sciences
                Anatomy
                Head
                Jaw
                Teeth
                Biology and Life Sciences
                Anatomy
                Head
                Jaw
                Medicine and Health Sciences
                Anatomy
                Head
                Jaw
                Biology and Life Sciences
                Anatomy
                Head
                Eyes
                Medicine and Health Sciences
                Anatomy
                Head
                Eyes
                Biology and Life Sciences
                Anatomy
                Ocular System
                Eyes
                Medicine and Health Sciences
                Anatomy
                Ocular System
                Eyes
                Biology and Life Sciences
                Taxonomy
                New Species Reports
                Computer and Information Sciences
                Data Management
                Taxonomy
                New Species Reports
                Custom metadata
                All relevant data are within the manuscript and its Supporting Information files.

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