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Ancestral reconstruction of reproductive traits shows no tendency toward terrestriality in leptodactyline frogs

BACKGROUND: Traditionally, the evolution of terrestrial reproduction in anurans from ancestors that bred in water has been accepted in the literature. Still, the existence of intermediate stages of water dependency, such as species that lay eggs close to water (e.g., in burrows) instead of in bodies...

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Autores principales: Pereira, Elisa Barreto, Collevatti, Rosane Garcia, Kokubum, Marcelo Nogueira de Carvalho, Miranda, Núbia Esther de Oliveira, Maciel, Natan Medeiros
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4437749/
https://www.ncbi.nlm.nih.gov/pubmed/25987435
http://dx.doi.org/10.1186/s12862-015-0365-6
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author Pereira, Elisa Barreto
Collevatti, Rosane Garcia
Kokubum, Marcelo Nogueira de Carvalho
Miranda, Núbia Esther de Oliveira
Maciel, Natan Medeiros
author_facet Pereira, Elisa Barreto
Collevatti, Rosane Garcia
Kokubum, Marcelo Nogueira de Carvalho
Miranda, Núbia Esther de Oliveira
Maciel, Natan Medeiros
author_sort Pereira, Elisa Barreto
collection PubMed
description BACKGROUND: Traditionally, the evolution of terrestrial reproduction in anurans from ancestors that bred in water has been accepted in the literature. Still, the existence of intermediate stages of water dependency, such as species that lay eggs close to water (e.g., in burrows) instead of in bodies of water, supports the hypothesis of an ordered and gradual evolution in the direction of a more terrestrial form of reproduction. However, this conventional view has recently been challenged for some anurans groups. Leptodactylinae frogs are a remarkable example of anurans with an outstanding diversity in terms of reproductive features, with distinct water dependency among lineages. Here, we tested the hypothesis of a gradual and ordered tendency towards terrestriality in Leptodactylinae, including the existence of obligatory intermediate stages, such as semi-terrestrial reproductive strategies. We also addressed the association between reproductive modes and the morphological and ecological features. RESULTS: An ancestral reconstruction analysis indicated that even though shifts from aquatic to terrestrial breeding occurred throughout the history of Leptodactylus and Adenomera, shifts from terrestrial to aquatic reproduction happened at almost the same frequency. Our results also demonstrated that reproductive modes for semi-terrestrial tadpoles were not necessarily an intermediate form between aquatic and terrestrial breeds. Correlations among reproductive modes and other life-history traits suggested that tadpole environment, clutch size, nuptial spines, and egg pigmentation were co-evolving and driven by water dependency. CONCLUSIONS: Our results found no evidence of evolutionary tendencies toward terrestriality in Leptodactylinae. We found reversals from terrestrial to aquatic tadpole development and no evidence of obligatory intermediate stages, such as semi-terrestrial reproductive strategies. We also found correlations between reproductive modes and other life-history traits driven by water dependence. Aquatic reproductive modes are associated with higher clutch sizes, lentic waters, and the presence of nuptial spines and egg pigmentation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0365-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-44377492015-05-20 Ancestral reconstruction of reproductive traits shows no tendency toward terrestriality in leptodactyline frogs Pereira, Elisa Barreto Collevatti, Rosane Garcia Kokubum, Marcelo Nogueira de Carvalho Miranda, Núbia Esther de Oliveira Maciel, Natan Medeiros BMC Evol Biol Research Article BACKGROUND: Traditionally, the evolution of terrestrial reproduction in anurans from ancestors that bred in water has been accepted in the literature. Still, the existence of intermediate stages of water dependency, such as species that lay eggs close to water (e.g., in burrows) instead of in bodies of water, supports the hypothesis of an ordered and gradual evolution in the direction of a more terrestrial form of reproduction. However, this conventional view has recently been challenged for some anurans groups. Leptodactylinae frogs are a remarkable example of anurans with an outstanding diversity in terms of reproductive features, with distinct water dependency among lineages. Here, we tested the hypothesis of a gradual and ordered tendency towards terrestriality in Leptodactylinae, including the existence of obligatory intermediate stages, such as semi-terrestrial reproductive strategies. We also addressed the association between reproductive modes and the morphological and ecological features. RESULTS: An ancestral reconstruction analysis indicated that even though shifts from aquatic to terrestrial breeding occurred throughout the history of Leptodactylus and Adenomera, shifts from terrestrial to aquatic reproduction happened at almost the same frequency. Our results also demonstrated that reproductive modes for semi-terrestrial tadpoles were not necessarily an intermediate form between aquatic and terrestrial breeds. Correlations among reproductive modes and other life-history traits suggested that tadpole environment, clutch size, nuptial spines, and egg pigmentation were co-evolving and driven by water dependency. CONCLUSIONS: Our results found no evidence of evolutionary tendencies toward terrestriality in Leptodactylinae. We found reversals from terrestrial to aquatic tadpole development and no evidence of obligatory intermediate stages, such as semi-terrestrial reproductive strategies. We also found correlations between reproductive modes and other life-history traits driven by water dependence. Aquatic reproductive modes are associated with higher clutch sizes, lentic waters, and the presence of nuptial spines and egg pigmentation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0365-6) contains supplementary material, which is available to authorized users. BioMed Central 2015-05-20 /pmc/articles/PMC4437749/ /pubmed/25987435 http://dx.doi.org/10.1186/s12862-015-0365-6 Text en © Pereira et al.; licensee BioMed Central. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Pereira, Elisa Barreto
Collevatti, Rosane Garcia
Kokubum, Marcelo Nogueira de Carvalho
Miranda, Núbia Esther de Oliveira
Maciel, Natan Medeiros
Ancestral reconstruction of reproductive traits shows no tendency toward terrestriality in leptodactyline frogs
title Ancestral reconstruction of reproductive traits shows no tendency toward terrestriality in leptodactyline frogs
title_full Ancestral reconstruction of reproductive traits shows no tendency toward terrestriality in leptodactyline frogs
title_fullStr Ancestral reconstruction of reproductive traits shows no tendency toward terrestriality in leptodactyline frogs
title_full_unstemmed Ancestral reconstruction of reproductive traits shows no tendency toward terrestriality in leptodactyline frogs
title_short Ancestral reconstruction of reproductive traits shows no tendency toward terrestriality in leptodactyline frogs
title_sort ancestral reconstruction of reproductive traits shows no tendency toward terrestriality in leptodactyline frogs
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4437749/
https://www.ncbi.nlm.nih.gov/pubmed/25987435
http://dx.doi.org/10.1186/s12862-015-0365-6
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