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Phenotypic integration mediated by hormones: associations among digit ratios, body size and testosterone during tadpole development

BACKGROUND: Developmental associations often explain phenotypic integration. The intersected hormonal regulation of ontogenetic processes fosters predictions of steroid-mediated phenotypic integration among sexually dimorphic traits, a statement defied by associations between classical dimorphism pr...

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Autores principales: Lofeu, Leandro, Brandt, Renata, Kohlsdorf, Tiana
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5541650/
https://www.ncbi.nlm.nih.gov/pubmed/28768472
http://dx.doi.org/10.1186/s12862-017-1021-0
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author Lofeu, Leandro
Brandt, Renata
Kohlsdorf, Tiana
author_facet Lofeu, Leandro
Brandt, Renata
Kohlsdorf, Tiana
author_sort Lofeu, Leandro
collection PubMed
description BACKGROUND: Developmental associations often explain phenotypic integration. The intersected hormonal regulation of ontogenetic processes fosters predictions of steroid-mediated phenotypic integration among sexually dimorphic traits, a statement defied by associations between classical dimorphism predictors (e.g. body size) and traits that apparently lack sex-specific functions (e.g. ratios between the lengths of Digits II and IV - 2D:4D). Developmental bases of female-biased 2D:4D have been identified, but these remain unclear for taxa presenting male-biased 2D:4D (e.g. anura). Here we propose two alternative hypotheses to investigate evolution of male-biased 2D:4D associated with sexually dimorphic body size using Leptodactylus frogs: I)‘hypothesis of sex-specific digit responses’ - Digit IV would be reactive to testosterone but exhibit responses in the opposite direction of those observed in female-biased 2D:4D lineages, so that Digit IV turns shorter in males; II) ‘hypothesis of identity of the dimorphic digit’- Digit II would be the dimorphic digit. RESULTS: We compiled the following databases using Leptodactylus frogs: 1) adults of two species from natural populations and 2) testosterone-treated L. fuscus at post-metamorphic stage. Studied traits seem monomorphic in L. fuscus; L. podicipinus exhibits male-biased 2D:4D. When present, 2D:4D dimorphism was male-biased and associated with dimorphic body size; sex differences resided on Digit II instead of IV, corroborating our ‘hypothesis of identity of the dimorphic digit’. Developmental steroid roles were validated: testosterone-treated L. fuscus frogs were smaller and exhibited masculinized 2D:4D, and Digit II was the digit that responded to testosterone. CONCLUSION: We propose a model where evolution of sexual dimorphism in 2D:4D first originates from the advent, in a given digit, of increased tissue sensitivity to steroids. Phenotypic integration with other sexually dimorphic traits would then occur through multi-trait hormonal effects during development. Such process of phenotypic integration seems fitness-independent in its origin and might explain several cases of steroid-mediated integration among sexually dimorphic traits. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-017-1021-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-55416502017-08-07 Phenotypic integration mediated by hormones: associations among digit ratios, body size and testosterone during tadpole development Lofeu, Leandro Brandt, Renata Kohlsdorf, Tiana BMC Evol Biol Research Article BACKGROUND: Developmental associations often explain phenotypic integration. The intersected hormonal regulation of ontogenetic processes fosters predictions of steroid-mediated phenotypic integration among sexually dimorphic traits, a statement defied by associations between classical dimorphism predictors (e.g. body size) and traits that apparently lack sex-specific functions (e.g. ratios between the lengths of Digits II and IV - 2D:4D). Developmental bases of female-biased 2D:4D have been identified, but these remain unclear for taxa presenting male-biased 2D:4D (e.g. anura). Here we propose two alternative hypotheses to investigate evolution of male-biased 2D:4D associated with sexually dimorphic body size using Leptodactylus frogs: I)‘hypothesis of sex-specific digit responses’ - Digit IV would be reactive to testosterone but exhibit responses in the opposite direction of those observed in female-biased 2D:4D lineages, so that Digit IV turns shorter in males; II) ‘hypothesis of identity of the dimorphic digit’- Digit II would be the dimorphic digit. RESULTS: We compiled the following databases using Leptodactylus frogs: 1) adults of two species from natural populations and 2) testosterone-treated L. fuscus at post-metamorphic stage. Studied traits seem monomorphic in L. fuscus; L. podicipinus exhibits male-biased 2D:4D. When present, 2D:4D dimorphism was male-biased and associated with dimorphic body size; sex differences resided on Digit II instead of IV, corroborating our ‘hypothesis of identity of the dimorphic digit’. Developmental steroid roles were validated: testosterone-treated L. fuscus frogs were smaller and exhibited masculinized 2D:4D, and Digit II was the digit that responded to testosterone. CONCLUSION: We propose a model where evolution of sexual dimorphism in 2D:4D first originates from the advent, in a given digit, of increased tissue sensitivity to steroids. Phenotypic integration with other sexually dimorphic traits would then occur through multi-trait hormonal effects during development. Such process of phenotypic integration seems fitness-independent in its origin and might explain several cases of steroid-mediated integration among sexually dimorphic traits. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-017-1021-0) contains supplementary material, which is available to authorized users. BioMed Central 2017-08-02 /pmc/articles/PMC5541650/ /pubmed/28768472 http://dx.doi.org/10.1186/s12862-017-1021-0 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
Lofeu, Leandro
Brandt, Renata
Kohlsdorf, Tiana
Phenotypic integration mediated by hormones: associations among digit ratios, body size and testosterone during tadpole development
title Phenotypic integration mediated by hormones: associations among digit ratios, body size and testosterone during tadpole development
title_full Phenotypic integration mediated by hormones: associations among digit ratios, body size and testosterone during tadpole development
title_fullStr Phenotypic integration mediated by hormones: associations among digit ratios, body size and testosterone during tadpole development
title_full_unstemmed Phenotypic integration mediated by hormones: associations among digit ratios, body size and testosterone during tadpole development
title_short Phenotypic integration mediated by hormones: associations among digit ratios, body size and testosterone during tadpole development
title_sort phenotypic integration mediated by hormones: associations among digit ratios, body size and testosterone during tadpole development
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5541650/
https://www.ncbi.nlm.nih.gov/pubmed/28768472
http://dx.doi.org/10.1186/s12862-017-1021-0
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