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Complex sexually dimorphic traits shape the parallel evolution of a novel reproductive strategy in Sulawesi ricefishes (Adrianichthyidae)

BACKGROUND: Pelvic brooding is a form of uni-parental care, and likely evolved in parallel in two lineages of Sulawesi ricefishes. Contrary to all other ricefishes, females of pelvic brooding species do not deposit eggs at a substrate (transfer brooding), but carry them until the fry hatches. We ass...

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Autores principales: Spanke, Tobias, Hilgers, Leon, Wipfler, Benjamin, Flury, Jana M., Nolte, Arne W., Utama, Ilham V., Misof, Bernhard, Herder, Fabian, Schwarzer, Julia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8056572/
https://www.ncbi.nlm.nih.gov/pubmed/33879056
http://dx.doi.org/10.1186/s12862-021-01791-z
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author Spanke, Tobias
Hilgers, Leon
Wipfler, Benjamin
Flury, Jana M.
Nolte, Arne W.
Utama, Ilham V.
Misof, Bernhard
Herder, Fabian
Schwarzer, Julia
author_facet Spanke, Tobias
Hilgers, Leon
Wipfler, Benjamin
Flury, Jana M.
Nolte, Arne W.
Utama, Ilham V.
Misof, Bernhard
Herder, Fabian
Schwarzer, Julia
author_sort Spanke, Tobias
collection PubMed
description BACKGROUND: Pelvic brooding is a form of uni-parental care, and likely evolved in parallel in two lineages of Sulawesi ricefishes. Contrary to all other ricefishes, females of pelvic brooding species do not deposit eggs at a substrate (transfer brooding), but carry them until the fry hatches. We assume that modifications reducing the costs of egg carrying are beneficial for pelvic brooding females, but likely disadvantageous in conspecific males, which might be resolved by the evolution of sexual dimorphism via sexual antagonistic selection. Thus we hypothesize that the evolution of pelvic brooding gave rise to female-specific skeletal adaptations that are shared by both pelvic brooding lineages, but are absent in conspecific males and transfer brooding species. To tackle this, we combine 3D-imaging and morphometrics to analyze skeletal adaptations to pelvic brooding. RESULTS: The morphology of skeletal traits correlated with sex and brooding strategy across seven ricefish species. Pelvic brooding females have short ribs caudal of the pelvic girdle forming a ventral concavity and clearly elongated and thickened pelvic fins compared to both sexes of transfer brooding species. The ventral concavity limits the body cavity volume in female pelvic brooders. Thus body volumes are smaller compared to males in pelvic brooding species, a pattern sharply contrasted by transfer brooding species. CONCLUSIONS: We showed in a comparative framework that highly similar, sexually dimorphic traits evolved in parallel in both lineages of pelvic brooding ricefish species. Key traits, present in all pelvic brooding females, were absent or much less pronounced in conspecific males and both sexes of transfer brooding species, indicating that they are non-beneficial or even maladaptive for ricefishes not providing extended care. We assume that the combination of ventral concavity and robust, elongated fins reduces drag of brooding females and provides protection and stability to the egg cluster. Thus ricefishes are one of the rare examples where environmental factors rather than sexual selection shaped the evolution of sexually dimorphic skeletal adaptations. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-021-01791-z.
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spelling pubmed-80565722021-04-21 Complex sexually dimorphic traits shape the parallel evolution of a novel reproductive strategy in Sulawesi ricefishes (Adrianichthyidae) Spanke, Tobias Hilgers, Leon Wipfler, Benjamin Flury, Jana M. Nolte, Arne W. Utama, Ilham V. Misof, Bernhard Herder, Fabian Schwarzer, Julia BMC Ecol Evol Research Article BACKGROUND: Pelvic brooding is a form of uni-parental care, and likely evolved in parallel in two lineages of Sulawesi ricefishes. Contrary to all other ricefishes, females of pelvic brooding species do not deposit eggs at a substrate (transfer brooding), but carry them until the fry hatches. We assume that modifications reducing the costs of egg carrying are beneficial for pelvic brooding females, but likely disadvantageous in conspecific males, which might be resolved by the evolution of sexual dimorphism via sexual antagonistic selection. Thus we hypothesize that the evolution of pelvic brooding gave rise to female-specific skeletal adaptations that are shared by both pelvic brooding lineages, but are absent in conspecific males and transfer brooding species. To tackle this, we combine 3D-imaging and morphometrics to analyze skeletal adaptations to pelvic brooding. RESULTS: The morphology of skeletal traits correlated with sex and brooding strategy across seven ricefish species. Pelvic brooding females have short ribs caudal of the pelvic girdle forming a ventral concavity and clearly elongated and thickened pelvic fins compared to both sexes of transfer brooding species. The ventral concavity limits the body cavity volume in female pelvic brooders. Thus body volumes are smaller compared to males in pelvic brooding species, a pattern sharply contrasted by transfer brooding species. CONCLUSIONS: We showed in a comparative framework that highly similar, sexually dimorphic traits evolved in parallel in both lineages of pelvic brooding ricefish species. Key traits, present in all pelvic brooding females, were absent or much less pronounced in conspecific males and both sexes of transfer brooding species, indicating that they are non-beneficial or even maladaptive for ricefishes not providing extended care. We assume that the combination of ventral concavity and robust, elongated fins reduces drag of brooding females and provides protection and stability to the egg cluster. Thus ricefishes are one of the rare examples where environmental factors rather than sexual selection shaped the evolution of sexually dimorphic skeletal adaptations. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-021-01791-z. BioMed Central 2021-04-20 /pmc/articles/PMC8056572/ /pubmed/33879056 http://dx.doi.org/10.1186/s12862-021-01791-z Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Spanke, Tobias
Hilgers, Leon
Wipfler, Benjamin
Flury, Jana M.
Nolte, Arne W.
Utama, Ilham V.
Misof, Bernhard
Herder, Fabian
Schwarzer, Julia
Complex sexually dimorphic traits shape the parallel evolution of a novel reproductive strategy in Sulawesi ricefishes (Adrianichthyidae)
title Complex sexually dimorphic traits shape the parallel evolution of a novel reproductive strategy in Sulawesi ricefishes (Adrianichthyidae)
title_full Complex sexually dimorphic traits shape the parallel evolution of a novel reproductive strategy in Sulawesi ricefishes (Adrianichthyidae)
title_fullStr Complex sexually dimorphic traits shape the parallel evolution of a novel reproductive strategy in Sulawesi ricefishes (Adrianichthyidae)
title_full_unstemmed Complex sexually dimorphic traits shape the parallel evolution of a novel reproductive strategy in Sulawesi ricefishes (Adrianichthyidae)
title_short Complex sexually dimorphic traits shape the parallel evolution of a novel reproductive strategy in Sulawesi ricefishes (Adrianichthyidae)
title_sort complex sexually dimorphic traits shape the parallel evolution of a novel reproductive strategy in sulawesi ricefishes (adrianichthyidae)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8056572/
https://www.ncbi.nlm.nih.gov/pubmed/33879056
http://dx.doi.org/10.1186/s12862-021-01791-z
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