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Physiological mechanisms of adaptive developmental plasticity in Rana temporaria island populations

BACKGROUND: Adaptive plasticity is essential for many species to cope with environmental heterogeneity. In particular, developmental plasticity allows organisms with complex life cycles to adaptively adjust the timing of ontogenetic switch points. Size at and time to metamorphosis are reliable fitne...

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Autores principales: Burraco, Pablo, Valdés, Ana Elisa, Johansson, Frank, Gomez-Mestre, Ivan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5501514/
https://www.ncbi.nlm.nih.gov/pubmed/28683754
http://dx.doi.org/10.1186/s12862-017-1004-1
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author Burraco, Pablo
Valdés, Ana Elisa
Johansson, Frank
Gomez-Mestre, Ivan
author_facet Burraco, Pablo
Valdés, Ana Elisa
Johansson, Frank
Gomez-Mestre, Ivan
author_sort Burraco, Pablo
collection PubMed
description BACKGROUND: Adaptive plasticity is essential for many species to cope with environmental heterogeneity. In particular, developmental plasticity allows organisms with complex life cycles to adaptively adjust the timing of ontogenetic switch points. Size at and time to metamorphosis are reliable fitness indicators in organisms with complex cycles. The physiological machinery of developmental plasticity commonly involves the activation of alternative neuroendocrine pathways, causing metabolic alterations. Nevertheless, we have still incomplete knowledge about how these mechanisms evolve under environments that select for differences in adaptive plasticity. In this study, we investigate the physiological mechanisms underlying divergent degrees of developmental plasticity across Rana temporaria island populations inhabiting different types of pools in northern Sweden. METHODS: In a laboratory experiment we estimated developmental plasticity of amphibian larvae from six populations coming from three different island habitats: islands with only permanent pools, islands with only ephemeral pools, and islands with a mixture of both types of pools. We exposed larvae of each population to either constant water level or simulated pool drying, and estimated their physiological responses in terms of corticosterone levels, oxidative stress, and telomere length. RESULTS: We found that populations from islands with only temporary pools had a higher degree of developmental plasticity than those from the other two types of habitats. All populations increased their corticosterone levels to a similar extent when subjected to simulated pool drying, and therefore variation in secretion of this hormone does not explain the observed differences among populations. However, tadpoles from islands with temporary pools showed lower constitutive activities of catalase and glutathione reductase, and also showed overall shorter telomeres. CONCLUSIONS: The observed differences are indicative of physiological costs of increased developmental plasticity, suggesting that the potential for plasticity is constrained by its costs. Thus, high levels of responsiveness in the developmental rate of tadpoles have evolved in islands with pools at high but variable risk of desiccation. Moreover, the physiological alterations observed may have important consequences for both short-term odds of survival and long term effects on lifespan. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-017-1004-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-55015142017-07-10 Physiological mechanisms of adaptive developmental plasticity in Rana temporaria island populations Burraco, Pablo Valdés, Ana Elisa Johansson, Frank Gomez-Mestre, Ivan BMC Evol Biol Research Article BACKGROUND: Adaptive plasticity is essential for many species to cope with environmental heterogeneity. In particular, developmental plasticity allows organisms with complex life cycles to adaptively adjust the timing of ontogenetic switch points. Size at and time to metamorphosis are reliable fitness indicators in organisms with complex cycles. The physiological machinery of developmental plasticity commonly involves the activation of alternative neuroendocrine pathways, causing metabolic alterations. Nevertheless, we have still incomplete knowledge about how these mechanisms evolve under environments that select for differences in adaptive plasticity. In this study, we investigate the physiological mechanisms underlying divergent degrees of developmental plasticity across Rana temporaria island populations inhabiting different types of pools in northern Sweden. METHODS: In a laboratory experiment we estimated developmental plasticity of amphibian larvae from six populations coming from three different island habitats: islands with only permanent pools, islands with only ephemeral pools, and islands with a mixture of both types of pools. We exposed larvae of each population to either constant water level or simulated pool drying, and estimated their physiological responses in terms of corticosterone levels, oxidative stress, and telomere length. RESULTS: We found that populations from islands with only temporary pools had a higher degree of developmental plasticity than those from the other two types of habitats. All populations increased their corticosterone levels to a similar extent when subjected to simulated pool drying, and therefore variation in secretion of this hormone does not explain the observed differences among populations. However, tadpoles from islands with temporary pools showed lower constitutive activities of catalase and glutathione reductase, and also showed overall shorter telomeres. CONCLUSIONS: The observed differences are indicative of physiological costs of increased developmental plasticity, suggesting that the potential for plasticity is constrained by its costs. Thus, high levels of responsiveness in the developmental rate of tadpoles have evolved in islands with pools at high but variable risk of desiccation. Moreover, the physiological alterations observed may have important consequences for both short-term odds of survival and long term effects on lifespan. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-017-1004-1) contains supplementary material, which is available to authorized users. BioMed Central 2017-07-07 /pmc/articles/PMC5501514/ /pubmed/28683754 http://dx.doi.org/10.1186/s12862-017-1004-1 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
Burraco, Pablo
Valdés, Ana Elisa
Johansson, Frank
Gomez-Mestre, Ivan
Physiological mechanisms of adaptive developmental plasticity in Rana temporaria island populations
title Physiological mechanisms of adaptive developmental plasticity in Rana temporaria island populations
title_full Physiological mechanisms of adaptive developmental plasticity in Rana temporaria island populations
title_fullStr Physiological mechanisms of adaptive developmental plasticity in Rana temporaria island populations
title_full_unstemmed Physiological mechanisms of adaptive developmental plasticity in Rana temporaria island populations
title_short Physiological mechanisms of adaptive developmental plasticity in Rana temporaria island populations
title_sort physiological mechanisms of adaptive developmental plasticity in rana temporaria island populations
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5501514/
https://www.ncbi.nlm.nih.gov/pubmed/28683754
http://dx.doi.org/10.1186/s12862-017-1004-1
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