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Increased exposure to acute thermal stress is associated with a non-linear increase in recombination frequency and an independent linear decrease in fitness in Drosophila

BACKGROUND: Meiotic recombination rate has long been known to be phenotypically plastic. How plastic recombination evolves and is maintained remains controversial; though a leading model for the evolution of plastic recombination rests on the tenet that organismal fitness and recombination frequency...

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Autores principales: Jackson, Savannah, Nielsen, Dahlia M., Singh, Nadia D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4551699/
https://www.ncbi.nlm.nih.gov/pubmed/26310872
http://dx.doi.org/10.1186/s12862-015-0452-8
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author Jackson, Savannah
Nielsen, Dahlia M.
Singh, Nadia D.
author_facet Jackson, Savannah
Nielsen, Dahlia M.
Singh, Nadia D.
author_sort Jackson, Savannah
collection PubMed
description BACKGROUND: Meiotic recombination rate has long been known to be phenotypically plastic. How plastic recombination evolves and is maintained remains controversial; though a leading model for the evolution of plastic recombination rests on the tenet that organismal fitness and recombination frequency are negatively correlated. Motivated by the mounting evidence that meiotic recombination frequencies increase in response to stress, here we test for a negative correlation between fitness and recombination frequency. Specifically, the fitness-associated recombination model (FAR) predicts that if stress increases meiotic recombination frequency, then increasing exposure to stressful conditions will yield an increasing magnitude of the recombinational response, while concomitantly decreasing fitness. RESULTS: We use heat shock as a stressor to test this prediction in Drosophila melanogaster. We find that increased exposure to heat shock conditions is associated with a non-linear increase in meiotic recombination frequency. We also find an independent effect of heat shock on organismal fitness, with fitness decreasing with increased duration of thermal stress. CONCLUSIONS: Our results thus support the foundation of the FAR model for the evolution of plastic recombination. Our data also suggest that modulating recombination frequency is one mechanism by which organisms can rapidly respond to environmental cues and confer increased adaptive potential to their offspring. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0452-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-45516992015-08-29 Increased exposure to acute thermal stress is associated with a non-linear increase in recombination frequency and an independent linear decrease in fitness in Drosophila Jackson, Savannah Nielsen, Dahlia M. Singh, Nadia D. BMC Evol Biol Research Article BACKGROUND: Meiotic recombination rate has long been known to be phenotypically plastic. How plastic recombination evolves and is maintained remains controversial; though a leading model for the evolution of plastic recombination rests on the tenet that organismal fitness and recombination frequency are negatively correlated. Motivated by the mounting evidence that meiotic recombination frequencies increase in response to stress, here we test for a negative correlation between fitness and recombination frequency. Specifically, the fitness-associated recombination model (FAR) predicts that if stress increases meiotic recombination frequency, then increasing exposure to stressful conditions will yield an increasing magnitude of the recombinational response, while concomitantly decreasing fitness. RESULTS: We use heat shock as a stressor to test this prediction in Drosophila melanogaster. We find that increased exposure to heat shock conditions is associated with a non-linear increase in meiotic recombination frequency. We also find an independent effect of heat shock on organismal fitness, with fitness decreasing with increased duration of thermal stress. CONCLUSIONS: Our results thus support the foundation of the FAR model for the evolution of plastic recombination. Our data also suggest that modulating recombination frequency is one mechanism by which organisms can rapidly respond to environmental cues and confer increased adaptive potential to their offspring. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0452-8) contains supplementary material, which is available to authorized users. BioMed Central 2015-08-27 /pmc/articles/PMC4551699/ /pubmed/26310872 http://dx.doi.org/10.1186/s12862-015-0452-8 Text en © Jackson et al. 2015 Open Access This 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
Jackson, Savannah
Nielsen, Dahlia M.
Singh, Nadia D.
Increased exposure to acute thermal stress is associated with a non-linear increase in recombination frequency and an independent linear decrease in fitness in Drosophila
title Increased exposure to acute thermal stress is associated with a non-linear increase in recombination frequency and an independent linear decrease in fitness in Drosophila
title_full Increased exposure to acute thermal stress is associated with a non-linear increase in recombination frequency and an independent linear decrease in fitness in Drosophila
title_fullStr Increased exposure to acute thermal stress is associated with a non-linear increase in recombination frequency and an independent linear decrease in fitness in Drosophila
title_full_unstemmed Increased exposure to acute thermal stress is associated with a non-linear increase in recombination frequency and an independent linear decrease in fitness in Drosophila
title_short Increased exposure to acute thermal stress is associated with a non-linear increase in recombination frequency and an independent linear decrease in fitness in Drosophila
title_sort increased exposure to acute thermal stress is associated with a non-linear increase in recombination frequency and an independent linear decrease in fitness in drosophila
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4551699/
https://www.ncbi.nlm.nih.gov/pubmed/26310872
http://dx.doi.org/10.1186/s12862-015-0452-8
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