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Maternal and Embryonic Stress Influence Offspring Behavior in the Cuttlefish Sepia officinalis

Stress experienced during prenatal development—either applied to reproducing females (maternal stress), directly to developing offspring (embryonic stress) or in combination—is associated with a range of post-natal behavioral effects in numerous organisms. We conducted an experiment to discern if ma...

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Autores principales: O'Brien, Caitlin E., Jozet-Alves, Christelle, Mezrai, Nawel, Bellanger, Cécile, Darmaillacq, Anne-Sophie, Dickel, Ludovic
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5717421/
https://www.ncbi.nlm.nih.gov/pubmed/29249984
http://dx.doi.org/10.3389/fphys.2017.00981
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author O'Brien, Caitlin E.
Jozet-Alves, Christelle
Mezrai, Nawel
Bellanger, Cécile
Darmaillacq, Anne-Sophie
Dickel, Ludovic
author_facet O'Brien, Caitlin E.
Jozet-Alves, Christelle
Mezrai, Nawel
Bellanger, Cécile
Darmaillacq, Anne-Sophie
Dickel, Ludovic
author_sort O'Brien, Caitlin E.
collection PubMed
description Stress experienced during prenatal development—either applied to reproducing females (maternal stress), directly to developing offspring (embryonic stress) or in combination—is associated with a range of post-natal behavioral effects in numerous organisms. We conducted an experiment to discern if maternal and embryonic stressors affect the behavior of hatchlings of the cuttlefish Sepia officinalis, a species with features that allow for the examination of these stress types in isolation. Separating the impact of stress transmitted through the mother vs. stress experienced by the embryo itself will help clarify the behavioral findings in viviparous species for which it is impossible to disentangle these effects. We also compared the effect of a naturally-occurring (predator cue) and an “artificial” (bright, randomly-occurring LED light) embryonic stressor. This allowed us to test the hypothesis that a threat commonly faced by a species (natural threat) would be met with a genetically-programmed and adaptive response while a novel one would confound innate defense mechanisms and lead to maladaptive effects. We found that the maternal stressor was associated with significant differences in body patterning and activity patterns. By contrast, embryonic exposure to stressors increased the proportion of individuals that pursued prey. From these results, it appears that in cuttlefish, maternal and embryonic stressors affect different post-natal behavior in offspring. In addition, the effect of the artificial stressor suggests that organisms can sometimes react adaptively to a stressor even if it is not one that has been encountered during the evolutionary history of the species.
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spelling pubmed-57174212017-12-15 Maternal and Embryonic Stress Influence Offspring Behavior in the Cuttlefish Sepia officinalis O'Brien, Caitlin E. Jozet-Alves, Christelle Mezrai, Nawel Bellanger, Cécile Darmaillacq, Anne-Sophie Dickel, Ludovic Front Physiol Physiology Stress experienced during prenatal development—either applied to reproducing females (maternal stress), directly to developing offspring (embryonic stress) or in combination—is associated with a range of post-natal behavioral effects in numerous organisms. We conducted an experiment to discern if maternal and embryonic stressors affect the behavior of hatchlings of the cuttlefish Sepia officinalis, a species with features that allow for the examination of these stress types in isolation. Separating the impact of stress transmitted through the mother vs. stress experienced by the embryo itself will help clarify the behavioral findings in viviparous species for which it is impossible to disentangle these effects. We also compared the effect of a naturally-occurring (predator cue) and an “artificial” (bright, randomly-occurring LED light) embryonic stressor. This allowed us to test the hypothesis that a threat commonly faced by a species (natural threat) would be met with a genetically-programmed and adaptive response while a novel one would confound innate defense mechanisms and lead to maladaptive effects. We found that the maternal stressor was associated with significant differences in body patterning and activity patterns. By contrast, embryonic exposure to stressors increased the proportion of individuals that pursued prey. From these results, it appears that in cuttlefish, maternal and embryonic stressors affect different post-natal behavior in offspring. In addition, the effect of the artificial stressor suggests that organisms can sometimes react adaptively to a stressor even if it is not one that has been encountered during the evolutionary history of the species. Frontiers Media S.A. 2017-12-01 /pmc/articles/PMC5717421/ /pubmed/29249984 http://dx.doi.org/10.3389/fphys.2017.00981 Text en Copyright © 2017 O'Brien, Jozet-Alves, Mezrai, Bellanger, Darmaillacq and Dickel. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
O'Brien, Caitlin E.
Jozet-Alves, Christelle
Mezrai, Nawel
Bellanger, Cécile
Darmaillacq, Anne-Sophie
Dickel, Ludovic
Maternal and Embryonic Stress Influence Offspring Behavior in the Cuttlefish Sepia officinalis
title Maternal and Embryonic Stress Influence Offspring Behavior in the Cuttlefish Sepia officinalis
title_full Maternal and Embryonic Stress Influence Offspring Behavior in the Cuttlefish Sepia officinalis
title_fullStr Maternal and Embryonic Stress Influence Offspring Behavior in the Cuttlefish Sepia officinalis
title_full_unstemmed Maternal and Embryonic Stress Influence Offspring Behavior in the Cuttlefish Sepia officinalis
title_short Maternal and Embryonic Stress Influence Offspring Behavior in the Cuttlefish Sepia officinalis
title_sort maternal and embryonic stress influence offspring behavior in the cuttlefish sepia officinalis
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5717421/
https://www.ncbi.nlm.nih.gov/pubmed/29249984
http://dx.doi.org/10.3389/fphys.2017.00981
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