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

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          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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          Most cited references 77

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          Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization.

          Recent evidence in natural and semi-natural settings has revealed a variety of left-right perceptual asymmetries among vertebrates. These include preferential use of the left or right visual hemifield during activities such as searching for food, agonistic responses, or escape from predators in animals as different as fish, amphibians, reptiles, birds, and mammals. There are obvious disadvantages in showing such directional asymmetries because relevant stimuli may be located to the animal's left or right at random; there is no a priori association between the meaning of a stimulus (e.g., its being a predator or a food item) and its being located to the animal's left or right. Moreover, other organisms (e.g., predators) could exploit the predictability of behavior that arises from population-level lateral biases. It might be argued that lateralization of function enhances cognitive capacity and efficiency of the brain, thus counteracting the ecological disadvantages of lateral biases in behavior. However, such an increase in brain efficiency could be obtained by each individual being lateralized without any need to align the direction of the asymmetry in the majority of the individuals of the population. Here we argue that the alignment of the direction of behavioral asymmetries at the population level arises as an "evolutionarily stable strategy" under "social" pressures occurring when individually asymmetrical organisms must coordinate their behavior with the behavior of other asymmetrical organisms of the same or different species.
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            Maternal hormones as a tool to adjust offspring phenotype in avian species.

            Avian eggs contain substantial amounts of maternal hormones and so provide an excellent model to study hormone-mediated maternal effects. We review this new and rapidly evolving field, taking an ecological and evolutionary approach and focusing on effects and function of maternal androgens in offspring development. Manipulation of yolk levels of androgens within the physiological range indicates that maternal androgens affect behaviour, growth, morphology, immune function and survival of the offspring, in some cases even long after fledging. Descriptive and experimental studies show systematic variation in maternal androgen deposition both within and among clutches, as well as in relation to the sex of the embryo. We discuss the potential adaptive value of maternal androgen transfer at all these three levels. We conclude that maternal androgen deposition in avian eggs provides a flexible mechanism of non-genetic inheritance, by which the mother can favour some offspring over others, and adjust their developmental trajectories to prevailing environmental conditions, producing different phenotypes. However, the literature is less consistent than often assumed and at all three levels, the functional explanations need further experimental testing. The field would greatly benefit from an analysis of the underlying physiological mechanisms.
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              Developmental origins of disease paradigm: a mechanistic and evolutionary perspective.

              Fetal growth is determined by the interaction between the environment and the fetal genome. The fetal environment, in turn, is determined by the maternal environment and by maternal and placental physiology. There is evidence that the interaction between the fetal environment and genome can determine the risk of postnatal disease, as well as the individual's capacity to cope with the postnatal environment. Furthermore, the role of various forms of maternal constraint of fetal growth in determining the persistence of these responses is reviewed. A limited number of biologic processes can contribute to the mechanistic basis of these phenomena. In addition to immediate homeostatic responses, the developing organism may make predictive adaptive responses of no immediate advantage but with long-term consequences. An evolutionary perspective is provided, as well as a review of possible biologic processes. The "developmental origins of disease" paradigm is a reflection of the persistence of such mechanisms in humans who now live in very different environments from those within which they evolved. The developmental origins paradigm and its underlying mechanistic and evolutionary basis have major implications for addressing the increasing burden of metabolic and cardiovascular disease.

                Author and article information

                Front Physiol
                Front Physiol
                Front. Physiol.
                Frontiers in Physiology
                Frontiers Media S.A.
                01 December 2017
                : 8
                Normandie Univ., UNICAEN, Rennes 1 Univ., UR1, CNRS, UMR 6552 ETHOS , Caen, France
                Author notes

                Edited by: Graziano Fiorito, Stazione Zoologica Anton Dohrn, Italy

                Reviewed by: Cinzia Chiandetti, University of Trieste, Italy; Enrico Alleva, Istituto Superiore di Sanità, Italy

                *Correspondence: Ludovic Dickel ludovic.dickel@

                This article was submitted to Invertebrate Physiology, a section of the journal Frontiers in Physiology

                Copyright © 2017 O'Brien, Jozet-Alves, Mezrai, Bellanger, Darmaillacq and Dickel.

                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.

                Page count
                Figures: 7, Tables: 2, Equations: 1, References: 81, Pages: 13, Words: 11102
                Original Research

                Anatomy & Physiology

                threat response, body patterning, activity, visual lateralization, predation


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