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Transgenerational transmission of a stress-coping phenotype programmed by early-life stress in the Japanese quail

View Article: PubMed Central - PubMed

ABSTRACT

An interesting aspect of developmental programming is the existence of transgenerational effects that influence offspring characteristics and performance later in life. These transgenerational effects have been hypothesized to allow individuals to cope better with predictable environmental fluctuations and thus facilitate adaptation to changing environments. Here, we test for the first time how early-life stress drives developmental programming and transgenerational effects of maternal exposure to early-life stress on several phenotypic traits in their offspring in a functionally relevant context using a fully factorial design. We manipulated pre- and/or post-natal stress in both Japanese quail mothers and offspring and examined the consequences for several stress-related traits in the offspring generation. We show that pre-natal stress experienced by the mother did not simply affect offspring phenotype but resulted in the inheritance of the same stress-coping traits in the offspring across all phenotypic levels that we investigated, shaping neuroendocrine, physiological and behavioural traits. This may serve mothers to better prepare their offspring to cope with later environments where the same stressors are experienced.

No MeSH data available.


Related in: MedlinePlus

Diagram of the experimental manipulation of maternal and offspring pre-natal and post-natal stress.We used four groups of Japanese quail females with different developmental experiences in order to obtain the offspring generation. One group was exposed to stress only during pre-natal development via injection of corticosterone in the egg yolk to simulate the transfer of CORT from the mother into her eggs (MatPreCort/MatPostCtrl, n = 11). One group was exposed to stress only during post-natal development by exposing chicks to unpredictable food availability between days 4 and 20 post-hatching (MatPreCtrl/MatPostFood-, n = 6). One group was exposed to stress during both pre- and post-natal development (MatPreCort/Mat/PostFood-, n = 6). The control group was exposed to neither stressor (MatPreCtrl/MatPostCtrl, n = 10). Each female bred once under control condition and once under unpredictable food availability in order to manipulate pre-natal stress of the offspring by increasing maternal stress levels during the laying period (Offspring pre-natal stress manipulation: pre-natally stressed n = 45, control n = 42). Half of the chicks from each pre-natal treatment were exposed to stress again using an unpredictable food availability paradigm (n = 44) while the other half were exposed to control conditions during post-natal development (n = 43). As for the offspring, we thus created four treatment groups: OffPreCtrl/OffPostCtrl (n = 22); OffPreCtrl/OffPostFood- (n = 20), OffPreFood-/OffPostCtrl (n = 21) and OffPreFood-/OffPostFood- (n = 24). This experimental design resulted in 16 treatment combinations.
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f1: Diagram of the experimental manipulation of maternal and offspring pre-natal and post-natal stress.We used four groups of Japanese quail females with different developmental experiences in order to obtain the offspring generation. One group was exposed to stress only during pre-natal development via injection of corticosterone in the egg yolk to simulate the transfer of CORT from the mother into her eggs (MatPreCort/MatPostCtrl, n = 11). One group was exposed to stress only during post-natal development by exposing chicks to unpredictable food availability between days 4 and 20 post-hatching (MatPreCtrl/MatPostFood-, n = 6). One group was exposed to stress during both pre- and post-natal development (MatPreCort/Mat/PostFood-, n = 6). The control group was exposed to neither stressor (MatPreCtrl/MatPostCtrl, n = 10). Each female bred once under control condition and once under unpredictable food availability in order to manipulate pre-natal stress of the offspring by increasing maternal stress levels during the laying period (Offspring pre-natal stress manipulation: pre-natally stressed n = 45, control n = 42). Half of the chicks from each pre-natal treatment were exposed to stress again using an unpredictable food availability paradigm (n = 44) while the other half were exposed to control conditions during post-natal development (n = 43). As for the offspring, we thus created four treatment groups: OffPreCtrl/OffPostCtrl (n = 22); OffPreCtrl/OffPostFood- (n = 20), OffPreFood-/OffPostCtrl (n = 21) and OffPreFood-/OffPostFood- (n = 24). This experimental design resulted in 16 treatment combinations.

Mentions: In this study, we manipulated pre- or/and post-natal stress in both mothers and their offspring in Japanese quail and examined the consequences for several phenotypic traits in the offspring generation, integrating information across physiological, neuroendocrine and behavioural levels. In all offspring, we determined the HPA axis activity by measuring the physiological response (i.e. changes in blood glucocorticoid (GC) levels) to an acute stressor. This stress response enhances physiological processes and behaviours to remove the individual from the stressor and/or facilitate coping. Although this acute response is adaptive, prolonged or repeated exposure to high GC levels can be costly over the long term21. The physiological stress response is tightly regulated by a negative feedback loop at the level of the hippocampus, hypothalamus and pituitary gland to down-regulate the HPA axis, which is mediated by the glucocorticoid receptor (GR) and the mineralocorticoid receptor (MR)2122. We therefore measured the relative expression of both receptors within the HPA axis. At the behavioural level, we measured the exploration of a novel environment. An increased exploration of a novel environment is usually associated with a better capacity to cope with stressful challenges23. We used four groups of Japanese quail (Coturnix japonica) mothers with different developmental experiences: one of the groups was exposed to stress during pre-natal development via injection of corticosterone (CORT) in the egg yolk to simulate the transfer of CORT from the mother into her eggs (n = 11), one group was exposed to stress during post-natal development by exposing chicks to an unpredictable food availability paradigm simulating a stressful foraging environment (n = 6), one group was exposed to stress during both pre- and post-natal development (n = 6) and one control group (n = 10) was exposed to neither stressor624. The offspring of these females were directly exposed to stress during pre-natal development by manipulating maternal stress levels during the laying period using an unpredictable food availability paradigm (n = 45), or to control conditions (n = 42). Half of the chicks from each pre-natal treatment were exposed to stress using again an unpredictable food availability paradigm (n = 44) while the other half were exposed to control conditions during post-natal development (n = 43) (Fig. 1). This experimental design allowed us to determine the relative contribution of pre-natal and post-natal experiences and their potential interactive effects on offspring adult phenotype. It also allowed us to tease apart the effects of direct exposure of offspring to stress during their pre-natal (i.e. via manipulation of maternal stress), and/or post-natal development and the transgenerational effects of maternal exposure to early-life stress during their own pre- and/or post-natal development on shaping offspring phenotype.


Transgenerational transmission of a stress-coping phenotype programmed by early-life stress in the Japanese quail
Diagram of the experimental manipulation of maternal and offspring pre-natal and post-natal stress.We used four groups of Japanese quail females with different developmental experiences in order to obtain the offspring generation. One group was exposed to stress only during pre-natal development via injection of corticosterone in the egg yolk to simulate the transfer of CORT from the mother into her eggs (MatPreCort/MatPostCtrl, n = 11). One group was exposed to stress only during post-natal development by exposing chicks to unpredictable food availability between days 4 and 20 post-hatching (MatPreCtrl/MatPostFood-, n = 6). One group was exposed to stress during both pre- and post-natal development (MatPreCort/Mat/PostFood-, n = 6). The control group was exposed to neither stressor (MatPreCtrl/MatPostCtrl, n = 10). Each female bred once under control condition and once under unpredictable food availability in order to manipulate pre-natal stress of the offspring by increasing maternal stress levels during the laying period (Offspring pre-natal stress manipulation: pre-natally stressed n = 45, control n = 42). Half of the chicks from each pre-natal treatment were exposed to stress again using an unpredictable food availability paradigm (n = 44) while the other half were exposed to control conditions during post-natal development (n = 43). As for the offspring, we thus created four treatment groups: OffPreCtrl/OffPostCtrl (n = 22); OffPreCtrl/OffPostFood- (n = 20), OffPreFood-/OffPostCtrl (n = 21) and OffPreFood-/OffPostFood- (n = 24). This experimental design resulted in 16 treatment combinations.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC5384203&req=5

f1: Diagram of the experimental manipulation of maternal and offspring pre-natal and post-natal stress.We used four groups of Japanese quail females with different developmental experiences in order to obtain the offspring generation. One group was exposed to stress only during pre-natal development via injection of corticosterone in the egg yolk to simulate the transfer of CORT from the mother into her eggs (MatPreCort/MatPostCtrl, n = 11). One group was exposed to stress only during post-natal development by exposing chicks to unpredictable food availability between days 4 and 20 post-hatching (MatPreCtrl/MatPostFood-, n = 6). One group was exposed to stress during both pre- and post-natal development (MatPreCort/Mat/PostFood-, n = 6). The control group was exposed to neither stressor (MatPreCtrl/MatPostCtrl, n = 10). Each female bred once under control condition and once under unpredictable food availability in order to manipulate pre-natal stress of the offspring by increasing maternal stress levels during the laying period (Offspring pre-natal stress manipulation: pre-natally stressed n = 45, control n = 42). Half of the chicks from each pre-natal treatment were exposed to stress again using an unpredictable food availability paradigm (n = 44) while the other half were exposed to control conditions during post-natal development (n = 43). As for the offspring, we thus created four treatment groups: OffPreCtrl/OffPostCtrl (n = 22); OffPreCtrl/OffPostFood- (n = 20), OffPreFood-/OffPostCtrl (n = 21) and OffPreFood-/OffPostFood- (n = 24). This experimental design resulted in 16 treatment combinations.
Mentions: In this study, we manipulated pre- or/and post-natal stress in both mothers and their offspring in Japanese quail and examined the consequences for several phenotypic traits in the offspring generation, integrating information across physiological, neuroendocrine and behavioural levels. In all offspring, we determined the HPA axis activity by measuring the physiological response (i.e. changes in blood glucocorticoid (GC) levels) to an acute stressor. This stress response enhances physiological processes and behaviours to remove the individual from the stressor and/or facilitate coping. Although this acute response is adaptive, prolonged or repeated exposure to high GC levels can be costly over the long term21. The physiological stress response is tightly regulated by a negative feedback loop at the level of the hippocampus, hypothalamus and pituitary gland to down-regulate the HPA axis, which is mediated by the glucocorticoid receptor (GR) and the mineralocorticoid receptor (MR)2122. We therefore measured the relative expression of both receptors within the HPA axis. At the behavioural level, we measured the exploration of a novel environment. An increased exploration of a novel environment is usually associated with a better capacity to cope with stressful challenges23. We used four groups of Japanese quail (Coturnix japonica) mothers with different developmental experiences: one of the groups was exposed to stress during pre-natal development via injection of corticosterone (CORT) in the egg yolk to simulate the transfer of CORT from the mother into her eggs (n = 11), one group was exposed to stress during post-natal development by exposing chicks to an unpredictable food availability paradigm simulating a stressful foraging environment (n = 6), one group was exposed to stress during both pre- and post-natal development (n = 6) and one control group (n = 10) was exposed to neither stressor624. The offspring of these females were directly exposed to stress during pre-natal development by manipulating maternal stress levels during the laying period using an unpredictable food availability paradigm (n = 45), or to control conditions (n = 42). Half of the chicks from each pre-natal treatment were exposed to stress using again an unpredictable food availability paradigm (n = 44) while the other half were exposed to control conditions during post-natal development (n = 43) (Fig. 1). This experimental design allowed us to determine the relative contribution of pre-natal and post-natal experiences and their potential interactive effects on offspring adult phenotype. It also allowed us to tease apart the effects of direct exposure of offspring to stress during their pre-natal (i.e. via manipulation of maternal stress), and/or post-natal development and the transgenerational effects of maternal exposure to early-life stress during their own pre- and/or post-natal development on shaping offspring phenotype.

View Article: PubMed Central - PubMed

ABSTRACT

An interesting aspect of developmental programming is the existence of transgenerational effects that influence offspring characteristics and performance later in life. These transgenerational effects have been hypothesized to allow individuals to cope better with predictable environmental fluctuations and thus facilitate adaptation to changing environments. Here, we test for the first time how early-life stress drives developmental programming and transgenerational effects of maternal exposure to early-life stress on several phenotypic traits in their offspring in a functionally relevant context using a fully factorial design. We manipulated pre- and/or post-natal stress in both Japanese quail mothers and offspring and examined the consequences for several stress-related traits in the offspring generation. We show that pre-natal stress experienced by the mother did not simply affect offspring phenotype but resulted in the inheritance of the same stress-coping traits in the offspring across all phenotypic levels that we investigated, shaping neuroendocrine, physiological and behavioural traits. This may serve mothers to better prepare their offspring to cope with later environments where the same stressors are experienced.

No MeSH data available.


Related in: MedlinePlus