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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

Maternal exposure to pre-natal stress resulted in an attenuated stress response in their offspring.CORT level modification in response to a capture-handling-restraint protocol in offspring of mothers exposed to pre- and post-natal control treatments (white dots and solid line), of mothers exposed to pre-natal control and post-natal stress treatments (white dots and dashed line), of mothers exposed to pre-natal stress and post-natal control treatments (black dots and solid line) and of mothers exposed to pre- and post-natal stress treatments (black dots and dashed line). Values are means ± SEM. Different letters indicate significant differences.
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f2: Maternal exposure to pre-natal stress resulted in an attenuated stress response in their offspring.CORT level modification in response to a capture-handling-restraint protocol in offspring of mothers exposed to pre- and post-natal control treatments (white dots and solid line), of mothers exposed to pre-natal control and post-natal stress treatments (white dots and dashed line), of mothers exposed to pre-natal stress and post-natal control treatments (black dots and solid line) and of mothers exposed to pre- and post-natal stress treatments (black dots and dashed line). Values are means ± SEM. Different letters indicate significant differences.

Mentions: Corticosterone (CORT) levels of offspring measured in adulthood were significantly influenced by the time upon capture by the experimenter (Table 1). Basal CORT (i.e. measured within 3 minutes of capture: 0.89 ± 0.07 ng.ml−1) was lower than CORT levels at 10 (2.65 ± 0.23 ng.ml−1) (t71 = 12.4, p < 0.0001) and at 30 (1.43 ± 0.13 ng.ml−1) minutes after capture (t171 = 6.0, p = 0.001) and the level at 10 minutes was higher than at 30 minutes after capture (t170 = 6.4, p < 0.001) (Fig. 2). This stress response over time was significantly influenced by maternal developmental experience at both developmental stages (maternal pre-natal treatment × maternal post-natal treatment × sampling time; Table 1). The multiple comparisons showed that this effect was mainly driven by maternal pre-natal treatment: for individuals whose mothers were exposed to pre-natal stress (MatPreCort), CORT concentrations significantly decreased between 10 and 30 minutes after capture (t170 ≥ 4.2, p ≤ 0.003; Fig. 2) and levels 30 min after capture did not significantly differ from baseline (MatPreCort) (t172 ≤ 2.0, p ≥ 0.69; Fig. 2) regardless of the maternal post-natal treatment. This decrease was not significant for individuals whose mothers were exposed to the pre-natal control treatment (MatPreCtrl) (t170 ≤ 2.3, p ≥ 0.48; Fig. 2), where CORT levels 30 min after capture remained significantly higher than basal levels (t172 ≥ 3.8, p ≤ 0.010; Fig. 2) regardless of the maternal post-natal treatment. However, offspring CORT levels 30 min after capture were not significantly different between individuals from mothers exposed to pre-natal stress (MatPreCort) or pre-natal control treatment (MatPreCtrl) regardless of maternal post-natal treatment (t160 ≤ 1.3, p ≥ 0.97; Fig. 2).


Transgenerational transmission of a stress-coping phenotype programmed by early-life stress in the Japanese quail
Maternal exposure to pre-natal stress resulted in an attenuated stress response in their offspring.CORT level modification in response to a capture-handling-restraint protocol in offspring of mothers exposed to pre- and post-natal control treatments (white dots and solid line), of mothers exposed to pre-natal control and post-natal stress treatments (white dots and dashed line), of mothers exposed to pre-natal stress and post-natal control treatments (black dots and solid line) and of mothers exposed to pre- and post-natal stress treatments (black dots and dashed line). Values are means ± SEM. Different letters indicate significant differences.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5384203&req=5

f2: Maternal exposure to pre-natal stress resulted in an attenuated stress response in their offspring.CORT level modification in response to a capture-handling-restraint protocol in offspring of mothers exposed to pre- and post-natal control treatments (white dots and solid line), of mothers exposed to pre-natal control and post-natal stress treatments (white dots and dashed line), of mothers exposed to pre-natal stress and post-natal control treatments (black dots and solid line) and of mothers exposed to pre- and post-natal stress treatments (black dots and dashed line). Values are means ± SEM. Different letters indicate significant differences.
Mentions: Corticosterone (CORT) levels of offspring measured in adulthood were significantly influenced by the time upon capture by the experimenter (Table 1). Basal CORT (i.e. measured within 3 minutes of capture: 0.89 ± 0.07 ng.ml−1) was lower than CORT levels at 10 (2.65 ± 0.23 ng.ml−1) (t71 = 12.4, p < 0.0001) and at 30 (1.43 ± 0.13 ng.ml−1) minutes after capture (t171 = 6.0, p = 0.001) and the level at 10 minutes was higher than at 30 minutes after capture (t170 = 6.4, p < 0.001) (Fig. 2). This stress response over time was significantly influenced by maternal developmental experience at both developmental stages (maternal pre-natal treatment × maternal post-natal treatment × sampling time; Table 1). The multiple comparisons showed that this effect was mainly driven by maternal pre-natal treatment: for individuals whose mothers were exposed to pre-natal stress (MatPreCort), CORT concentrations significantly decreased between 10 and 30 minutes after capture (t170 ≥ 4.2, p ≤ 0.003; Fig. 2) and levels 30 min after capture did not significantly differ from baseline (MatPreCort) (t172 ≤ 2.0, p ≥ 0.69; Fig. 2) regardless of the maternal post-natal treatment. This decrease was not significant for individuals whose mothers were exposed to the pre-natal control treatment (MatPreCtrl) (t170 ≤ 2.3, p ≥ 0.48; Fig. 2), where CORT levels 30 min after capture remained significantly higher than basal levels (t172 ≥ 3.8, p ≤ 0.010; Fig. 2) regardless of the maternal post-natal treatment. However, offspring CORT levels 30 min after capture were not significantly different between individuals from mothers exposed to pre-natal stress (MatPreCort) or pre-natal control treatment (MatPreCtrl) regardless of maternal post-natal treatment (t160 ≤ 1.3, p ≥ 0.97; Fig. 2).

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