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Stress and the Offspring: Adaptive Transgenerational Effects of Unpredictability on Behaviour and Gene Expression in Chickens (Gallus gallus)
Linköping University, Department of Physics, Chemistry and Biology, Zoology . Linköping University, The Institute of Technology. (Applied Ethology)
2008 (English)Licentiate thesis, comprehensive summary (Other academic)
Abstract [en]

Environmental stress has shown to affect both the exposed individuals and the development of their offspring. Generally, it is thought that the stressed organism responds to stress by trying to adapt to it. This thesis investigates possible evolutionary consequences of cross-generational transmissions of stress, where the parent has been stressed but the offspring has not. In two studies we have exposed chicken parents of different breeds to an unpredictable circadian light rhythm, to investigate the influence of genetic background on the transmission of behaviour and patterns of genome-wide gene expression across generations. In Paper I, we can show that the domesticated chicken, by means of epigenetic factors, transmit their behaviours as well as their gene expression profiles to their offspring to a higher extent than their wild ancestor, the red junglefowl. Furthermore, in Paper II, even though the offspring never experienced the stress or had any contact with their stressed parents, they seemed to have adapted to it, which suggests that the parents might have prepared (or pre-adapted) them for living in the unpredictable environment. Additionally, eggs of stressed hens showed increased levels of estradiol that might have affected gene expression of specific immune genes, which were up-regulated in the offspring of stressed parents. It is possible that the traditional distinction between stress responses and evolutionary adaptation may be reevaluated, since our results indicate that they could be parts of the same evolutionary event.

Place, publisher, year, edition, pages
Linköping: Linköping University Electronic Press , 2008. , 22 p.
Linköping Studies in Science and Technology. Thesis, ISSN 0280-7971 ; 1385
Keyword [en]
Chicken, Red junglefowl, Domestication, Epigenetics, Transgenerational, Inheritance, Gene expression, Microarray, qRT-PCR, Immunogenetics, Immunoglobulin, Estradiol, Steriod hormones, Prenatal stress, Epigenetic inheritance, Adaptation, Stress, Behaviour
URN: urn:nbn:se:liu:diva-15518ISBN: 978-91-7393-753-5OAI: diva2:117473
2008-12-04, Schrödinger E324, Linköpings Universitet, Department of Physics, Chemistry and Biology, 58183 Linköping, Sweden , Linköping, 13:00 (English)
Available from: 2008-11-14 Created: 2008-11-13 Last updated: 2009-05-11Bibliographically approved
List of papers
1. Transmission of Stress-Induced Learning Impairment and Associated Brain Gene Expression from Parents to Offspring in Chickens
Open this publication in new window or tab >>Transmission of Stress-Induced Learning Impairment and Associated Brain Gene Expression from Parents to Offspring in Chickens
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2007 (English)In: PLoS ONE, ISSN 1932-6203, Vol. 2, no 4, e364- p.Article in journal (Refereed) Published
Abstract [en]

Background: Stress influences many aspects of animal behaviour and is a major factor driving populations to adapt to changing living conditions, such as during domestication. Stress can affect offspring through non-genetic mechanisms, but recent research indicates that inherited epigenetic modifications of the genome could possibly also be involved.

Methodology/Principal Findings: Red junglefowl (RJF, ancestors of modern chickens) and domesticated White Leghorn (WL) chickens were raised in a stressful environment (unpredictable light-dark rhythm) and control animals in similar pens, but on a 12/12 h light-dark rhythm. WL in both treatments had poorer spatial learning ability than RJF, and in both populations, stress caused a reduced ability to solve a spatial learning task. Offspring of stressed WL, but not RJF, raised without parental contact, had a reduced spatial learning ability compared to offspring of non-stressed animals in a similar test as that used for their parents. Offspring of stressed WL were also more competitive and grew faster than offspring of non-stressed parents. Using a whole-genome cDNA microarray, we found that in WL, the same changes in hypothalamic gene expression profile caused by stress in the parents were also found in the offspring. In offspring of stressed WL, at least 31 genes were up- or down-regulated in the hypothalamus and pituitary compared to offspring of non-stressed parents.

Conclusions/ Significance: Our results suggest that, in WL the gene expression response to stress, as well as some behavioural stress responses, were transmitted across generations. The ability to transmit epigenetic information and behaviour modifications between generations may therefore have been favoured by domestication. The mechanisms involved remain to be investigated; epigenetic modifications could either have been inherited or acquired de novo in the specific egg environment. In both cases, this would offer a novel explanation to rapid evolutionary adaptation of a population.

Stress, Prenatal stress, Animal behaviour, Gene expresssion, Domestication, Chicken, Red junglefowl, White Leghorn, Epigenetics, Transgenerational effects, Epigenetic inheritance, Maternal effects, Paternal effects
urn:nbn:se:liu:diva-15529 (URN)10.1371/journal.pone.0000364 (DOI)
Available from: 2008-11-17 Created: 2008-11-14 Last updated: 2011-08-22Bibliographically approved
2. Transgenerational Phenotypic Tuning of Offspring: Adaptive Responses to a Prenatal Environmental Challenge in Chickens
Open this publication in new window or tab >>Transgenerational Phenotypic Tuning of Offspring: Adaptive Responses to a Prenatal Environmental Challenge in Chickens
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2008 (English)Manuscript (preprint) (Other academic)
Abstract [en]

Stress may affect both the exposed individuals and the development of their offspring. We have previously shown that offspring of stressed domestic chickens can inherit the stressed-induced learning impairments of their parents and the associated modifications in brain gene expression. In this study we investigated possible adaptive aspects of such cross-generation transmissions. We hypothesized that stress would cause chickens to show a more conservative feeding strategy and to be more dominant, and that these adaptations would be transmitted to the offspring. Parents were raised in an unpredictable diurnal light rhythm (stress treatment) or in control conditions (12:12 h light:dark). In a foraging test, stressed birds pecked more at freely available than at hidden and more attractive food compared to birds from the control group. Female offspring of stressed birds, raised in control conditions without parental contact, showed a similar foraging behavior, differing from offspring of control birds. Furthermore, adult offspring of stressed birds performed more food pecks in a dominance test, showed a higher preference for high energy food, survived better, and were heavier than offspring of control parents. One possible explanation for the more dominant behavior of these birds might be increased androgen/estrogen effects from the yolk during their embryonic phase leading to increased anabolism and androgenic behavior. Using cDNA microarrays, we found that some of the differential brain gene expression caused by stress tended to be mirrored in the offspring, indicating transgenerational effects.  In particular, several immunoglobulin genes seemed to be affected similarly in both stressed parents and their offspring. Estradiol, but not corticoserone, testosterone, androstendion, or dihydrotestosterone, was significantly higher in egg yolk from stressed birds, suggesting a possible mechanism for these effects. Our findings suggest that stress may cause adaptive responses in feeding behavior, which may be transmitted to the offspring by means of epigenetic regulation of immune genes. This may in turn prepare the offspring for coping with an unpredictable environment.

59 p.
Stress, Prenatal stress, Adaptation, Animal behaviour, Gene expresssion, Microarray, Domestication, Chicken, Epigenetics, Transgenerational effects, Estradiol, Steroid hormones, Epigenetic inheritance, Maternal effects, Paternal effects
urn:nbn:se:liu:diva-15530 (URN)978-91-7393-753-5 (ISBN)
Available from: 2008-11-17 Created: 2008-11-14 Last updated: 2013-06-12Bibliographically approved

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