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Transmission of Stress-Induced Learning Impairment and Associated Brain Gene Expression from Parents to Offspring in Chickens
Linköping University, Department of Physics, Chemistry and Biology, Zoology . Linköping University, The Institute of Technology.
Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Ås, Norway.
Linköping University, Department of Physics, Chemistry and Biology, Zoology . Linköping University, The Institute of Technology.
Linköping University, Department of Physics, Chemistry and Biology. Linköping University, The Institute of Technology.
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2007 (English)In: PLoS ONE, ISSN 1932-6203, E-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.

Place, publisher, year, edition, pages
2007. Vol. 2, no 4, e364- p.
Keyword [en]
Stress, Prenatal stress, Animal behaviour, Gene expresssion, Domestication, Chicken, Red junglefowl, White Leghorn, Epigenetics, Transgenerational effects, Epigenetic inheritance, Maternal effects, Paternal effects
Identifiers
URN: urn:nbn:se:liu:diva-15529DOI: 10.1371/journal.pone.0000364OAI: oai:DiVA.org:liu-15529DiVA: diva2:117493
Available from: 2008-11-17 Created: 2008-11-14 Last updated: 2017-12-14Bibliographically approved
In thesis
1. Stress and the Offspring: Adaptive Transgenerational Effects of Unpredictability on Behaviour and Gene Expression in Chickens (Gallus gallus)
Open this publication in new window or tab >>Stress and the Offspring: Adaptive Transgenerational Effects of Unpredictability on Behaviour and Gene Expression in Chickens (Gallus gallus)
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.
Series
Linköping Studies in Science and Technology. Thesis, ISSN 0280-7971 ; 1385
Keyword
Chicken, Red junglefowl, Domestication, Epigenetics, Transgenerational, Inheritance, Gene expression, Microarray, qRT-PCR, Immunogenetics, Immunoglobulin, Estradiol, Steriod hormones, Prenatal stress, Epigenetic inheritance, Adaptation, Stress, Behaviour
Identifiers
urn:nbn:se:liu:diva-15518 (URN)978-91-7393-753-5 (ISBN)
Presentation
2008-12-04, Schrödinger E324, Linköpings Universitet, Department of Physics, Chemistry and Biology, 58183 Linköping, Sweden , Linköping, 13:00 (English)
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Supervisors
Available from: 2008-11-14 Created: 2008-11-13 Last updated: 2009-05-11Bibliographically approved
2. Heritable epigenetic responses to environmental challenges: Effects on behaviour, gene expression and DNA-methylation in the chicken
Open this publication in new window or tab >>Heritable epigenetic responses to environmental challenges: Effects on behaviour, gene expression and DNA-methylation in the chicken
2011 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Phenotypic variation within populations is a crucial factor in evolution and is mainly thought to be driven by heritable changes in the base sequence of DNA. Among our domesticated species we find some of the most variable species on earth today. This variety of breeds has appeared during a relatively short evolutionary time, and so far genetic studies have been unable to explain but a small portion of this variation, which indicates more novel mechanisms of inheritance and phenotypic plasticity. The aim of this study was therefore to investigate some of these alternative routes in the chicken, especially focusing on transgenerational effects of environmental challenges on behaviour and gene expression in relation to domestication. In two experiments a chronically unpredictable environment induced phenotypic changes in the parents that were mirrored in the unexposed offspring raised without parental contact. This transmission was especially clear in domesticated birds. A third experiment showed that repeated stress events very early in life could change the developmental program making the birds more resistant to stress later in life. Here, the phenotypic changes were also mirrored in the unexposed offspring and associated with inheritance of gene expression. Epigenetic factors, such as DNA-methylation, could play an important role in the mechanism of these transgenerational effects. A fourth experiment showed that wild types and domesticated chickens differed substantially in their patterns of DNA-methylation, where the domesticated breed had increased amount of promoter DNA-methylation. In line with the previous experiments, this breed also showed increased transmission of methylation marks to their  offspring. Conclusively, parental exposure of environmental challenges that introduce changes in behaviour, physiology and gene expression can under both chronic and temporal conditions be heritably programmed in the parent and transmitted to the unexposed offspring. Since heritable epigenetic variation between wild type and domesticated chickens is stable and numerous, it is possible that selection for favourable epigenomes could add another level to the evolutionary processes and therefore might explain some of the rapid changes in the history of the domesticated chicken. 

Place, publisher, year, edition, pages
Linköping: Linköping University Electronic Press, 2011. 53 p.
Series
Linköping Studies in Science and Technology. Dissertations, ISSN 0345-7524 ; 1383
National Category
Natural Sciences
Identifiers
urn:nbn:se:liu:diva-70155 (URN)978-91-7393-123-6 (ISBN)
Public defence
2011-09-16, Planck, Fysikhuset, Campus Valla, Linköpings universitet, Linköping, 09:15 (English)
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Supervisors
Available from: 2011-08-22 Created: 2011-08-22 Last updated: 2011-08-29Bibliographically approved

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Lindqvist, ChristinaNätt, DanielBaranowska, IzabellaJensen, Per

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