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Transmission of stress-induced learning impairment and associated brain gene expression from parents to offspring in chickens

Lindqvist, Christina; Janczak, Andrew M.; Nätt, Daniel; Baranowska Körberg, Izabella; Lindqvist, Niclas LU ; Wichman, Anette; Lundeberg, Joakim; Lindberg, Johan; Torjesen, Peter A and Jensen, Per (2007) In PLoS ONE 2(4).
Abstract

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 controt 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... (More)

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 controt 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. Conclusion/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.

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author
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published
in
PLoS ONE
volume
2
issue
4
publisher
Public Library of Science
external identifiers
  • scopus:35549009579
ISSN
1932-6203
DOI
10.1371/journal.pone.0000364
language
English
LU publication?
no
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c3c439df-b299-40d5-9a9a-95609ab4b750
date added to LUP
2017-06-02 15:14:31
date last changed
2017-11-05 05:18:04
@article{c3c439df-b299-40d5-9a9a-95609ab4b750,
  abstract     = {<p>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 controt 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. Conclusion/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.</p>},
  articleno    = {e364},
  author       = {Lindqvist, Christina and Janczak, Andrew M. and Nätt, Daniel and Baranowska Körberg, Izabella and Lindqvist, Niclas and Wichman, Anette and Lundeberg, Joakim and Lindberg, Johan and Torjesen, Peter A and Jensen, Per},
  issn         = {1932-6203},
  language     = {eng},
  month        = {04},
  number       = {4},
  publisher    = {Public Library of Science},
  series       = {PLoS ONE},
  title        = {Transmission of stress-induced learning impairment and associated brain gene expression from parents to offspring in chickens},
  url          = {http://dx.doi.org/10.1371/journal.pone.0000364},
  volume       = {2},
  year         = {2007},
}