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Heritable epigenetic responses to environmental challenges: Effects on behaviour, gene expression and DNA-methylation in the chicken
Linköping University, Department of Physics, Chemistry and Biology, Zoology . Linköping University, The Institute of Technology.
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: urn:nbn:se:liu:diva-70155ISBN: 978-91-7393-123-6 (print)OAI: oai:DiVA.org:liu-70155DiVA: diva2:436067
Public defence
2011-09-16, Planck, Fysikhuset, Campus Valla, Linköpings universitet, Linköping, 09:15 (English)
Opponent
Supervisors
Available from: 2011-08-22 Created: 2011-08-22 Last updated: 2011-08-29Bibliographically 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.

Keyword
Stress, Prenatal stress, Animal behaviour, Gene expresssion, Domestication, Chicken, Red junglefowl, White Leghorn, Epigenetics, Transgenerational effects, Epigenetic inheritance, Maternal effects, Paternal effects
Identifiers
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. Inheritance of Acquired Behaviour Adaptions and Brain Gene Expression in Chickens
Open this publication in new window or tab >>Inheritance of Acquired Behaviour Adaptions and Brain Gene Expression in Chickens
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2009 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 4, no 7, e6405- p.Article, review/survey (Other academic) Published
Abstract [en]

Background: Environmental challenges may affect both the exposed individuals and their offspring. We investigated possible adaptive aspects of such cross-generation transmissions, and hypothesized that chronic unpredictable food access 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.

Methodology/Principal Findings: Parents were raised in an unpredictable (UL) or in predictable diurnal light rhythm (PL, 12:12 h light:dark). In a foraging test, UL birds pecked more at freely available, rather than at hidden and more attractive food, compared to birds from the PL group. Female offspring of UL birds, raised in predictable light conditions without parental contact, showed a similar foraging behavior, differing from offspring of PL birds. Furthermore, adult offspring of UL 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 PL parents. Using cDNA microarrays, we found that the differential brain gene expression caused by the challenge was mirrored in the offspring. In particular, several immunoglobulin genes seemed to be affected similarly in both UL parents and their offspring. Estradiol levels were significantly higher in egg yolk from UL birds, suggesting one possible mechanism for these effects.

Conclusions/Significance: Our findings suggest that unpredictable food access caused seemingly adaptive responses in feeding behavior, which may have been transmitted to the offspring by means of epigenetic mechanisms, including regulation of immune genes. This may have prepared the offspring for coping with an unpredictable environment.

Citation: Nätt D, Lindqvist N, Stranneheim H, Lundeberg J, Torjesen PA, et al. (2009) Inheritance of Acquired Behaviour Adaptations and Brain Gene Expression in Chickens. PLoS ONE 4(7): e6405. doi:10.1371/journal.pone.0006405

Editor: Tom Pizzari, University of Oxford, United Kingdom

Received: March 26, 2009; Accepted: June 30, 2009; Published: July 28, 2009

Copyright: © 2009 Nätt et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: This project was funded by the Swedish Research Council (VR; www.vr.se; grant nrs 50280101 and 50280102) and the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (Formas; www.formas.se; grant no 221-2005-270). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the mauscript.

Competing interests: The authors have declared that no competing interests exist.

 

National Category
Biological Sciences
Identifiers
urn:nbn:se:liu:diva-19948 (URN)10.1371/journal.pone.0006405 (DOI)
Note
Original Publication: Daniel Nätt, Niclas Lindqvist, Henrik Stranneheim, Joakim Lundeberg, Peter A. Torjesen and Per Jensen, Inheritance of Acquired Behaviour Adaptions and Brain Gene Expression in Chickens, 2009, PLoS ONE, (4), 7, e6405. http://dx.doi.org/10.1371/journal.pone.0006405 Copyright: Authors Available from: 2009-08-25 Created: 2009-08-19 Last updated: 2017-12-13Bibliographically approved
3. Transgenerational effects of early experience on acute stress reactions in behaviour, steroid hormones and gene expression in the precocial chicken
Open this publication in new window or tab >>Transgenerational effects of early experience on acute stress reactions in behaviour, steroid hormones and gene expression in the precocial chicken
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2012 (English)In: Hormones and Behavior, ISSN 0018-506X, E-ISSN 1095-6867, Vol. 61, no 5, 711-718 p.Article in journal (Refereed) Published
Abstract [en]

Stress during early life can profoundly influence an individual’s phenotype. Effects can manifest in the short-term as well as later in life and even in subsequent generations. Transgenerational effects of stress are potentially mediated via modulation of the hypothalamic-pituitary-adrenal axis (HPA) as well as epigenetic mechanisms causing heritable changes in gene expression. To investigate these pathways we subjected domestic chicks (Gallus gallus) to intermittent social isolation, food restriction, and temperature stress for the first three weeks of life. The early life stress resulted in a dampened corticosterone response to restraint stress in the parents and male offspring. Stress-specific genes, such as early growth response 1 (EGR1) and corticotropin releasing hormone receptor 1 (CRHR1), were upregulated when chicks were tested in the context of restraint stress, but not under baseline conditions. Treatment differences in gene expression were also correlated across generations which indicate transgenerational epigenetic inheritance, possibly mediated by differences in maternal yolk estradiol and testosterone. In an associative learning test early stressed birds made more correct choices suggesting a higher coping ability in stressful situations. This study is the first to show transgenerational effects of early life stress in a precocial species by combining behavioural, endocrinological, and transcriptomic measurements.

Keyword
Early growth response, corticotropin releasing hormone receptor, postnatal stress, behaviour, epigenetics, transgenerational effects, steroid hormones, gene expression
National Category
Biological Sciences
Identifiers
urn:nbn:se:liu:diva-70157 (URN)10.1016/j.yhbeh.2012.03.006 (DOI)000304339800007 ()
Note
funding agencies|Swedish Research Council||Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning||Available from: 2011-08-22 Created: 2011-08-22 Last updated: 2017-12-08
4. Heritable genome-wide variation of gene expression and promoter methylation between wild and domesticated chickens
Open this publication in new window or tab >>Heritable genome-wide variation of gene expression and promoter methylation between wild and domesticated chickens
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2012 (English)In: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 13, no 59Article in journal (Refereed) Published
Abstract [en]

Variations in gene expression, mediated by epigenetic mechanisms, may cause broad phenotypic effects in animals. However, it has been debated to what extent expression variation and epigenetic modifications, such as patterns of DNA methylation, are transferred across generations, and therefore it is uncertain what role epigenetic variation may play in adaptation. Here, we show that in Red Junglefowl, ancestor of domestic chickens, gene expression and methylation profiles in thalamus/hypothalamus differ substantially from that of a domesticated egg laying breed. Expression as well as methylation differences are largely maintained in the offspring, demonstrating reliable inheritance of epigenetic variation. Some of the inherited methylation differences are tissue-specific, and the differential methylation at specific loci are little changed after eight generations of intercrossing between Red Junglefowl and domesticated laying hens. There was an over-representation of differentially expressed and methylated genes in selective sweep regions associated with chicken domestication. Hence, our results show that epigenetic variation is inherited in chickens, and we suggest that selection of favourable epigenomes, either by selection of genotypes affecting epigenetic states, or by selection of methylation states which are inherited independently of sequence differences, may have been an important aspect of chicken domestication.

Place, publisher, year, edition, pages
BioMed Central, 2012
Keyword
Domestication, gene expression, tiling array, behaviour, methylation
National Category
Biological Sciences
Identifiers
urn:nbn:se:liu:diva-70159 (URN)10.1186/1471-2164-13-59 (DOI)000301440800001 ()
Note

funding agencies|Swedish Research Council| 2008-14496-59340-36 |Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning| 221 2007 838 |

Available from: 2011-08-22 Created: 2011-08-22 Last updated: 2017-12-08Bibliographically approved

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