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Heritable genome-wide variation of gene expression and promoter methylation between wild and domesticated chickens
Linköping University, Department of Physics, Chemistry and Biology, Zoology. Linköping University, The Institute of Technology.
Department of Medical Biochemistry and Microbiology, Uppsala University, Sweden.
Linköping University, Department of Physics, Chemistry and Biology, Zoology. Linköping University, The Institute of Technology.ORCID iD: 0000-0003-2329-2635
Linköping University, Department of Physics, Chemistry and Biology, Zoology. Linköping University, The Institute of Technology.ORCID iD: 0000-0003-1262-4585
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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. Vol. 13, no 59
Keyword [en]
Domestication, gene expression, tiling array, behaviour, methylation
National Category
Biological Sciences
Identifiers
URN: urn:nbn:se:liu:diva-70159DOI: 10.1186/1471-2164-13-59ISI: 000301440800001OAI: oai:DiVA.org:liu-70159DiVA: diva2:436075
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
In thesis
1. 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)
Opponent
Supervisors
Available from: 2011-08-22 Created: 2011-08-22 Last updated: 2011-08-29Bibliographically approved
2. Chicken domestication: Effects of tameness on brain gene expression and DNA methylation
Open this publication in new window or tab >>Chicken domestication: Effects of tameness on brain gene expression and DNA methylation
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Domestication greatly increases phenotypic variation in a short time span, with selection for a single phenotype and a plethora of associated phenotypic changes as an outcome of the process. The domestication process influences the underlying genomic architecture of a species, and the success and speed of the process is likely influenced by it. The main aims of my thesis was to study how domestication affects the brain of chickens: specifically changes in morphology, gene expression, and DNA methylation. Differences in gene expression and DNA methylation between White Leghorn and Red Junglefowl chickens were mapped, and inheritance of these patterns were quantified, indicating a faithful transmission of breed-specific epigenetic markers. Selection on the behavioral trait fearfulness, generated high and low fearful lines of Red Junglefowl. Both the parental population and the fifth selected generation were used for the analyses in this thesis. One experiment studied morphological changes in the brain and other vital organs, and found that relative total brain size increased in high fearful birds, as a consequence of an increase in cerebral hemisphere size in high fearful birds and not in low fearful birds. Also, the relative heart, liver, spleen and testis size increased in high fearful birds, indicating correlated morphological changes with selection for fearfulness. Two additional experiments examined differential gene expression in the hypothalamus and the anterior cerebral hemisphere. The hypothalamus differed in expression of genes with reproductive and immunological functions, whilst the cerebral hemisphere differed in expression of genes related to social behaviors and neurological functions especially those upregulated in low fearful birds.  These results indicate the occurrence of tissue- and species-specific changes in gene expression as overlap with other domestication events were nearly nonexistent. A fourth experiment sought to associate the change in fear levels and gene expression differences with DNA methylation. Chromosomal regions with differential DNA methylation between high and low fearful birds were identified, and genes in these regions had annotated functions relevant to phenotypic differences between the selection lines. This thesis is the first to study the genetic alterations of domestication using the wild ancestor of an already domesticated species to repeat the domestication process selecting against fear of humans. The findings corroborate results from previous comparisons of wild and domestic animals, and further support the theory that rigorous selection for a behavioral trait can cause a cascade of genetic and epigenetic changes facilitating the domestication of a population.

Place, publisher, year, edition, pages
Linköping: Linköping University Electronic Press, 2016. 41 p.
Series
Linköping Studies in Science and Technology. Dissertations, ISSN 0345-7524 ; 1796
National Category
Genetics Evolutionary Biology Developmental Biology Medical Genetics Other Biological Topics
Identifiers
urn:nbn:se:liu:diva-132379 (URN)10.3384/diss.diva-132379 (DOI)9789176856697 (ISBN)
Public defence
2016-12-14, Planck, Fysikhuset, Campus Valla, Linköping, 09:15 (English)
Opponent
Supervisors
Available from: 2016-11-18 Created: 2016-11-04 Last updated: 2016-11-30Bibliographically approved

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