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Domestication Effects on the Stress Response in Chickens: Genetics, Physiology, and Behaviour
Linköping University, Department of Physics, Chemistry and Biology, Biology. Linköping University, Faculty of Science & Engineering.
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Animal domestication, the process where animals become adapted to living in proximity to humans, is associated with the alteration of multiple traits, including decreased fearfulness and stress response. With an estimated population of 50 billion, the domesticated chicken is the most populous avian species in the world. Hundreds of chicken breeds have been developed for meat and egg production, hobby or research purposes. Multidirectional selection and the relaxation of natural selection in captivity have created immense phenotypic diversity amongst domesticates in a relatively short evolutionary time. The extensive phenotypic diversity, existence of the wild ancestor, and feasibility of intercrossing various breeds makes the chicken a suitable model animal for deciphering genetic determinants of complex traits such as stress response. We used chicken domestication as a model to gain insights about the mechanisms that regulate stress response in an avian species. We studied behavioural and physiological stress response in the ancestral Red Junglefowl and one of its domesticated progenies, White Leghorn. An advanced intercross between the aforementioned breeds was later used to map genetic loci underlying modification of stress response. The general pattern of the stress response in chickens was comparable with that reported in mammals, however we identified distinctive differences in the stress modulatory pathways in chickens. We showed that changes in the expression levels of several stress modulatory genes in the brain, the pituitary and the adrenal glands underlie the observed modified stress response in domesticated chickens. Using quantitative trait loci (QTL) mapping, several QTL underlying stress induced corticosterone, aldosterone and baseline dehydroepiandrosterone (DHEA) levels were detected. As a next step, we combined QTL mapping with gene expression (eQTL) mapping and narrowed two QTL down to the putative causal genes, SERPINA10 and PDE1C. Both of these genes were differentially expressed in the adrenal glands of White Leghorn and the Red Junglefowl, had overlapping eQTL with hormonal QTL, and their expression levels in the adrenal glands were correlated with plasma levels of corticosterone and al-dosterone. These two genes thus serve as strong candidates for further functional investigation concerning modification of the stress response during domestication. This dissertation increase the knowledge about genetics and physiology of the stress response in an avian species and its modification during domestication. Our findings expand the basic knowledge about the stress response in chicken, which can potentially be used to improve welfare through appropriate genetic selection.

Place, publisher, year, edition, pages
Linköping: Linköping University Electronic Press, 2017. , p. 31
Series
Linköping Studies in Science and Technology. Dissertations, ISSN 0345-7524 ; 1842
Keywords [en]
Animal domestication, stress response, gene expression, QTL, eQTL
National Category
Genetics Evolutionary Biology Zoology Developmental Biology Genetics and Breeding
Identifiers
URN: urn:nbn:se:liu:diva-137350ISBN: 9789176855461 (print)OAI: oai:DiVA.org:liu-137350DiVA, id: diva2:1095500
Public defence
2017-06-09, Plank, Fysikhuset, Campus Valla, Linköping, 09:00
Opponent
Supervisors
Note

DOI does not work: 10.3384/diss.diva-137350

Available from: 2017-05-15 Created: 2017-05-15 Last updated: 2018-02-22Bibliographically approved
List of papers
1. Domestication effects on behavioural and hormonal responses to acute stress in chickens
Open this publication in new window or tab >>Domestication effects on behavioural and hormonal responses to acute stress in chickens
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2014 (English)In: Physiology and Behavior, ISSN 0031-9384, E-ISSN 1873-507X, Vol. 133, p. 161-169Article in journal (Refereed) Published
Abstract [en]

Comparative studies have shown that alterations in physiology, morphology and behaviour have arisen due tothe domestication. A driving factor behind many of the changes could be a shift in stress responses,withmodifiedendocrine and behavioural profiles. In the present study we compared two breeds of chicken (Gallus gallus), thedomesticWhite Leghorn (WL) egg laying breed and its ancestor, the Red Junglefowl (RJF). Birds were exposed toan acute stress event, invoked by 3 or 10 min of physical restraint. Theywere then continuouslymonitored for theeffects on a wide range of behaviours during a 60 min recovery phase. Blood samples were collected from thechicken at baseline, and after 10 and 60 min following a similar restraint stress, and the samples wereanalyzed for nine endogenous steroids of the HPA and HPG axes. Concentration of the steroids was determinedusing validated liquid chromatography tandem mass spectrometry methods. In RJF, an immediate behaviouralresponse was observed after release from restraint in several behaviours, with a relatively fast return to baselinewithin 1 h. In WL, somebehaviourswere affected for a longer period of time, and others not at all. Concentrationsof corticosterone increasedmore in RJF, but returned faster to baseline compared toWL. A range of baseline levelsfor HPG-related steroids differed between the breeds, and they were generally more affected by the stress in WLthan in RJF. In conclusion, RJF reacted stronger both behaviourally and physiologically to the restraint stress, butalso recovered faster. This would appear to be adaptive under natural conditions, whereas the stress recovery ofdomesticated birds has been altered by domestication and breeding for increased reproductive output.

Place, publisher, year, edition, pages
Elsevier, 2014
Keywords
Corticosterone Recovery Restraint White Leghorn Red Junglefowl
National Category
Biological Sciences
Identifiers
urn:nbn:se:liu:diva-107167 (URN)10.1016/j.physbeh.2014.05.024 (DOI)000340315100022 ()
Note

Funders: Swedish Research Council (VR) [621-2011-4731]; Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS) [221-2011-1088]; ERC (project Genewell) [322206]; Swedish Centre of Excellence in Animal Welfare; ARUP Institute for Clinical and Experimental Pathology

Available from: 2014-06-09 Created: 2014-06-09 Last updated: 2017-12-05
2. Domestication Effects on Stress Induced Steroid Secretion and Adrenal Gene Expression in Chickens
Open this publication in new window or tab >>Domestication Effects on Stress Induced Steroid Secretion and Adrenal Gene Expression in Chickens
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2015 (English)In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 5, p. 1-10, article id 15345Article in journal (Refereed) Published
Abstract [en]

Understanding the genetic basis of phenotypic diversity is a challenge in contemporary biology. Domestication provides a model for unravelling aspects of the genetic basis of stress sensitivity. The ancestral Red Junglefowl (RJF) exhibits greater fear-related behaviour and a more pronounced HPA-axis reactivity than its domesticated counterpart, the White Leghorn (WL). By comparing hormones (plasmatic) and adrenal global gene transcription profiles between WL and RJF in response to an acute stress event, we investigated the molecular basis for the altered physiological stress responsiveness in domesticated chickens. Basal levels of pregnenolone and dehydroepiandrosterone as well as corticosterone response were lower in WL. Microarray analysis of gene expression in adrenal glands showed a significant breed effect in a large number of transcripts with over-representation of genes in the channel activity pathway. The expression of the best-known steroidogenesis genes were similar across the breeds used. Transcription levels of acute stress response genes such as StAR, CH25 and POMC were upregulated in response to acute stress. Dampened HPA reactivity in domesticated chickens was associated with changes in the expression of several genes that presents potentially minor regulatory effects rather than by means of change in expression of critical steroidogenic genes in the adrenal.

Place, publisher, year, edition, pages
Nature Publishing Group, 2015
National Category
Bioinformatics and Systems Biology
Identifiers
urn:nbn:se:liu:diva-122305 (URN)10.1038/srep15345 (DOI)000362885300001 ()26471470 (PubMedID)
Note

Funding agencies: Swedish Research Council (VR) [621-2011-4731]; Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS) [221-2011-1088]; SRC [621-2011-5523]; ERC [322206]; Swedish Centre of Excellence in Animal Welfare

Available from: 2015-10-28 Created: 2015-10-28 Last updated: 2017-12-01
3. Genetic and Targeted eQTL Mapping Reveals Strong Candidate Genes Modulating the Stress Response During Chicken Domestication.
Open this publication in new window or tab >>Genetic and Targeted eQTL Mapping Reveals Strong Candidate Genes Modulating the Stress Response During Chicken Domestication.
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2017 (English)In: G3: Genes, Genomes, Genetics, ISSN 2160-1836, E-ISSN 2160-1836, Vol. 7, no 2Article in journal (Refereed) Published
Abstract [en]

The stress response has been largely modified in all domesticated animals, offering a strong tool for genetic mapping. In chickens, ancestral Red Junglefowl react stronger both in terms of physiology and behavior to a brief restraint stress than domesticated White Leghorn, demonstrating modified functions of the hypothalamic-pituitary-adrenal (HPA) axis. We mapped quantitative trait loci (QTL) underlying variations in stress-induced hormone levels using 232 birds from the 12th generation of an advanced intercross between White Leghorn and Red Junglefowl, genotyped for 739 genetic markers. Plasma levels of corticosterone, dehydroepiandrosterone (DHEA), and pregnenolone (PREG) were measured using LC-MS/MS in all genotyped birds. Transcription levels of the candidate genes were measured in the adrenal glands or hypothalamus of 88 out of the 232 birds used for hormone assessment. Genes were targeted for expression analysis when they were located in a hormone QTL region and were differentially expressed in the pure breed birds. One genome-wide significant QTL on chromosome 5 and two suggestive QTL together explained 20% of the variance in corticosterone response. Two significant QTL for aldosterone on chromosome 2 and 5 (explaining 19% of the variance), and one QTL for DHEA on chromosome 4 (explaining 5% of the variance), were detected. Orthologous DNA regions to the significant corticosterone QTL have been previously associated with the physiological stress response in other species but, to our knowledge, the underlying gene(s) have not been identified. SERPINA10 had an expression QTL (eQTL) colocalized with the corticosterone QTL on chromosome 5 and PDE1C had an eQTL colocalized with the aldosterone QTL on chromosome 2. Furthermore, in both cases, the expression levels of the genes were correlated with the plasma levels of the hormones. Hence, both these genes are strong putative candidates for the domestication-induced modifications of the stress response in chickens. Improved understanding of the genes associated with HPA-axis reactivity can provide insights into the pathways and mechanisms causing stress-related pathologies.

Place, publisher, year, edition, pages
The Genetics Society, 2017
Keywords
animal, domestication, quantitative trait, genes, corticosterone, aldosterone
National Category
Biological Sciences
Identifiers
urn:nbn:se:liu:diva-134649 (URN)10.1534/g3.116.037721 (DOI)000394357100015 ()27974436 (PubMedID)
Note

Funding agencies: Swedish Research Council (SRC) (Vetenskapsradet) [621-2011-4731]; Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (Forskningsradet for Miljo, Areella Naringar och Samhallsbyggande) [221-2011-1088]; European Research Co

Available from: 2017-02-21 Created: 2017-02-21 Last updated: 2017-11-29
4. QTL mapping of stress related gene expression in a cross between domesticated chickens and ancestral red junglefowl.
Open this publication in new window or tab >>QTL mapping of stress related gene expression in a cross between domesticated chickens and ancestral red junglefowl.
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2017 (English)In: Molecular and Cellular Endocrinology, ISSN 0303-7207, E-ISSN 1872-8057, Vol. 446, p. 52-58, article id S0303-7207(17)30090-4Article in journal (Refereed) Published
Abstract [en]

Domestication of animals is associated with numerous alterations in physiology, morphology, and behavior. Lower reactivity of the hypothalamic-pituitary-adrenal (HPA) axis and reduced fearfulness is seen in most studied domesticates, including chickens. Previously we have shown that the physiological stress response as well as expression levels of hundreds of genes in the hypothalamus and adrenal glands are different between domesticated White Leghorn and the progenitor of modern chickens, the Red Junglefowl. To map genetic loci associated with the transcription levels of genes involved in the physiological stress response, we conducted an eQTL analysis in the F12 generation of an inter-cross between White Leghorn and Red Junglefowl. We selected genes for further studies based on their known function in the regulation of the HPA axis or sympathoadrenal (SA) system, and measured their expression levels in the hypothalamus and the adrenal glands after a brief stress exposure (physical restraint). The expression values were treated as quantitative traits for the eQTL mapping. The plasma levels of corticosterone were also assessed. We analyzed the correlation between gene expression and corticosterone levels and mapped eQTL and their potential effects on corticosterone levels. The effects on gene transcription of a previously found QTL for corticosterone response were also investigated. The expression levels of the glucocorticoid receptor (GR) in the hypothalamus and several genes in the adrenal glands were correlated with the post-stress levels of corticosterone in plasma. We found several cis- and trans-acting eQTL for stress-related genes in both hypothalamus and adrenal. In the hypothalamus, one eQTL for c-FOS and one QTL for expression of GR were found. In the adrenal tissue, we identified eQTL for the genes NR0B1, RGS4, DBH, MAOA, GRIN1, GABRB2, GABRB3, and HSF1. None of the found eQTL were significant predictors of corticosterone levels. The previously found QTL for corticosterone was associated with GR expression in hypothalamus. Our data suggests that domestication related modification in the stress response is driven by changes in the transcription levels of several modulators of the HPA and SA systems in hypothalamus and adrenal glands and not by changes in the expression of the steroidogenic genes. The presence of eQTL for GR in hypothalamus combined with the negative correlation between GR expression and corticosterone response suggests GR as a candidate for further functional studies regarding modification of stress response during chicken domestication.

Keywords
Animal domestication, HPA axis, QTL, Stress response, eQTL
National Category
Biological Sciences
Identifiers
urn:nbn:se:liu:diva-136027 (URN)10.1016/j.mce.2017.02.010 (DOI)000399509600006 ()28189567 (PubMedID)
Note

Funding agencies: Swedish Research Council (VR) [621-2011-4731]; Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS) [221-2011-1088]; ERC [Genewell 322206]; SRC grant [VR 621-2011-4423, 2015-4870]; Swedish Centre of Excellence in A

Available from: 2017-03-27 Created: 2017-03-27 Last updated: 2017-05-18

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Fallahshahroudi, Amir

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