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The Physiology of Chicken Domestication: Involvement of the HPA-axis and the Autonomic Nervous System
Linköping University, Department of Physics, Chemistry and Biology, Biology. Linköping University, The Institute of Technology. (AVIAN)
2015 (English)Doctoral thesis, comprehensive summary (Other academic)Alternative title
Fysiologin bakom domesticeringen av våra industrihöns : HPA-axeln och det autonoma nervsystemets effekter (Swedish)
Abstract [sv]

Domesticering är en urvalsprocess för önskvärda egenskaper hos djur som över tid förändrar deras utseende, beteende och genetik. Några exempel av djur som genomgått denna riktade avel är vargen, mufflon, uroxen, vildsvinet och den röda djungelhönan som vi idag känner som hunden, fåret, kon, grisen och slaktkycklingen.

Några gemensamma egenskaper hos domesticerade djur är minskad rädsla för människor, och att de troligen har en högre stresstolerans jämfört med sina vilda förfäder. Det finns två huvudsakliga fysiologiska mekanismer som styr dessa responser, en hormonell och en nervös. Nervsystemet är i sin tur uppdelat i sympatiska och parasympatiska nervsystemet vilka har motsatta roller för kroppens funktioner. Under stress ger det sympatiska den så kallade ”Fight-and-flight”-responsen, och det parasympatiska aktiveras under vila och kallas ”rest-and-digest”-systemet. Det verkar troligt att domesticeringen agerat på dessa system för att minska rädsla och stress hos våra tamdjur.

Den här avhandlingen studerar stressresponser hos höns. Dessa används i stor skala inom livsmedelsindustrin, slaktkycklingen för köttproduktion samt värphöns för äggproduktion. De har avlats hårt för snabb tillväxt och hög äggproduktion. En slaktkyckling ökar sin vikt till 50 gånger kläckvikten på sex veckor! Det sympatiska nervsystemet, samt stresshormoner, agerar för nedbrytande och energifrisläppande mekanismer, och det parasympatiska samt låg stress verkar för uppbyggande och energisparande mekanismer. Därför bör avel på låg stress och låg sympatisk aktivitet vara fördelaktigt för hög tillväxt.

Experimenten i avhandlingen undersöker utvecklingen och mognaden av det autonoma nervsystemet hos kycklingar, domesticeringseffekter samt om stress tidigt i livet påverkar höns som vuxna. Vi fann att kycklingfoster redan vid 75 % av fosterutvecklingen har en funktionell parasympatisk stimulering på hjärtat och att dess inverkan ökar närmare kläckningen. Efter kläckning styrs hjärtat i huvudsak av det sympatiska nervsystemet och först vid ca 5 veckors ålder tycks systemet närma sig mognad. Vi hittade också domesticeringseffekter på hjärtfrekvensen, som styrs av det autonoma nervsystemet, hos framför allt slaktkycklingar som har en lägre hjärtfrekvens jämfört med djungelhönan.

Tidigare studier har indikerat att en gen som uttrycker ett protein i hjärnan, i sympatiska nervsystemet samt i binjurarna har varit viktig för aveln på våra tamhöns. Denna gen, ADRA2C, styr till exempel frisläppningen av stresshormon från binjurarna. Vi undersökte eventuella domesticeringseffekter på denna gen med avseende på genuttryck, proteinmängd, beteenden, tillväxt samt äggproduktion, men trots att starka indikationer på att genen borde ha viktiga effekter, hittade vi inget stöd för att det.

Det är inte enbart domesticering som kan ha inverkan på stress. Erfarenheter tidigt i livet kan förändra individens välmående som vuxen och även ha effekter på dess avkomma. Vi undersökte dessa aspekter hos höns som avlats för äggläggning genom att stressa dem under de första veckorna efter kläckning och följde dem till vuxen ålder. Fåglarna uppvisade livslång påverkan av sina erfarenheter och framför allt hanar var särskilt känsliga och fick långsiktiga förändringar i beteendet, försenad hormonfrisättning vid puberteten och förändrad genuttrycksprofil i hypotalamus. Dessa modifieringar kan vara ett resultat av att aveln riktat sig i huvudsak mot honor för deras äggläggningsförmåga, och att hanar därmed ej blivit lika motståndskraftiga mot stress tidigt i livet. Även hanar i avkomman påverkades av föräldrarnas tidiga erfarenheter. De hade förändrat beteende, ändrad hormonell stressrespons och förändrat genuttryck.

Sammantaget visar resultaten hur nervsystemet utvecklas hos höns, samt att nervsystemet förändrats av den moderna aveln. Vidare kunde vi visa att stress tidigt i livet hos höns kan få långsiktiga effekter som involverar stressresponsen vilket kan få konsekvenser för djurets välfärd.

Abstract [en]

Domestication, the rapid man-driven evolution propelled by heavy selection for desirable traits, has changed a variety of species including the wolf, mouflon, auroch, wild boar and Red Junglefowl dramatically. Despite the polyphyletic origin of these species, they all demonstrate, after years of selection, features of surprising similarity that have been coined the domestic phenotype. The domesticated versions of these species are now commonly known as the dog, sheep, cattle, pig and broiler chicken.

A common feature among domesticated animals is a reduced fearfulness towards humans, and plausibly higher stress tolerance and reduced stress response compared to their wild ancestors. The major physiological machinery controlling these behavioral modifications is the hypothalamic-pituitary-adrenal axis (HPA-axis) and the autonomic nervous system. The fight-and-flight response is mostly regulated by the sympathetic nervous system, both by increased adrenergic tone and by secretion of epinephrine from the adrenal medulla. These pathways are clear targets for domestication to reduce the stress response and fearfulness.

In this thesis, the development and maturation of the autonomic nervous system, domestication effects in regard to stress, and developmental programming of early postnatal stress in chickens have been investigated. During development, chicken fetuses already had a functional cardiac cholinergic tone at 75% of development, and it progressively increased to hatch. Postnatally, heart rate was predominantly under adrenergic control, and at five weeks of age heart rate appears to reach maturity. Furthermore, we found a specific domestication effect in broiler chickens, demonstrated by a reduced cardiac frequency.

Previous studies scanning for target genes explaining domestication in multiple chicken strains, in comparison to the Red Junglefowl, suggested an alteration in the gene coding for a receptor controlling epinephrine release from the adrenal medulla. This gene, the α-adrenergic receptor 2C (ADRA2C), was investigated with regard to gene expression, receptor density, behavioral effects, growth and fecundity, but no differences were found. We failed to find any domestication effects of ADRA2C and we conclude that despite the promising evidence from previous findings, this gene is not important in domestication.

Stressful events during early life can cause long term effects and even affect the next generation. We wanted to investigate if HyLine chickens selected for egg production where susceptible to stressful events early in life, and monitor these individuals to adulthood. We also investigated the offspring of these birds to determine whether early-stressed parents could change the phenotype in their offspring by epigenetic effects. We found that the parental generation was indeed affected by early stress, and males in particular were susceptible to long term behavioral modification, delayed puberty-related increase in testosterone and alteration in hypothalamic gene expression profiles. These modifications might be a result of modern selection on production-related traits in females, but not males. The offspring males were also altered with respect to behavioral, endocrinological, and transcriptomic measurements, and this study was the first to demonstrate transgenerational effects in a precocial species.

Place, publisher, year, edition, pages
Linköping: Linköping University Electronic Press, 2015. , 39 p.
Series
Linköping Studies in Science and Technology. Dissertations, ISSN 0345-7524 ; 1651
Keyword [en]
Domestication, chickens, HPA-axis, autonomic nervous system, heart rate, allometry
National Category
Zoology
Identifiers
URN: urn:nbn:se:liu:diva-117153ISBN: 978-91-7519-091-4 (print)OAI: oai:DiVA.org:liu-117153DiVA: diva2:806284
Public defence
2015-06-05, Planck, Fysikhuset, Campus Valla, Linköping, 10:00 (English)
Opponent
Supervisors
Available from: 2015-04-20 Created: 2015-04-20 Last updated: 2015-04-27Bibliographically approved
List of papers
1. Fetal development of baroreflex sensitivity: The chicken embryo as a case model
Open this publication in new window or tab >>Fetal development of baroreflex sensitivity: The chicken embryo as a case model
2011 (English)In: Respiratory Physiology & Neurobiology, ISSN 1569-9048, E-ISSN 1878-1519, Vol. 178, no 1, 75-83 p.Article, review/survey (Refereed) Published
Abstract [en]

The baroreflex is the main short term compensatory mechanism to buffer blood pressure changes and maintain circulatory homeostasis. Its ontogeny and importance during prenatal life is not fully understood so we used broiler chickens to investigate the maturation of the baroreflex in late incubation using a novel method that measured changes in heart rate during spontaneous fluctuations in blood pressure. Our results suggest that a baroreflex is already functional at d17 with no indication of further maturation in terms of sensitivity (gain at 17 d was 52.9 ± 8.3 and at 20 d 69.5 ± 16.2 ms kPa−1). The physiological relevance of these values is shown using data surrogation methods. Although the results contrast with the progressive baroreflex maturation indicated by the pharmacological method, we sustain that both methods provide information on baroreflex regulation. While the spontaneous method evaluates truly physiological (but small) pressure changes, the pharmacological method provides a more consistent and repetitive challenge for the reflex that requires a different recruitment of baroreflex effectors.

Place, publisher, year, edition, pages
Elsevier B.V., 2011
Keyword
Baroreflex sensitivity, Spontaneous baroreflex, Cardiovascular development, Sodium nitroprusside
National Category
Natural Sciences
Identifiers
urn:nbn:se:liu:diva-70254 (URN)10.1016/j.resp.2011.03.031 (DOI)000294098200010 ()
Note
Funding Agency|Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS)||Swedish Research Council for Natural Sciences (VR-NT)||University of Linkoping||Wallenberg Foundation||Available from: 2011-08-29 Created: 2011-08-29 Last updated: 2017-12-08
2. The maturation of heart rate control in the Red Junglefowl (Gallus gallus)
Open this publication in new window or tab >>The maturation of heart rate control in the Red Junglefowl (Gallus gallus)
2015 (English)Manuscript (preprint) (Other academic)
Abstract [en]

Fetal development of autonomic cardiac control has been thoroughly investigated in chickens, but the maturation of the autonomic nervous system after hatching has gained little attention. At hatch the heart is under a feeble nervous control and there are indications suggesting a rapid maturation process during the first two weeks of postnatal life. We aimed to characterize the maturation by measuring heart rate at baseline and stressful conditions during the first 5 weeks of life in the Red Junglefowl and using autonomic antagonists to quantify the contribution of sympathetic and parasympathetic activity. We also compared the Red Junglefowl to the domestic broiler chickens at hatch to investigate the impact of domestication processes on heart rate regulation.

During the first two postnatal weeks, baseline and stress heart rate progressively increased. After two weeks baseline heart rate decreased while heart rate during acute stress remained high. Adrenergic tone in Red Junglefowl increased as well early suggesting that the increase in heart rate was driven predominantly by adrenergic contributions. The adrenergic tone decreased by age after postnatal week one explaining the concomitant reduction in basal heart rate during this period. Broiler chickens possessed a strong cholinergic tone at hatch indicating that parasympathetic control has been favored perhaps due to heavy selection for somatic growth.

National Category
Biological Sciences
Identifiers
urn:nbn:se:liu:diva-117421 (URN)
Available from: 2015-04-27 Created: 2015-04-27 Last updated: 2015-04-27Bibliographically approved
3. Domestication Affected Heart Rate Regulation in Juvenile Chickens
Open this publication in new window or tab >>Domestication Affected Heart Rate Regulation in Juvenile Chickens
2015 (English)Manuscript (preprint) (Other academic)
Abstract [en]

The domestication process in chickens has involved strong selection for productive traits. There is a broad understanding of phenotypic differences between domestic breeds and their ancestor, the Red Junglefowl (RJF), on fear related behaviors, genetic architecture, physiology and productive traits. Some of these characters can potentially be explained by changes in the activity of the autonomic nervous system. To address these questions we measured heart rate as a proxy for autonomic activity in the Red Junglefowl and compared it with two domestic strains, a broiler (BRO) (meat production) and a White Leghorn strain (HY) (egg production) at two and six weeks of age. Autonomic tones were pharmacologically manipulated in broilers to assess heart rate regulation during maturation. To investigate the dynamics of  autonomic control animals were measured during baseline conditions and during acute stress.

At two weeks of age baseline heart rate was high in all strains (RJF: 541.2±18.3, HY: 506.8±38.8, BRO: 456.0±22.3) and progressively decreased with age (RJF: 491.3±10.9, HY: 386.8±25.1, BRO:_296.8±26.9). BRO had a lower heart rate compared to RJF and HY, and the differences could not be explained by allometry alone. There was a domestication effect in BRO but not HY, which were in general more similar to RJF. These findings suggest that positive selection for somatic growth has changed heart rate regulation in broilers. During acute stress heart rate did not decrease with age in the same way than baseline values, which means that there is an increased scope for raising heart rate above baseline with age. At least in broilers the increased heart rate scope is due to a recruitment in adrenergic control in absence of a patent cholinergic tone.

National Category
Biological Sciences
Identifiers
urn:nbn:se:liu:diva-117422 (URN)
Available from: 2015-04-27 Created: 2015-04-27 Last updated: 2015-04-27Bibliographically approved
4. The Strong Selective Sweep Candidate Gene ADRA2C Does Not Explain Domestication Related Changes In The Stress Response Of Chickens
Open this publication in new window or tab >>The Strong Selective Sweep Candidate Gene ADRA2C Does Not Explain Domestication Related Changes In The Stress Response Of Chickens
Show others...
2014 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 9, no 8, e103218- p.Article in journal (Refereed) Published
Abstract [en]

Analysis of selective sweeps to pinpoint causative genomic regions involved in chicken domestication has revealed a strongselective sweep on chromosome 4 in layer chickens. The autoregulatory a-adrenergic receptor 2C (ADRA2C) gene is theclosest to the selective sweep and was proposed as an important gene in the domestication of layer chickens. The ADRA2Cpromoter region was also hypermethylated in comparison to the non-selected ancestor of all domesticated chicken breeds,the Red Junglefowl, further supporting its relevance. In mice the receptor is involved in the fight-or-flight response as itmodulates epinephrine release from the adrenals. To investigate the involvement of ADRA2C in chicken domestication, wemeasured gene expression in the adrenals and radiolabeled receptor ligand in three brain regions comparing the domesticWhite Leghorn strain with the wild ancestor Red Junglefowl. In adrenals ADRA2C was twofold greater expressed than therelated receptor gene ADRA2A, indicating that ADRA2C is the predominant modulator of epinephrine release but no straindifferences were measured. In hypothalamus and amygdala, regions associated with the stress response, and in striatum,receptor binding pIC50 values ranged between 8.1–8.4, and the level was not influenced by the genotyped allele. Becausechicken strains differ in morphology, physiology and behavior, differences attributed to a single gene may be lost in thenoise caused by the heterogeneous genetic background. Therefore an F10 advanced intercross strain between WhiteLeghorn and Red Junglefowl was used to investigate effects of ADRA2C alleles on fear related behaviors and fecundity. Wedid not find compelling genotype effects in open field, tonic immobility, aerial predator, associative learning or fecundity.Therefore we conclude that ADRA2C is probably not involved in the domestication of the stress response in chicken, and thestrong selective sweep is probably caused by selection of some unknown genetic element in the vicinity of the gene.

Place, publisher, year, edition, pages
Public Library of Science, 2014
National Category
Biological Sciences
Identifiers
urn:nbn:se:liu:diva-109431 (URN)10.1371/journal.pone.0103218 (DOI)000341105100015 ()25111139 (PubMedID)
Available from: 2014-08-18 Created: 2014-08-18 Last updated: 2017-12-05
5. Early stress causes sex-specific, life-long changes in behaviour, levels of gonadal hormones, and gene expression in chickens
Open this publication in new window or tab >>Early stress causes sex-specific, life-long changes in behaviour, levels of gonadal hormones, and gene expression in chickens
Show others...
2015 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 10, no 5, e0125808Article in journal (Refereed) Published
Abstract [en]

Early stress can have long-lasting phenotypic effects. Previous research shows that male and female chickens differ in many behavioural aspects, and respond differently to chronic stress. The present experiment aimed to broadly characterize long-term sex differences in responses to brief events of stress experienced during the first weeks of life. Chicks from a commercial egg-laying hybrid were exposed to stress by inducing periods of social isolation during their first three weeks of life, followed by a broad behavioural, physiological and genomic characterization throughout life. Early stressed males, but not females, where more anxious in an open field-test, stayed shorter in tonic immobility and tended to have delayed sexual maturity, as shown by a tendency for lower levels of testosterone compared to controls. While early stressed females did not differ from non-stressed in fear and sexual maturation, they were more socially dominant than controls. The differential gene expression profile in hypothalamus was significantly correlated from 28 to 213 days of age in males, but not in females. In conclusion, early stress had a more pronounced long-term effect on male than on female chickens, as evidenced by behavioral, endocrine and genomic responses. This may either be attributed to inherent sex differences due to evolutionary causes, or possibly to different stress related selection pressures on the two sexes during commercial chicken breeding.

Place, publisher, year, edition, pages
Public Library of Science, 2015
National Category
Biological Sciences
Identifiers
urn:nbn:se:liu:diva-117423 (URN)10.1371/journal.pone.0125808 (DOI)000354916100036 ()
Available from: 2015-04-27 Created: 2015-04-27 Last updated: 2017-12-04Bibliographically approved
6. 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
Show others...
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

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