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Transgenerational effects of early experience on acute stress reactions in behaviour, steroid hormones and gene expression in the precocial chicken
Linköping University, Department of Physics, Chemistry and Biology, Zoology. Linköping University, The Institute of Technology.
Linköping University, Department of Physics, Chemistry and Biology, Zoology. Linköping University, The Institute of Technology.
Linköping University, Department of Physics, Chemistry and Biology, Zoology. Linköping University, The Institute of Technology.
Linköping University, Department of Physics, Chemistry and Biology, Zoology. Linköping University, The Institute of Technology.
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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.

Place, publisher, year, edition, pages
2012. Vol. 61, no 5, 711-718 p.
Keyword [en]
Early growth response, corticotropin releasing hormone receptor, postnatal stress, behaviour, epigenetics, transgenerational effects, steroid hormones, gene expression
National Category
Biological Sciences
Identifiers
URN: urn:nbn:se:liu:diva-70157DOI: 10.1016/j.yhbeh.2012.03.006ISI: 000304339800007OAI: oai:DiVA.org:liu-70157DiVA: diva2:436071
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
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. The Physiology of Chicken Domestication: Involvement of the HPA-axis and the Autonomic Nervous System
Open this publication in new window or tab >>The Physiology of Chicken Domestication: Involvement of the HPA-axis and the Autonomic Nervous System
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Alternative title[sv]
Fysiologin bakom domesticeringen av våra industrihöns : HPA-axeln och det autonoma nervsystemets effekter
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
Domestication, chickens, HPA-axis, autonomic nervous system, heart rate, allometry
National Category
Zoology
Identifiers
urn:nbn:se:liu:diva-117153 (URN)978-91-7519-091-4 (ISBN)
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

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Goerlich, Vivian C.Nätt, DanielElfwing, MagnusJensen, Per

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