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Early domestication?: Phenotypic alterations of Red Junglefowl selected for divergent fear of humans
Linköpings universitet, Institutionen för fysik, kemi och biologi, Biologi. Linköpings universitet, Tekniska fakulteten.
2016 (Engelska)Doktorsavhandling, sammanläggning (Övrigt vetenskapligt)
Abstract [en]

Domestication is the process through which animals adapt to conditions provided by humans. The domesticated phenotype differs from wild ancestors in a number of traits relating to physiology, morphology and behaviour. One of the most striking differences is the animals’ fear response towards humans, and reduced fear of humans is assumed to have been an early prerequisite for the success of domestication. The early alterations seen in the domesticated phenotype may be traits developed as a correlated selection response due to tameness rather than selected upon one by one.

This thesis summarizes a project where Red Junglefowl were selected for divergent fear of humans during six generations. In every generation, fear response to human was assessed in a standardized test and, according to fear score, the animals were bred for either high fear of humans (H) or low fear of humans (L). The animals were, above that of the standardized selection test, behaviourally phenotyped in different tests in each generation mainly focusing on fear, exploration and social behaviour. In addition to behaviour, the animals were phenotyped for body weight, egg weight, metabolism, feed intake, plumage condition, blood plasma corticosterone and peripheral serotonin. After culling, vital organs and brains were harvested and weighed.

In paper I, we demonstrated that the selection trait has a significant genetic heritability and is genetically correlated with other behavioural responses associated with fearfulness and exploration. In paper II, we concluded that animals from the L strain had better plumage condition, higher weight, laid larger eggs and also generated larger offspring. Furthermore, when tested in a social dominance test with a limited resource, they received less and performed more aggression regardless of whether the restricted source was edible or not. In paper III, we revealed that animals from the L strain had higher basal metabolic rate as chicks, gained more weight in relation to feed intake and were bolder in a Novel Object test. Furthermore, the L males had higher plasma levels of peripheral serotonin, but the corticosterone after a restraint stress test did not differ. In paper IV and V, we concluded the project by comparing brain and organ weights as well as behaviour of the parental generation (P0) with the fifth selected generation (S5). The absolute brain weight as well as the weight specific brain weight were larger in the animals selected on H than in the L-animals. The relative weight of telencephalon was significantly higher in H whereas relative weight of cerebellum was significantly lower. Heart, liver, spleen and testes were all relatively heavier in H animals than in L. Interestingly, the behaviours assessed in P0 and S5 seemed to be rather resilient to the selection with only small differences in S5.

To summarize, the selection on divergent tameness in Red Junglefowl has affected several phenotypic traits associated with the domesticated phenotype. The results of this project indicate that tameness in Red Junglefowl could be an underlying factor driving trait modifications towards the domesticated phenotype.

Abstract [sv]

Den här avhandlingen är ett resultat av ett projekt där vi avlat djur på tamhet för att undersöka egenskapens roll i den tidiga domesticeringen. De domesticerade djur som vi har i vår närhet har alla genomgått en process där de har anpassats för vår miljö. Det skulle kunna liknas vid en snabb evolution, där ett djurs utseende och beteende förändras under en relativt sett kort tid genom avel av människan. Domesticerade djur skiljer sig från sina vilda släktingar på många olika sätt, de kan vara både mindre och större är ursprunget, finnas i olika färgvariationer, ha ändrade kroppsproportioner och de skiljer sig även åt i tröskelvärden för beteende från de vilda djuren. Skillnaderna mellan domesticerade djur och ursprunget är förvånansvärt lika mellan djurarter och man brukar kalla detta för den domesticerade fenotypen.

I det här projektet ville vi se om den domesticerade fenotypen egentligen är en biprodukt som uppkommer om man avlar djur på tamhet, på så sätt skulle rädslan för människor vara en nyckelegenskap för domesticeringen. För att undersöka detta använde vi det röda djungelhönset (RJF) som alla domesticerade höns härstammar ifrån. I sex generationer avlades RJF som antingen hade hög eller låg rädsla för människor. Eftersom vi bara har ett avelskriterium kan vi dra slutsatsen att om dessa djur kommer att skilja sig åt på fler sätt så beror det på korrelerade selektionseffekter. Det vill säga, man avlar på en egenskap och andra egenskaper följer med.

I varje generation har vi utfört beteendetester på djuren som främst varit kopplade till rädsla, utforskande och sociala beteenden. Utöver beteendetesterna har vi undersökt djurens kroppsvikt, äggvikt, metabolism, födointag, fjäderdräkt och tagit blodprov för att mäta kortikosteron och serotonin. När djuren har avlivats har vi vägt hjärnan, hjärtat, levern, mjälten och testiklarna.

Efter sex generationer av selekterad avel hade hönsen i projektet förändrats på olika sätt. Först och främst konstaterade vi att rädslan för människa är möjlig att avla på då den har en signifikant genetisk arvbarhet. De djuren som har en låg rädsla för människor har blivit större, socialt dominanta, lägger större ägg och får större avkomma. Metabolismen har påverkats så att de höns som har låg rädsla för människor har högre metabolism och omsätter även maten mer till tillväxt än de djuren med hög rädsla. Aveln har även påverkat djurens morfologi, de djuren som har hög rädsla för människor och alltså kan anses vara mer som ursprunget har större hjärna, hjärta, lever och mjälte. Många av dessa förändringar som uppkommit redan efter sex generationer korrelerar med de skillnader man ser mellan vilda och domesticerade djur vilket påvisar vikten av egenskapen för domesticeringsprocessen.

Ort, förlag, år, upplaga, sidor
Linköping: Linköping University Electronic Press, 2016. , 40 s.
Serie
Linköping Studies in Science and Technology. Dissertations, ISSN 0345-7524 ; 1790
Nationell ämneskategori
Biologiska vetenskaper Evolutionsbiologi
Identifikatorer
URN: urn:nbn:se:liu:diva-132003DOI: 10.3384/diss.diva-132003ISBN: 9789176856857 (tryckt)OAI: oai:DiVA.org:liu-132003DiVA: diva2:1036456
Disputation
2016-12-07, Planck, Fysikhuset, Campus Valla, Linköping, 09:15 (Engelska)
Opponent
Handledare
Tillgänglig från: 2016-11-17 Skapad: 2016-10-13 Senast uppdaterad: 2016-11-22Bibliografiskt granskad
Delarbeten
1. Heritability and Genetic Correlations of Fear-Related Behaviour in Red Jungelfowl -Possible Implications for Early Domestication
Öppna denna publikation i ny flik eller fönster >>Heritability and Genetic Correlations of Fear-Related Behaviour in Red Jungelfowl -Possible Implications for Early Domestication
2012 (Engelska)Ingår i: PLoS ONE, ISSN 1932-6203, Vol. 7, nr 4, e35162- s.Artikel i tidskrift (Refereegranskat) Published
Abstract [en]

Domesticated species differ from their wild ancestors in a number of traits, generally referred to as the domesticated phenotype. Reduced fear of humans is assumed to have been an early prerequisite for the successful domestication of virtually all species. We hypothesized that fear of humans is linked to other domestication related traits. For three generations, we selected Red Junglefowl (ancestors of domestic chickens) solely on the reaction in a standardized Fear of Human-test. In this, the birds were exposed for a gradually approaching human, and their behaviour was continuously scored. This generated three groups of animals, high (H), low (L) and intermediate (I) fearful birds. The birds in each generation were additionally tested in a battery of behaviour tests, measuring aspects of fearfulness, exploration, and sociality. The results demonstrate that the variation in fear response of Red Junglefowl towards humans has a significant genetic component and is genetically correlated to behavioural responses in other contexts, of which some are associated with fearfulness and others with exploration. Hence, selection of Red Junglefowl on low fear for humans can be expected to lead to a correlated change of other behavioural traits over generations. It is therefore likely that domestication may have caused an initial suite of behavioural modifications, even without selection on anything besides tameness.

Nationell ämneskategori
Naturvetenskap
Identifikatorer
urn:nbn:se:liu:diva-76833 (URN)10.1371/journal.pone.0035162 (DOI)000305336200026 ()
Tillgänglig från: 2012-04-20 Skapad: 2012-04-20 Senast uppdaterad: 2016-11-17
2. Red Junglefowl (Gallus gallus) selected for low fear of humans are larger, more dominant and produce larger offspring
Öppna denna publikation i ny flik eller fönster >>Red Junglefowl (Gallus gallus) selected for low fear of humans are larger, more dominant and produce larger offspring
2014 (Engelska)Ingår i: animal, ISSN 1751-7311, Vol. 8, nr 9, 1498-1505 s.Artikel i tidskrift (Refereegranskat) Published
Abstract [en]

Many traits associated with domestication are suggested to have developed as correlated responses to reduced fear of humans. Tameness may have reduced the stress of living in human proximity and improved welfare in captivity. We selected Red Junglefowl (ancestors of all domestic chickens) for four generations on high or low fear towards humans, mimicking an important aspect of the earliest period of domestication, and tested birds from the third and fourth generation in three different social tests. Growth and plumage condition, as well as size of eggs and offspring were also recorded, as indicators of some aspects of welfare. Birds selected for low fear had higher weight, laid larger eggs and generated larger offspring, and had a better plumage condition. In a social dominance test they also performed more aggressive behaviour and received less of the same, regardless of whether the restricted resource was feed or not. Hence, dominance appeared to increase as a consequence of reduced fear of humans. Furthermore, egg size and the weight of the offspring were larger in the less fearful birds, and plumage condition better, which could be interpreted as the less fearful animals being better adapted to the environment in which they were selected.

Ort, förlag, år, upplaga, sidor
Cambridge University Press, 2014
Nyckelord
Red Junglefowl, domestication, fearfulness, selection, social behaviour
Nationell ämneskategori
Biologiska vetenskaper
Identifikatorer
urn:nbn:se:liu:diva-109499 (URN)10.1017/S1751731114001426 (DOI)000342219000013 ()24910136 (PubMedID)
Tillgänglig från: 2014-08-20 Skapad: 2014-08-20 Senast uppdaterad: 2016-11-17
3. Is domestication driven by reduced fear of humans? Boldness, metabolism and serotonin levels in divergently selected red junglefowl (Gallus gallus)
Öppna denna publikation i ny flik eller fönster >>Is domestication driven by reduced fear of humans? Boldness, metabolism and serotonin levels in divergently selected red junglefowl (Gallus gallus)
2015 (Engelska)Ingår i: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 11, nr 9, 20150509Artikel i tidskrift (Refereegranskat) Published
Abstract [en]

Domesticated animals tend to develop a coherent set of phenotypic traits. Tameness could be a central underlying factor driving this, and we therefore selected red junglefowl, ancestors of all domestic chickens, for high or low fear of humans during six generations. We measured basal metabolic rate (BMR), feed efficiency, boldness in a novel object (NO) test, corticosterone reactivity and basal serotonin levels (related to fearfulness) in birds from the fifth and sixth generation of the high- and low-fear lines, respectively (44-48 individuals). Corticosterone response to physical restraint did not differ between selection lines. However, BMR was higher in low-fear birds, as was feed efficiency. Low-fear males had higher plasma levels of serotonin and both low-fear males and females were bolder in an NO test. The results show that many aspects of the domesticated phenotype may have developed as correlated responses to reduced fear of humans, an essential trait for successful domestication.

Ort, förlag, år, upplaga, sidor
ROYAL SOC, 2015
Nyckelord
genetics; domestication; stress
Nationell ämneskategori
Zoologi Evolutionsbiologi
Identifikatorer
urn:nbn:se:liu:diva-123162 (URN)10.1098/rsbl.2015.0509 (DOI)000364772300009 ()26382075 (PubMedID)
Anmärkning

Funding Agencies|research council Formas; ERC [322206]

Tillgänglig från: 2015-12-07 Skapad: 2015-12-04 Senast uppdaterad: 2017-01-18Bibliografiskt granskad
4. Effects of Divergent Selection for Fear of Humans on Behaviour in Red Junglefowl
Öppna denna publikation i ny flik eller fönster >>Effects of Divergent Selection for Fear of Humans on Behaviour in Red Junglefowl
2016 (Engelska)Ingår i: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 11, nr 11, 1-12 s.Artikel i tidskrift (Refereegranskat) Published
Abstract [en]

Domestication has caused a range of similar phenotypic changes across taxa, relating to physiology, morphology and behaviour. It has been suggested that this recurring domesticated phenotype may be a result of correlated responses to a central trait, namely increased tameness. We selected Red Junglefowl, the ancestors of domesticated chickens, during five generations for reduced fear of humans. This caused a marked and significant response in tameness, and previous studies have found correlated effects on growth, metabolism, reproduction, and some behaviour not directly selected for. Here, we report the results from a series of behavioural tests carried out on the initial parental generation (P0) and the fifth selected generation (S5), focusing on behaviour not functionally related to tameness, in order to study any correlated effects. Birds were tested for fear of humans, social reinstatement tendency, open field behaviour at two different ages, foraging/exploration, response to a simulated aerial predator attack and tonic immobility. In S5, there were no effects of selection on foraging/exploration or tonic immobility, while in the social reinstatement and open field tests there were significant interactions between selection and sex. In the aerial predator test, there were significant main effects of selection, indicating that fear of humans may represent a general wariness towards predators. In conclusion, we found only small correlated effects on behaviours not related to the tameness trait selected for, in spite of them showing high genetic correlations to fear of humans in a previous study on the same population. This suggests that species-specific behaviour is generally resilient to changes during domestication.

Ort, förlag, år, upplaga, sidor
PLOS, 2016
Nationell ämneskategori
Utvecklingsbiologi Genetik
Identifikatorer
urn:nbn:se:liu:diva-132742 (URN)10.1371/journal.pone.0166075 (DOI)000387909300035 ()27851792 (PubMedID)
Anmärkning

European Research Council [322206]; FORMAS [221-2007-838]; Vetenskapsradet [621-2008-5437]

Tillgänglig från: 2016-11-22 Skapad: 2016-11-22 Senast uppdaterad: 2016-12-18Bibliografiskt granskad

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