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From Wild to Tame: Domestication of the social brain in Red Junglefowl selected for tameness
Linköping University, Department of Physics, Chemistry and Biology, Biology. Linköping University, Faculty of Science & Engineering.ORCID iD: 0000-0002-3680-0769
2025 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Domestication has led to profound changes in animal behaviour, physiology, and brain morphology. This phenomenon is known as the domestication syndrome. One of the main early drivers for these phenotypic changes is hypothesised to be selection for tameness, i.e. reduced fear of humans and that this trait is heritable. Previous studies on domestication in animals have shown that selection for tameness not only changes inter-specific behaviour, as shown towards humans, but also intra-specific behaviour. This thesis examines how selection for tameness in Red Junglefowl (Gallus gallus) influences social interactions and cerebellar traits, shedding light on the mechanism underlying domestication-related changes. Paper I, II, and IV, focus on how social behaviour in chickens has been shaped by domestication, with domesticated breeds often displaying different social strategies compared to their wild ancestor. To investigate whether selection for tameness alone can drive these changes (paper I), we studied Red Junglefowl lines selected for either high (HF) or low (LF) fear of humans over multiple generations. In a semi-natural setting, we separated HF from LF and made groups consisting of two males and two females. LF birds exhibited more social conflicts and increased male crowing, while HF birds spent more time in proximity and engaged in more non-aggressive social pecking. These differences reflects behavioural distinctions found between wild Red junglefowl and domesticated laying hens, supporting the hypothesis that domestication-related social changes can arise as a side effect of tameness. In addition to changes in conspecific interactions, domesticated chickens exhibit reduced fearfulness and stress responses compared to their wild counterparts (paper II). Behavioural testing in a risk-taking scenario of domesticated White Leghorns (Gallus gallus domesticus) and parental Red junglefowl chicks confirmed that junglefowl were more fearful but also more exploratory. Importantly, social partners helped buffer fear responses in both breeds, with a stronger effect in Red Junglefowl. This suggests that domestication has not only reduced overall fear but also modified the role of social support in managing stress. To investigate the effect of a social buffer further, we gave adult chickens the choice of a known vs unknown social buffer (paper III). Four gradient groups of domestication were tested: White leghorn (WL), the parentals of unselected Red Junglefowl (RJF), low-fear Red Junglefowl (LF), high-fear Red Junglefowl (HF). The birds were tested one by one, in an arena, where they could freely investigate the area, but on each side, there were a couple of same sex birds, one with known birds, and one with unknown birds. We found that LF birds engaged in more non-aggressive social exploration and emitted more food calls; behaviours more commonly associated with domesticated chickens. While unselected RJF males showed increased interest in unfamiliar birds and displayed more agonistic behaviours, whereas this pattern was not mirrored in the HF and LF lines, suggesting that selection for tameness and fearfulness alters social coping. Notably, LF males showed similarities to domesticated White Leghorns, further supporting the idea that tameness selection contributes to shifts in social behaviour. Surprisingly, the WL females showed more agonistic behaviour, mostly towards strange birds, which could be explained by increased motivation to feed and consequently resource defence. The cerebellum, a key brain region in motor coordination and complex cognitive functions, has by different degrees, been shown to be affected by domestication in several species. While domesticated chickens have smaller relative brain size than their wild ancestors, their cerebellum has been relatively enlarged. To explore whether this pattern could be attributed to tameness selection, we examined brain morphology in HF and LF Red Junglefowl (paper III). LF birds exhibited reduced relative brain mass, particularly in the non-cerebellar brain regions, aligning with patterns observed in dully domesticated breeds. HF birds had higher neuronal density in the cerebellum, suggesting that while overall cerebellar size is increased in domesticated-like birds, it does not affect the number of neurons in the cerebellum. Hence, the reason for conserving the cerebellum size, is not more neurons. Thus, to map out the reason for the increased relative cerebellum size, different cerebellar behavioural tests assessing motor coordination, balance and social navigation, were conducted (paper V). There was no significant difference in coordination or balance between HF and LF chicks, but HF birds completed an obstacle course more quickly, possible due to increased social motivation. LF birds exhibited more reorientation pauses, which may reflect higher exploratory tendencies rather than deficits in movement control. Although the HF birds had shorter latency in an obstacle course, there was no significant difference in a rotarod test, which indicates that HF does not necessarily have superior motor skills.  In a Y-maze test assessing social preferences, HF birds showed preference for a non-aggressive rooster, indicating a possible link between fearfulness and risk-taking behaviour and social orientation, whereas this was not observed in the LF birds. The findings suggest that selection for tameness alone can drive significant changes in social behaviour, mirroring domestication effects seen in the modern domesticated chickens. These changes include increased social conflict, altered social exploration patterns, and a shift in social attraction. While LF birds have relatively larger cerebellum, this does not necessarily enhance coordination but may influence social processing, highlighting the complex relationship between tameness, behaviour, and brain morphology.

Place, publisher, year, edition, pages
Linköping: Linköping University Electronic Press, 2025. , p. 49
Series
Linköping Studies in Science and Technology. Dissertations, ISSN 0345-7524 ; 2442
Keywords [en]
Domestication, Red Junglefowl, Tameness, Chickens, Selection, Domestication syndrome
National Category
Behavioral Sciences Biology
Identifiers
URN: urn:nbn:se:liu:diva-212986DOI: 10.3384/9789181180459ISBN: 9789181180442 (print)ISBN: 9789181180459 (electronic)OAI: oai:DiVA.org:liu-212986DiVA, id: diva2:1951898
Public defence
2025-05-23, E324, Schrödinger, F-building, Campus Valla, Linköping, 09:15
Opponent
Supervisors
Available from: 2025-04-14 Created: 2025-04-14 Last updated: 2025-04-14Bibliographically approved
List of papers
1. Selection for Reduced Fear of Humans Changes Intra-Specific Social Behavior in Red Junglefowl - Implications for Chicken Domestication
Open this publication in new window or tab >>Selection for Reduced Fear of Humans Changes Intra-Specific Social Behavior in Red Junglefowl - Implications for Chicken Domestication
2022 (English)In: Genes, E-ISSN 2073-4425, Vol. 13, no 1, article id 43Article in journal (Refereed) Published
Abstract [en]

The domestic fowl has a different social behavior compared to their ancestor, the red junglefowl. To examine whether selection for tameness has affected their intra-specific social behavior, 32 red junglefowl from two selection lines, one selected for increased tameness and one selected for a high fear of humans for ten generations, were kept in a group of two females and two males each and were observed in a semi-natural undisturbed enclosure. Birds selected for a low fear of humans had more social conflict, and the males from this selection crowed more and were more often observed in low social proximity to others. The high-fear birds spent more time close together with the rest of the group and performed more social, non-aggressive pecking. These results are consistent with known differences between ancestral red junglefowl and domesticated laying hens. Our results show that intra-specific social behavior has been affected as a side-effect of selection for increased tameness. This may have interesting implications for the emergence of the domestication syndrome in chickens.

Place, publisher, year, edition, pages
MDPI, 2022
Keywords
aggression; tameness; fowl
National Category
Endocrinology and Diabetes
Identifiers
urn:nbn:se:liu:diva-182933 (URN)10.3390/genes13010043 (DOI)000749524100001 ()35052386 (PubMedID)
Available from: 2022-02-17 Created: 2022-02-17 Last updated: 2025-04-14
2. Domestication and social environment modulate fear responses in young chickens
Open this publication in new window or tab >>Domestication and social environment modulate fear responses in young chickens
2023 (English)In: Behavioural Processes, ISSN 0376-6357, E-ISSN 1872-8308, Vol. 210, article id 104906Article in journal (Refereed) Published
Abstract [en]

Domesticated species differ from their wild ancestors in a mosaic of traits. Classical domestication theories agree that reactivity to fear and stress is one of the main traits affected. Domesticated species are expected to be less fear and stress prone to than their wild counterparts. To test this hypothesis, we compared the behavioural responses of White Leghorn (WL) chicks to their wild counterparts, Red Junglefowl (RJF) chicks in risk-taking situations. In order to obtain food, the chicks faced an unknown and potentially harmful object at the presence or absence of a social partner. We found that according to our predictions, RJF were more stressed and fearful of the object than the WL. Still, RJF were more explorative than WL. Additionally, the presence of a social partner reduced the fear response in both, but had a stronger effect on RJF. Finally, WL were more food orientated than the RJF. Our results confirmed classical domestication hypotheses of downregulation of the stress system and importance of the social partner in domesticated farm chicken.

Place, publisher, year, edition, pages
ELSEVIER, 2023
Keywords
Chicken; Domestication; Red junglefowl; Risk-taking; Social buffer; Social support; Stress response
National Category
Behavioral Sciences Biology
Identifiers
urn:nbn:se:liu:diva-196806 (URN)10.1016/j.beproc.2023.104906 (DOI)001029994800001 ()37311492 (PubMedID)
Note

Funding Agencies|Austrian Science Fund (FWF) [W1262-B29]; Swedish Research Council [2019-04869]

Available from: 2023-08-23 Created: 2023-08-23 Last updated: 2025-04-14
3. Selection for Reduced Fear of Humans Changes Brain and Cerebellum Size in Red Junglefowl in Line with Effects of Chicken Domestication
Open this publication in new window or tab >>Selection for Reduced Fear of Humans Changes Brain and Cerebellum Size in Red Junglefowl in Line with Effects of Chicken Domestication
2023 (English)In: Brain Sciences, E-ISSN 2076-3425, Vol. 13, no 7, article id 988Article in journal (Refereed) Published
Abstract [en]

A central part of the domestication syndrome is a reduction in relative brain size. In chickens, it has previously been shown that domesticated birds have smaller relative brain mass, but larger relative mass of cerebellum, compared to their ancestors, the Red Junglefowl. It has been suggested that tameness may drive the domestication syndrome, so we examined the relationship between brain characteristics and tameness in 31 Red Junglefowl from lines divergently selected during ten generations for tameness. Our focus was on the whole brain, cerebellum, and the remainder of the brain. We used the isotropic fractionator technique to estimate the total number of cells in the cerebellum and differentiate between neurons and non-neuronal cells. We stained the cell nuclei with DAPI and performed cell counting using a fluorescence microscope. NeuN immunostaining was used to identify neurons. The absolute and relative masses of the brains and their regions were determined through weighing. Our analysis revealed that birds selected for low fear of humans (LF) had smaller relative brain mass compared to those selected for high fear of humans (HF). Sex had a significant impact only on the absolute size of the cerebellum, not its relative size. These findings support the notion that selection for increased tameness leads to an enlargement of the relative size of cerebellum in chickens consistent with comparisons of domesticated and ancestral chickens. Surprisingly, the HF birds had a higher density of neurons in the cerebellum compared to the LF line, despite having a smaller cerebellum overall. These findings highlight the intricate relationship between brain structure and behavior in the context of domestication.

Place, publisher, year, edition, pages
MDPI, 2023
Keywords
domestication; chicken; cerebellum
National Category
Neurosciences
Identifiers
urn:nbn:se:liu:diva-196719 (URN)10.3390/brainsci13070988 (DOI)001035057500001 ()37508920 (PubMedID)
Available from: 2023-08-21 Created: 2023-08-21 Last updated: 2025-04-14
4. Social preferences in chickens-effects of domestication and tameness
Open this publication in new window or tab >>Social preferences in chickens-effects of domestication and tameness
2024 (English)In: FRONTIERS IN ANIMAL SCIENCE, ISSN 2673-6225, Vol. 5, article id 1487688Article in journal (Refereed) Published
Abstract [en]

It has been suggested that evolution of domesticated phenotypes may have evolved as a result of correlated selection responses to reduced fear, a prominent feature in early domestication. To investigate whether domestication changes in social preferences can be attributed to increased tameness, we studied two lines of Red Junglefowl, ancestors of domesticated chickens, bidirectionally selected during 12 generations for high (HF) or low (LF) fear of humans and compared the differences between these lines to those between unselected Red Junglefowl (RJF) and domesticated White Leghorn egg layers (WL). One bird at a time was observed on its own for 12 min in an arena with one adjacent pen behind netting on each side. One of the adjacent pens contained familiar birds, and the other contained unfamiliar birds. Towards the end of the observation period, a sudden stressful stimulus was displayed, and we compared the reactions of the breeds to this as well. Male RJF spent more time close to the unfamiliar birds than WL, and performed more agonistic behaviour, but this was not mirrored in the selected birds. For females, it was WL that performed the most agonistic behaviour. Both LF and WL males showed more non-agonistic social exploration than HF and RJF respectively. Male LF and WL emitted more food calls than HF and RJF respectively. We conclude that several differences between RJF and WL were mirrored in the selection lines, with LF behaving more like domesticated WL. This is in line with the hypothesis that selection for tameness may have driven domestication related changes in social behaviour against conspecifics.

Place, publisher, year, edition, pages
FRONTIERS MEDIA SA, 2024
Keywords
domestication; Red Junglefowl (Gallus gallus); social preference; chickens; tameness; social behaviour; White Leghorn
National Category
Behavioral Sciences Biology
Identifiers
urn:nbn:se:liu:diva-210701 (URN)10.3389/fanim.2024.1487688 (DOI)001386214700001 ()2-s2.0-85213518316 (Scopus ID)
Note

Funding Agencies|Vetenskapsrdet10.13039/501100004359

Available from: 2025-01-09 Created: 2025-01-09 Last updated: 2025-05-06

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