Cerebellum size is related to fear memory and domestication of chickens.

Red Junglefowl (Gallus gallus) were selected for divergent levels of fear of humans during eight generations, causing the selection lines to differ in fear levels as well as in the proportional brain and cerebellum masses. Birds from the two lines were then crossed to obtain an F3 intercross in order to study the correlations between brain mass and fear learning. We exposed 105 F3-animals individually to a fear habituation and memory test at 8 days of age, where the reactions to repeated light flashes were assessed on 2 consecutive days. After culling, the absolute and relative sizes of each of four brain regions were measured. Stepwise regression was used to analyse the effects of the size of each brain region on habituation and memory. There were no effects of any brain region on the habituation on day one. However, birds with a larger absolute size of cerebellum had significantly reduced reactions to the fearful stimuli on day two, indicating a better memory of the stimuli. No other regions had significant effects. We conclude that increased cerebellum size may have been important in facilitating chicken domestication, allowing them to adapt to a life with humans.

Is domestication driven by reduced fear of humans? Boldness, metabolism and serotonin levels in divergently selected red junglefowl (Gallus gallus).

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.

Tameness correlates with domestication related traits in a Red Junglefowl intercross.

Early animal domestication may have been driven by selection on tameness. Selection on only tameness can bring about correlated selection responses in other traits, not intentionally selected upon, which may be one cause of the domesticated phenotype. We predicted that genetically reduced fear towards humans in Red Junglefowl, ancestors of domesticated chickens, would be correlated to other traits included in the domesticated phenotype. Fear level was determined by a standardised behaviour test, where the reaction towards an approaching human was recorded. We first selected birds for eight generations for either high or low fear levels in this test, to create two divergent selection lines. An F3 intercross, with birds from the eighth generation as parentals, was generated to study correlations between fear-of-human scores and other unselected phenotypes, possibly caused by pleiotropy or linkage. Low fear-of-human scores were associated with higher body weight and growth rates, and with increased activity in an open field test, indicating less general fearfulness. In females, low fear-of-human scores were also associated with more efficient fear habituation and in males with an increased tendency to emit food calls in a mirror test, indicating increased social dominance. Low fear-of-human scores were also associated with smaller brain relative to body weight, and with larger cerebrum relative to total brain weight in females. All these effects are in line with the changes observed in domesticated chickens compared to their ancestors, and we conclude that tameness may have been a driving factor underlying some aspects of the domesticated phenotype.

Long-term stress in dogs is related to the human-dog relationship and personality traits.

Previously, we found that dogs belonging to the herding breed group, selected for human cooperation, synchronise their long-term stress levels with their owners. The aim of the current study was to investigate features that could influence long-term stress levels in ancient dog breeds, genetically closer to wolves, and dogs specifically selected to work independently of their owner. Twenty-four ancient breed dogs and 18 solitary hunting dogs were recruited and hair samples were obtained from both dogs and owners from which hair cortisol concentration (HCC) was analysed. Additionally, the owners completed lifestyle surveys, the Monash Dog Owner Relationship Scale (MDORS) on human-dog relationship, and both dog and owner personality questionnaires (Dog Personality questionnaire and Big Five Inventory survey). The results from the MDORS indicate that the subscale Perceived cost correlated to the dog HCC of tested breed groups: solitary hunting breeds (χ2 = 4.95, P = 0.026, ß = 0.055), ancient breeds (χ2 = 2.74, P = 0.098, ß = 0.027), and herding dogs included from a previous study (χ2 = 6.82, P = 0.009, ß = - 0.061). The HCC of the solitary hunting dogs was also related to the owner personality traits Agreeableness (χ2 = 12.30, P < 0.001, ß = - 0.060) and Openness (χ2 = 9.56, P = 0.002, ß = 0.048) suggesting a more substantial influence of the owner on the solitary hunting dog's HCC compared to the ancient breeds. No effect of owner HCC on dog HCC was found in either ancient or in solitary hunting breeds. Hence, the long-term stress synchronisation is likely to be a trait in breeds selected for human cooperation. In conclusion, dog HCC is often related to the owners' personality, but is primarily influenced by the owner-dog relationship.

Gut Microbiota Linked with Reduced Fear of Humans in Red Junglefowl Has Implications for Early Domestication.

Domestication of animals can lead to profound phenotypic modifications within short evolutionary time periods, and for many species behavioral selection is likely at the forefront of this process. Animal studies have strongly implicated that the gut microbiome plays a major role in host behavior and cognition through the microbiome-gut-brain axis. Consequently, herein, it is hypothesized that host gut microbiota may be one of the earliest phenotypes to change as wild animals were domesticated. Here, the gut microbiome community in two selected lines of red junglefowl that are selected for either high or low fear of humans up to eight generations is examined. Microbiota profiles reveal taxonomic differences in gut bacteria known to produce neuroactive compounds between the two selection lines. Gut-brain module analysis by means of genome-resolved metagenomics identifies enrichment in the microbial synthesis and degradation potential of metabolites associated with fear extinction and reduces anxiety-like behaviors in low fear fowls. In contrast, high fear fowls are enriched in gut-brain modules from the butyrate and glutamate pathways, metabolites associated with fear conditioning. Overall, the results identify differences in the composition and functional potential of the gut microbiota across selection lines that may provide insights into the mechanistic explanations of the domestication process.

Selection for reduced fear in red junglefowl changes brain composition and affects fear memory.

Brain size reduction is a common trait in domesticated species when compared to wild conspecifics. This reduction can happen through changes in individual brain regions as a response to selection on specific behaviours. We selected red junglefowl for 10 generations for diverging levels of fear towards humans and measured brain size and composition as well as habituation learning and conditioned place preference learning in young chicks. Brain size relative to body size as well as brainstem region size relative to whole brain size were significantly smaller in chicks selected for low fear of humans compared to chicks selected for high fear of humans. However, when including allometric effects in the model, these differences disappear but a tendency towards larger cerebra in low-fear chickens remains. Low-fear line chicks habituated more effectively to a fearful stimulus with prior experience of that same stimulus, whereas high-fear line chicks with previous experience of the stimulus had a response similar to naive chicks. The phenotypical changes are in line with previously described effects of domestication.

Activity, social and sexual behaviour in Red Junglefowl selected for divergent levels of fear of humans.

The domesticated phenotype is a set of behavioural, morphological and physiological traits that is common for domesticated species. Previous research has found that selection for tameness only can give rise to correlated selection responses that resemble the domesticated phenotype. It has therefore been suggested that tameness may drive the domesticated phenotype as correlated traits. We selected Red Junglefowl for divergent levels of fear of human for eight generations and assessed possible correlated selection responses in other behaviours in semi-natural settings. Behavioural studies were carried out on birds from generations six to eight, and at different ages, in order to study possible effects on general activity, social behaviour and male courtship behaviour. We found that the differences between selection lines changed with age. Adult low fear birds were generally more active and high fear males showed a more intense courtship behaviour. Our study shows that several behaviours can be modified through correlated selection responses by selection on reduced fear of humans only, emphasising the putative role of tameness as a driver of domestication related phenotypes.