Effects of the domestic thyroid stimulating hormone receptor (TSHR) variant on the hypothalamic-pituitary-thyroid axis and behavior in chicken.

Domestic chickens are less fearful, have a faster sexual development, grow bigger, and lay more eggs than their primary ancestor, the red junglefowl. Several candidate genetic variants selected during domestication have been identified, but only a few studies have directly linked them with distinct phenotypic traits. Notably, a variant of the thyroid stimulating hormone receptor (TSHR) gene has been under strong positive selection over the past millennium, but it's function and mechanisms of action are still largely unresolved. We therefore assessed the abundance of the domestic TSHR variant and possible genomic selection signatures in an extensive data set comprising multiple commercial and village chicken populations as well as wild-living extant members of the genus Gallus. Furthermore, by mean of extensive backcrossing we introgressed the wild-type TSHR variant from red junglefowl into domestic White Leghorn chickens and investigated gene expression, hormone levels, cold adaptation, and behavior in chickens possessing either the wild-type or domestic TSHR variant. While the domestic TSHR was the most common variant in all studied domestic populations and in one of two red junglefowl population, it was not detected in the other Gallus species. Functionally, the individuals with the domestic TSHR variant had a lower expression of the TSHR in the hypothalamus and marginally higher in the thyroid gland than wild-type TSHR individuals. Expression of TSHB and DIO2, two regulators of sexual maturity and reproduction in birds, was higher in the pituitary gland of the domestic-variant chickens. Furthermore, the domestic variant was associated with higher activity in the open field test. Our findings confirm that the spread of the domestic TSHR variant is limited to domesticated chickens, and to a lesser extent, their wild counterpart, the red junglefowl. Furthermore, we showed that effects of genetic variability in TSHR mirror key differences in gene expression and behavior previously described between the red junglefowl and domestic chicken.

Optimism, pessimism and judgement bias in animals: A systematic review and meta-analysis.

Just as happy people see the proverbial glass as half-full, 'optimistic' or 'pessimistic' responses to ambiguity might also reflect affective states in animals. Judgement bias tests, designed to measure these responses, are an increasingly popular way of assessing animal affect and there is now a substantial, but heterogeneous, literature on their use across different species, affect manipulations, and study designs. By conducting a systematic review and meta-analysis of 459 effect sizes from 71 studies of non-pharmacological affect manipulations on 22 non-human species, we show that animals in relatively better conditions, assumed to generate more positive affect, show more 'optimistic' judgements of ambiguity than those in relatively worse conditions. Overall effects are small when considering responses to all cues, but become more pronounced when non-ambiguous training cues are excluded from analyses or when focusing only on the most divergent responses between treatment groups. Task type (go/no-go; go/go active choice), training cue reinforcement (reward-punishment; reward-null; reward-reward) and sex of animals emerge as potential moderators of effect sizes in judgement bias tests.

Experimentally induced increases in fecundity lead to greater nestling care in blue tits.

Models on the evolution of bi-parental care typically assume that maternal investment in offspring production is fixed and predict subsequent contributions to offspring care by the pair are stabilized by partial compensation. While experimental tests of this prediction are supportive, exceptions are commonplace. Using wild blue tits ( Cyanistes caeruleus), we provide, to our knowledge, the first investigation into the effects of increasing maternal investment in offspring production for subsequent contributions to nestling provisioning by mothers and male partners. Females that were induced to lay two extra eggs provisioned nestlings 43% more frequently than controls, despite clutch size being made comparable between treatment groups at the onset of incubation. Further, experimental males did not significantly reduce provisioning rates as expected by partial compensation, and if anything contributed slightly (9%) more than controls. Finally, nestlings were significantly heavier in experimental nests compared with controls, suggesting that the 22% average increase in provisioning rates by experimental pairs was beneficial. Our results have potential implications for our understanding of provisioning rules, the maintenance of bi-parental care and the timescale over which current-future life-history trade-offs operate. We recommend greater consideration of female investment at the egg stage to more fully understand the evolutionary dynamics of bi-parental care.

The Domestic BCO2 Allele Buffers Low-Carotenoid Diets in Chickens: Possible Fitness Increase Through Species Hybridization.

Domestic animals are adapted to conditions vastly different from those of their wild ancestors, and this is particularly true for their diets. The most numerous of all domestic species, the chicken, originated from the Red Junglefowl (RJF), a native of subtropical forests in Southeast Asia. Surprisingly however, in domestic chicken breeds, a common haplotype of the ß-carotene oxygenase 2 (BCO2) gene, which is involved in carotenoid metabolism, is introgressed from a related species, the Gray Junglefowl, and has been under strong selective pressure during domestication. This suggests that a hybridization event may have conferred a fitness advantage on chickens carrying the derived allele. To investigate the possible biological function of the introgressed BCO2 allele in chicken, we introgressed the ancestral BCO2 allele into domestic White Leghorn chickens. We measured gene expression as well as carotenoid accumulation in skin and eggs of chickens carrying either the ancestral or the derived BCO2 allele. The derived haplotype was associated with down-regulation of BCO2 in skin, muscle, and adipose tissue, but not in liver or duodenum, indicating that carotenoid accumulation occurred in the tissues with reduced gene expression. Most importantly, we found that hens with the derived BCO2 genotype were capable of allocating stored carotenoids to their eggs, suggesting a functional benefit through buffering any shortage in the diet during egg production. Nevertheless, it is of interest that loss of function mutations in BCO2 gene are prevalent in other domesticates including cows, rabbits, and sheep, and, given the importance of carotenoids in development, reproduction, and immunity, it is possible that derived BCO2 alleles may provide a general mechanism in multiple domestic species to deal with higher demand for carotenoids in an environment with carotenoid shortage in the diet.

The relationship between learning speed and personality is age- and task-dependent in red junglefowl.

ABSTRACT: Cognition is fundamental to animals' lives and an important source of phenotypic variation. Nevertheless, research on individual variation in animal cognition is still limited. Further, although individual cognitive abilities have been suggested to be linked to personality (i.e., consistent behavioral differences among individuals), few studies have linked performance across multiple cognitive tasks to personality traits. Thus, the interplays between cognition and personality are still unclear. We therefore investigated the relationships between an important aspect of cognition, learning, and personality, by exposing young and adult red junglefowl (Gallus gallus) to multiple learning tasks (discriminative, reversal, and spatial learning) and personality assays (novel arena, novel object, and tonic immobility). Learning speed was not correlated across learning tasks, and learning speed in discrimination and spatial learning tasks did not co-vary with personality. However, learning speed in reversal tasks was associated with individual variation in exploration, and in an age-dependent manner. More explorative chicks learned the reversal task faster than less explorative ones, while the opposite association was found for adult females (learning speed could not be assayed in adult males). In the same reversal tasks, we also observed a sex difference in learning speed of chicks, with females learning faster than males. Our results suggest that the relationship between cognition and personality is complex, as shown by its task- and age-dependence, and encourage further investigation of the causality and dynamics of this relationship. SIGNIFICANCE STATEMENT: In the ancestor of today's chickens, the red junglefowl, we explored how personality and cognition relate by exposing both chicks and adults to several learning tasks and personality assays. Our birds differed in personality and learning speed, while fast learners in one task did not necessarily learn fast in another (i.e., there were no overall "smarter" birds). Exploration correlated with learning speed in the more complex task of reversal learning: faster exploring chicks, but slower exploring adult females, learned faster, compared to less explorative birds. Other aspects of cognition and personality did not correlate. Our results suggest that cognition and personality are related, and that the relationship can differ depending on task and age of the animal.

Heritabilities and co-variation among cognitive traits in red junglefowl.

Natural selection can act on between-individual variation in cognitive abilities, yet evolutionary responses depend on the presence of underlying genetic variation. It is, therefore, crucial to determine the relative extent of genetic versus environmental control of these among-individual differences in cognitive traits to understand their causes and evolutionary potential. We investigated heritability of associative learning performance and of a cognitive judgement bias (optimism), as well as their covariation, in a captive pedigree-bred population of red junglefowl (Gallus gallus, n > 300 chicks over 5 years). We analysed performance in discriminative and reversal learning (two facets of associative learning), and cognitive judgement bias, by conducting animal models to disentangle genetic from environmental contributions. We demonstrate moderate heritability for reversal learning, and weak to no heritability for optimism and discriminative learning, respectively. The two facets of associative learning were weakly negatively correlated, consistent with hypothesized trade-offs underpinning individual cognitive styles. Reversal, but not discriminative learning performance, was associated with judgement bias; less optimistic individuals reversed a previously learnt association faster. Together these results indicate that genetic and environmental contributions differ among traits. While modular models of cognitive abilities predict a lack of common genetic control for different cognitive traits, further investigation is required to fully ascertain the degree of covariation between a broader range of cognitive traits and the extent of any shared genetic control.This article is part of the theme issue 'Causes and consequences of individual differences in cognitive abilities'.

Early experience affects adult personality in the red junglefowl: A role for cognitive stimulation?

Despite intense research efforts, biologists are still puzzled by the existence of animal personality. While recent studies support a link between cognition and personality, the directionality of this relationship still needs to be clarified. Early-life experiences can affect adult behaviour, and among these, cognitive stimulation has been suggested theoretically to influence personality. Yet, the influence of early cognitive stimulation has rarely been explored in empirical investigations of animal behaviour and personality. We investigated the effect of early cognitive stimulation on adult personality in the red junglefowl (Gallus gallus). To this end, we assessed adult behaviour across a number of personality assays and compared behaviour of individuals previously exposed to a series of learning tasks as chicks, with that of control individuals lacking this experience. We found that individuals exposed to early stimulation were, as adults, more vigilant and performed fewer escape attempts in personality assays. Other behaviours describing personality traits in the fowl were not affected. We conclude that our results support the hypothesis that early stimulation can affect aspects of adult behaviour and personality, suggesting a hitherto underappreciated causality link between cognition and personality. Future research should aim to confirm these findings and resolve their underlying dynamics and proximate mechanisms.

The price of associating with breeders in the cooperatively breeding chestnut-crowned babbler: foraging constraints, survival and sociality.

Understanding the costs of living with breeders might offer new insights into the factors that counter evolutionary transitions from selfish individuals to cooperative societies. While selection on early dispersal is well understood, it is less clear whether costs are also associated with remaining with family members during subsequent breeding, a prerequisite to the evolution of kin-based cooperation. We propose and test the hypothesis that living in groups containing breeders is costly and that such costs are exacerbated by increasing group size. For example, in group-living central-place foragers, group members might suffer from resource depletion when foraging in a restricted area during breeding and significant costs of repeatedly travelling between foraging patches and the site of offspring. Using the cooperatively breeding chestnut-crowned babbler (Pomatostomus ruficeps), for which grouping during breeding is obligatory, we show that reproduction is associated with substantially reduced foraging areas and evidence of resource depletion, particularly in larger groups. Such effects largely persisted from the onset of incubation through to offspring independence 4-5 months later. All group members, irrespective of their breeder or helper status, lost significant body mass over this period, and, in males, mass loss was associated with reduced interannual survival. Although babblers are constrained from living outside of breeding groups due to high risks of predation and the poor success of breeding without helpers, we suggest that the effects we describe may generally select against group living during breeding attempts in species where constraints to independent breeding and costs of dispersal are less acute.

High atmospheric temperatures and 'ambient incubation' drive embryonic development and lead to earlier hatching in a passerine bird.

Tropical and subtropical species typically experience relatively high atmospheric temperatures during reproduction, and are subject to climate-related challenges that are largely unexplored, relative to more extensive work conducted in temperate regions. We studied the effects of high atmospheric and nest temperatures during reproduction in the zebra finch. We characterized the temperature within nests in a subtropical population of this species in relation to atmospheric temperature. Temperatures within nests frequently exceeded the level at which embryo's develop optimally, even in the absence of parental incubation. We experimentally manipulated internal nest temperature to demonstrate that an average difference of 6°C in the nest temperature during the laying period reduced hatching time by an average of 3% of the total incubation time, owing to 'ambient incubation'. Given the avian constraint of laying a single egg per day, the first eggs of a clutch are subject to prolonged effects of nest temperature relative to later laid eggs, potentially increasing hatching asynchrony. While birds may ameliorate the negative effects of ambient incubation on embryonic development by varying the location and design of their nests, high atmospheric temperatures are likely to constitute an important selective force on avian reproductive behaviour and physiology in subtropical and tropical regions, particularly in the light of predicted climate change that in many areas is leading to a higher frequency of hot days during the periods when birds breed.

Hormonal and behavioural symmetries between the sexes in the Northern bald ibis.

Seasonal patterns of fecal androgen and corticosteroid levels were measured in a semi-tame colony of Northern bald ibis (Geronticus eremita) and put in perspective with socio-sexual patterns. Northern bald ibis are monomorphic, monogamous, year-round social colonial breeders. Steroids levels were assessed from the pre-mating until the end of the mating season in the sexes, age groups, and social categories. Male immunoreactive androgen concentrations, determined by enzyme immuno-assay from feces, were relatively low, even during the mating phase, and were close to the female levels. Sexual monomorphy and symmetries in socio-sexual and parental roles may account for this similarity. Males and females responded in a similar way to social challenges from conspecifics, particularly during pair-formation. Singletons showed higher androgen metabolites levels than paired individuals. Corticosterone metabolites were relatively high during periods of social instability in the mating phase and were highest in low-ranking, young individuals. We suggest that the challenge hypothesis may even apply to females in this non-passerine bird.