Abstracts (first author)

Talk 

Selection on epigenetic variation may have been important in domestication of chickens

Author(s): Jensen P, Nätt D, Jonsson M, Beltéky J, Wright D

Summary:

Epigenetic variation may cause broad phenotypic effects in animals. However, it has been debated to what extent expression variation and epigenetic modifications, such as patterns of DNA methylation, are transferred across generations, and therefore it is uncertain what role epigenetic variation may play in evolutionary processes. We compared gene expression and methylation profiles in thalamus/hypothalamus in Red Junglefowl, the ancestor of domestic chickens, and a domesticated egg laying breed (White Leghorn, WL). There were significant differeces in gene expression as well as methylation, which were largely maintained in the offspring, demonstrating reliable inheritance of epigenetic variation. More than 70% of the differentially methylated loci were hypermethylated in WL, indicating that methylations have accumulated during domestication. Furthermore, there was an over-representation of differentially expressed and methylated genes in selective sweep regions, previously shown to be associated with chicken domestication. The results show that epigenetic variation is inherited in chickens, and we suggest that selection of favourable epigenomes, may have been an important aspect of chicken domestication. This could have happened either by selection of genotypes affecting epigenetic states, or by selection of methylation states which are inherited independently of sequence differences. The relationship between specific epigenetic variants and phenotype remains to be investigated.


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Abstracts (coauthor)

Summary:

Environmental changes and selection puts pressure on an organism’s ability to adapt to new settings. An example where accelerated evolution in a short time-span has generated a large variety of phenotypes is seen in domestication, where artificial selection for desired traits have driven diversity not just from the founding origin but also in a range of different directions. Among the proposed explanations for this rapid change in phenotypes are epigenetic mechanisms. These are not only more frequent and flexible than genomic mutations, but their potential to shape individuals as well as their offspring make them viable targets for investigating the effects of environmental conditions or stimuli on an organism. With the chicken (Gallus gallus) as our model organism, we have been attempting to not only characterize behavioural differences between domestic chickens and their wild ancestors, but also specify genetic and epigenetic changes by looking at mutations, gene expression and epigenetic markers such as DNA methylation. Besides clear behaviour differences, we have found correlational changes between methylation patterns and gene expression, along with an enrichment of methylation in domestic chicken promoters. The genomic and epigenomic background, along with behavioural aspects, are currently being investigated in several projects including the effects of early stress, and an artificial selection line. Our hope is that the information generated from our experiments will give us insight in the stability and transmission of epigenetic markers, and let us expand the field of behavioural epigenetics. With knowledge about epigenetic changes in domestic animals, our understanding of their susceptibility to environmental changes such as stress or nutrition may help us in increasing animal welfare for both poultry and livestock.

Summary:

Domestication is a form of strong directional selection imparting wide-ranging phenotypic changes to animals and plants, and ever since Darwin considered a model of evolution. Changes in behaviour, particularly fearful and social behaviour, are at the heart of animal domestication. A wild by domestic advanced intercross of chickens is a powerful study system for the genetics and genomics of domestication phenotypes. We applied quantitative trait locus (QTL) mapping and genetical genomics to fear-related behaviours.

QTL mapping in 572 birds from an eight-generation intercross revealed ~44 loci for behaviour in three test situations: an open field, a social reinstatement, and a tonic immobility test. The tests have separate but overlapping architectures with a few potentially pleiotropic loci and small to moderate QTL effect sizes.

To search for underlying genes we mapped transcriptome-wide expression QTL (eQTL) in hypothalamus from 129 birds. Out of 634 eQTL, 16 candidate quantitative trait genes had eQTL coinciding with behaviour QTL and a gene expression—behaviour correlation.

Structural equations modelling found eight genes in four QTL to be consistent with a causal role of gene expression: PRDX4 (a periredoxin), ACOT9 (an acyl-coenzyme A thioesterase) and SRPX (Sushi repeat-containing) are candidates for a social reinstatement and tonic immobility locus on chromosome 1; TTRAP (TRAF and TNF receptor-associated protein) and an unknown EST sequence 60386624F1 for a social reinstatement QTL on chromosome 2; ADAM10 (disintegrin and metalloproteinase domain-containing) and APBA2 (Amyloid beta A4 precursor protein-binding) for an open field locus on chromosome 10; and the unknown LOC770352 for a second open field QTL on chromsome 10.

In conclusion, our mapping gives genetic and gene expression evidence for unexpected putative quantitative trait genes for fearful behaviour under chicken domestication.

Summary:

During domestication, chickens have been selected for genotypes which confer selective advantages in conditions under human care and rearing, but little is known about the detailed genetic mechanisms involved. In a recent study of selective sweeps associated with domestication, resequencing of different chicken breeds reveled a number of strongly selected loci. One of those, containing the α-adrenergic receptor 2C (ADRA2C), was found to be selected in layer chickens. Furthermore, previous studies from our group show that the receptor is hyper-methylated in White Leghorn (WL) chickens compared to the Red Junglefowl (RJF) ancestor, suggesting the gene to be differently expressed. ADRA2C is a presynaptic autoreceptor modulating epinephrine and norepinephrine release within the central nervous system and secretion of epinephrine from the adrenals. A down-regulation is associated with increased catecholamine secretion. Hence, domestication on the receptor might have an impact on stress responses, memory formation and egg production. We used F9-birds from an intercross between domesticated WL and RJF, and selected parents which were heterozygous for the mutation in ADRA2C generating offspring with all genotypes represented. This allowed within-family comparisons of the effects of the mutation against a randomly recombined genome. We used an array of stress related behavioral tests and we measured differences in brain expression of the gene as well as receptor density. Briefly birds with the mutation tended to have impaired associative learning and recovered more quickly after exposed to an aerial predator model. We hypothesize that the domestication of chickens have selected birds with hypo-expressed levels of ADRA2C, generating an increased catecholamine release, and that this has caused modifications of the stress response.

TSHR -a possible domestication gene

Author(s): Karlsson, A, Svemer F, Eriksson J, Andersson L, Jensen P

Summary:

Domestication, the process where wild animals adapt to captivity, offers an excellent model to study evolution. Strong selection for traits of human interest causes genetic adaptations and a rapid change in morphology, physiology and behaviour. The Red Jungle Fowl (Gallus gallus) is the wild ancestor of domesticated chickens. Resequencing has revealed a selective sweep in domestic chickens over the thyroid stimulating hormone receptor gene (TSHR). A missense mutation in TSHR causing a glycine to arginine change is the most obvious candidate causal mutation for the sweep. Thyroid hormones are important in development and the thyroid system is suggested to correlate with stress response and hence behaviour in animals. Fast development and altered behavioural responses are traits shared by all domesticated animals. Therefore, we hypothesize that a mutation in the TSHR gene has been of selective advantage during the domestication of the chicken. To study this, we used intercrosses between Red Junglefowl and domesticated White Leghorns. We included 28 birds homozygous for the TSHR mutation, 34 homozygous for the wild-type allele and 62 heterozygous birds, and subjected them to a broad phenotyping. Incubation time was recorded in order to measure development and behavioral tests for social, aggressive and fear behaviors were conducted. Individuals homozygous for the TSHR mutation had longer incubation time (21,7 ± 1,3 vs. 18,0±1,2 and 18,2±1,0 h from first hatch p<0,05), showed less aggression in a social dominance test (8,6±4,8 vs. 26,9±4,8 and 18,6±4,8 number of observations p<0,05) and less fear in a fear of human test (2,2±2,5 vs. 14,9±2,3 and 16,3±1,9 % of observations p<0,05) in comparison to the other genotypes. The results are in line with previous studies comparing pure-bred domestic White Leghorns with pure-bred Red Jungle Fowl. This indicates that a mutation in the TSHR gene could have been of selective advantage during the domestication of the chicken.

Summary:

The genetic analysis of phenotypes and the identification of the causative underlying genes remains central to molecular and evolutionary biology. By utilizing the domestication process it is possible to exploit the large differences between domesticated animals and their wild counterparts to study both this and the mechanism of domestication itself. Domestication itself is characterized by strong directional selection, which can leave putative signatures of this selection present in the genome in the form of reduced heterozygosity (referred to as selective sweeps). We have generated multiple intercrosses and advanced intercrosses based on wild-derived and domestic chickens to fine-map genomic regions (or QTL) affecting a sexual ornament (one to less than 400kb in size). These regions have been over-laid with putative selective sweeps identified in domestic chickens (each approximately 40kb in length), and found to be significantly associated with them. By using expression QTL analysis, we show that two genes in the 400kb region, HAO1 and BMP2, are controlling multiple aspects of the domestication phenotype, from a sexual ornament to multiple life-history traits. Resequencing of these animals reveals four differentially-fixed polymorphisms between the parental lines exist in strongly conserved regions within the selective sweep present within this region, which are candidate causative QTN. This study demonstrates the potential for large-effect mutations in domestication, as well as the use of selective sweeps to identify putative QTN in such instances.

Summary:

Domesticated animals can serve as models to study evolutionary processes. The hormonal stress responses of wild and domesticated animals have rarely been thoroughly compared. The Red Jungle fowl (RJF) is considered to be the main ancestor of all domesticated chicken breeds. The aim of this study was to investigate the impact of domestication on behaviour and reactivity of HPA/HPG axis to a stressful physical restraint episode. Using liquid chromatography tandem mass spectrometry methods (LC-MS/MS), plasma concentrations of 5 classes of steroids, namely, pregnanes, progestines, androgens, estrogens and glucocorticoids were measured at basal level, 10 and 60 minutes after restraint in domesticated female White Leghorn (WL) and RJF. In behaviour tests, WL had a slower stress recovery, whilst RJF resumed baselines in behaviour more quickly. Corticosterone level was significantly influenced by the stressor (p ≤ 0.001) in both breeds. RJF had significantly higher acute stress response (p ≤0.05) but quicker stress recovery compared to WL. In RJF, most other hormones were not influenced by the stressor while they were mostly significantly affected in the domesticated WL. Among the hormones which were differently altered in WL and RJF, dehydroepiandrosterone (DHEA), an androgen which is also involved in social and aggressive behaviour in birds, showed the most pronounced breed difference (p ≤ 0.005) and response to stress (p ≤ 0.001) in WL and might be highlighted as an important hormone in relation to both stress and domestication of chicken. To our knowledge this is the first comprehensive study, investigating the impact of stress on behaviour and a wide range of steroid and neurosteroid hormones in any domesticated animal and it´s wild ancestor. In conclusion, our study shows that the domesticated phenotype in chicken is related to lower HPA axis reactivity and higher HPG axis activity, which cannot be maintained in stressful situations.

Contacts

Chairman: Octávio S. Paulo
Tel: 00 351 217500614 direct
Tel: 00 351 217500000 ext22359
Fax: 00 351 217500028
email: mail@eseb2013.com

Address

XIV Congress of the European Society for Evolutionary Biology

Organization Team
Department of Animal Biology (DBA)
Faculty of Sciences of the University of Lisbon
P-1749-016 Lisbon
Portugal

Website

Computational Biology & Population Genomics Group 
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