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.

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.