Whole-genome resequencing reveals loci under selection during chicken domestication

Abstract

The domestication of the chicken over a period of several thousand years and its later specialization into meat producing (broiler) and egg producing (layer) lines is an informative model of domestication and phenotypic evolution. A study using massively parallel sequencing of domestic chicken and its wild ancestor, the red jungle fowl, reveals a number of 'selective sweeps', where benign genetic variations closely linked to a mutation that dramatically enhances survival increase in frequency relative to other alleles. Most striking of these — found in all domestic chickens — is one at a locus encoding thyroid stimulating hormone receptor, which has a key role in metabolism and vertebrate reproductive timing. This sweep may be related to a classic feature of domesticated animals, the absence of the strict regulation of seasonal reproduction found in wild populations. Several of the selective sweeps detected in broilers overlap genes associated with growth, appetite and metabolic regulation. Here, the genomes of birds representing eight populations of domestic chickens are compared with the genome of their wild ancestor, the red jungle fowl. The results reveal selective sweeps of favourable alleles and mutations that may have contributed to domestication. One selective sweep, for instance, occurred at the locus encoding the thyroid stimulating hormone receptor, which is important in metabolism and in the timing of vertebrate reproduction. Domestic animals are excellent models for genetic studies of phenotypic evolution1,2,3. They have evolved genetic adaptations to a new environment, the farm, and have been subjected to strong human-driven selection leading to remarkable phenotypic changes in morphology, physiology and behaviour. Identifying the genetic changes underlying these developments provides new insight into general mechanisms by which genetic variation shapes phenotypic diversity. Here we describe the use of massively parallel sequencing to identify selective sweeps of favourable alleles and candidate mutations that have had a prominent role in the domestication of chickens (Gallus gallus domesticus) and their subsequent specialization into broiler (meat-producing) and layer (egg-producing) chickens. We have generated 44.5-fold coverage of the chicken genome using pools of genomic DNA representing eight different populations of domestic chickens as well as red jungle fowl (Gallus gallus), the major wild ancestor4. We report more than 7,000,000 single nucleotide polymorphisms, almost 1,300 deletions and a number of putative selective sweeps. One of the most striking selective sweeps found in all domestic chickens occurred at the locus for thyroid stimulating hormone receptor (TSHR), which has a pivotal role in metabolic regulation and photoperiod control of reproduction in vertebrates. Several of the selective sweeps detected in broilers overlapped genes associated with growth, appetite and metabolic regulation. We found little evidence that selection for loss-of-function mutations had a prominent role in chicken domestication, but we detected two deletions in coding sequences that we suggest are functionally important. This study has direct application to animal breeding and enhances the importance of the domestic chicken as a model organism for biomedical research.