Genomic analyses reveal a lack of widespread strong selection in indigenous chickens

Abstract

The study of domestication has been revolutionized with the advent of molecular genetics. Chickens, with their clear domestication history, emerge as an excellent model for study into the paths of evolution in domestication and improvement. Here we used genomic data from wild, indigenous, and commercial chickens to better understand how genetic drift and selection translate into their differentiations. Our investigation into the patterns of allelic change and divergence reveals a polygenic architecture governing genetic differentiation during domestication and improvement. We uncover distinctive population-specific differentiations in terms of genes and functions among wild, indigenous, and commercial chickens. Using Runs Of Homozygosity (ROH) based mixed model approach developed in this study, we identified only directional selection signatures occurring in wild and commercial chickens. Notably, our findings suggest that indigenous chickens serve as reservoirs of genetic diversity, necessary for rapid adaptation to new environments or subsequent modern breeding. This work provides unprecedented insights into the chicken domestication and improvement, and it illuminates our understanding of the domestication of other animal species.

Keywords: Allelic changes; Chicken domestication; Neural crest hypothesis; Polygenic architecture; ROH-based mixed model.

Fig. 1

Population genetic structure and diversities for chickens. (a) PCA projection of all chicken samples. (b) Unrooted neighbor-joining tree constructed by IBS distances. (c) Heatmap of pairwise outgroup-f₃ statistics of all chicken breeds, with yellow color indicating higher genetic similarity between breeds. (d) Nucleotide genetic diversity (Pi) (lines) and haplotype H12 statistic (bars) for chickens at three evolutionary stages.

Fig. 2

Genetic differentiation and allelic change in wild, indigenous and commercial chickens. (a) Genome-wide F_ST between wild chickens (green), indigenous chickens (purple) and commercial chickens (yellow). (b) Allele frequency distribution of the reference alleles in wild chickens (green), indigenous chickens (purple) and commercial chickens (yellow). (c) Changes in allele frequency between wild chickens and indigenous chickens. (d) Changes in allele frequency between indigenous chickens and commercial chickens. (e) Changes in allele frequency between wild chickens and commercial chickens.

Fig. 3

Polygenic architecture of genetic differentiation during domestication and improvement. (a) The GMM partitioning of F_ST distributions in chicken domestication. The red line indicates the expected normal distribution. GMM partitioning suggests that F_ST values can be best partitioned into four distributions (the optimal number of Gaussian components is four), each characterized by specific mean, standard deviation (SD), and weight (weight 1: 0.205; weight 2: 0.334; weight 3: 0.374; and weight 4: 0.087). (b) The GMM partitioning of F_ST distributions in chicken improvement. Four partitioned distributions are also observed (weight 1: 0.190; weight 2: 0.304; weight 3: 0.402; and weight 4: 0.103). (c) The percentage of variance explained (PVE) by each chromosome during domestication was scaled with its size, as measured by the Pearson correlation coefficient. (d) The PVE by each chromosome during improvement was scaled with its size, as measured by the Pearson correlation coefficient.

Fig. 4

LSBL analysis and functional annotation for genes under population-specific differentiation. (a) Genome-wide distribution of LSBL statistics. From the inner ring to the outer ring: wild, indigenous, and commercial chickens. (b) Overlapping of significant windows across the three stages. (c) Enrichment network constructed by similarities of enriched terms. Network nodes represent the enriched pathways. The size of the circles indicates significance. The line indicates similarity within and between clusters. (d) TRH gene association network.

Fig. 5

The results of ROH modeling. (a)-(c) Manhattan plots of the ROH modeling signals for the comparisons between the three stages. Categorical coding is applied for the evolutionary stages. The upper right corner is the OR estimates. An OR greater than 1 signifies a higher likelihood of being ROH, indicating directional selection at the stage used in the numerator in OR calculation. (d) Manhattan plot of the ROH modeling signals for three continuous stages. Ordinal coding is applied for the evolutionary stages. In the upper right corner, the Wayne diagram displays overlapping results between the two coding strategies.

Fig. 6

Differentiation across indigenous chicken breeds. (a) Manhattan plot of genomic differentiation compared to genome background from Procrustes analysis. (b) Detailed Procrustes projections of two consecutive significant windows. Each set of local F_ST matrix and global F_ST matrix is connected by a solid blue line, the hollow and solid dots correspond to two sets of F_ST matrices, and the colors of the dots represents the subspecies of indigenous chicken breeds, where the lines indicate the VR. (c) Stacked distributions of residual vectors for windows exhibiting high heterogeneity in indigenous chicken breeds (Beijing Fatty Chicken (BF), HuiYang Bearded chicken (HY), Jinhu chicken (JH), LangShan chicken (LS), QingYuan chicken (QY), Silkie chicken (SK), and WenChang chicken (WC)). (d) Phylogenetic weighting in the Twisst analysis of four taxa. Indigenous chicken breeds except SK and BF are combined into a single taxon. RJFs are used as the outgroup. (e) Phylogenetic weighting in the Twisst analysis of five taxa. SK, BF, and RJFs are removed. Unrooted phylogenetic tree is used.

Fig. 7

An illustration of selection intensity trends among wild, indigenous, and commercial chickens. The blue line represents the general understanding based on previous reports, while the red line represents the findings from the present study. The x-axis categorizes the evolutionary stages into wild, indigenous, and commercial, and the y-axis is the intensity of selection. The present study reveals a different trend compared to the general understanding, highlighting a lower intensity of selection in indigenous chickens.