The wild species genome ancestry of domestic chickens

Abstract

Background: Hybridisation and introgression play key roles in the evolutionary history of animal species. They are commonly observed within several orders in wild birds. The domestic chicken Gallus gallus domesticus is the most common livestock species. More than 65 billion chickens are raised annually to produce meat and 80 million metric tons of egg for global human consumption by the commercial sector. Unravelling the origin of its genetic diversity has major application for sustainable breeding improvement programmes.

Results: In this study, we report genome-wide analyses for signatures of introgression between indigenous domestic village chicken and the four wild Gallus species. We first assess the genome-wide phylogeny and divergence time across the genus Gallus. Genome-wide sequence divergence analysis supports a sister relationship between the Grey junglefowl G. sonneratii and Ceylon junglefowl G. lafayettii. Both species form a clade that is sister to the Red junglefowl G. gallus, with the Green junglefowl G. varius the most ancient lineage within the genus. We reveal extensive bidirectional introgression between the Grey junglefowl and the domestic chicken and to a much lesser extent with the Ceylon junglefowl. We identify a single case of Green junglefowl introgression. These introgressed regions include genes with biological functions related to development and immune system.

Conclusions: Our study shows that while the Red junglefowl is the main ancestral species, introgressive hybridisation episodes have impacted the genome and contributed to the diversity of the domestic chicken, although likely at different levels across its geographic range.

Keywords: Chicken domestication; Chicken introgression; Divergence time; Evolution; Galliformes; Gallus species; Genetic diversity; Interspecies hybridisation; Livestock species; Speciation.

Fig. 1.

a The geographic distribution of the four junglefowl species. The sympatric geographic regions between the Indian red junglefowl (Gallus gallus murghi) and the Grey junglefowl on the Indian subcontinent and between the Javanese red junglefowl (Gallus gallus bankiva) and the Green junglefowl on the Indonesian Islands are annotated with dots on the map. The map was drawn by overlaying the distribution map of each species obtained from the Handbook of the Birds of the World (consulted in December 2018). Autosomal—b principal component and c admixture analysis. Junglefowl species photo credits: Peter Ericsson (Red junglefowl), Clement Francis (Grey junglefowl), Markus Lilje (Ceylon junglefowl), and Eric Tan (Green junglefowl)

Fig. 2.

The genome-wide phylogeny of the genus Gallus. a, c, d Neighbour-joining phylogenetic trees for the autosomes, Z chromosome, and mitochondrial DNA, respectively. b The distance matrix of the autosomes constructed from the NeighborNet network of SplitsTree4. d The three Grey junglefowl mtDNA haplotypes embedded within the domestic/Red junglefowl lineage are indicated with a black arrow. All the trees are rooted with the common Pheasant Phasianus colchicus

Fig. 3.

Topology weighting by iterative sampling of sub-trees (Twisst). a The 15 possible topologies (T1–T15) from 5 taxa. As the number of possible topologies works best for a maximum of 5 taxa [22] and with the presence of 7 taxa in this study, we ran the analysis thrice: with b domestic chicken “D,” c Red junglefowl “R,” and d Javanese Red junglefowl “J.” The average weightings (%) for each of the 15 topologies are included in each bar and as well as indicated on the Y axis. Domestic chicken or Red junglefowl or Javanese red junglefowl (DRJ), Grey junglefowl (Gy), Ceylon junglefowl (Cy), Green junglefowl (Gn), and common Pheasant (CP)

Fig. 4.

The f_d plots test for the comparison between the Grey junglefowl and the domestic chicken populations from a Ethiopia and Saudi Arabia, b Sri Lanka, and c Southeast Asia (Indonesia), and East Asia (China). d Geographical map showing the countries and regions of origin for each domestic chicken population. The Grey junglefowl G. sonneratii geographic distribution is India. Genes within the candidate regions highlighted by their sizes are described in Additional file 4: Table S2 and Additional file 8: Table S3. Y axis: f_d value spanning 0 to 1, X axis: autosomal chromosomes number from 1 to 28. See Additional files 16 and 19 for the domestic–Ceylon and the domestic–Green junglefowl comparisons, respectively

Fig. 5.

A 120-kb (Chr 6: 21,729,370–21,849,500 bp, based on GRCg6a reference) introgressed region from the Grey junglefowl into the domestic chicken. A f_d plot. B Twisst plot (B₁ its topologies and B₂ their proportions). The most consistent topology (80%) has a monophyletic relationship between targetDom (introgressed domestic haplotypes) and Grey junglefowl. C dxy and D Fst. Eth, Sau, SriLanka, and SE + E are domestic chickens from Ethiopia, Saudi Arabia, Sri Lanka, and Southeast Asia (Indonesia) + East Asia (China), respectively. targetDom are the introgressed domestic chicken haplotypes from Grey junglefowl (GreyJ) denoted as (*) in E haplotype-based network and F maximum likelihood tree

Fig. 6.

Topologies (Twisst), their estimated proportions, and network analyses for the introgression from a domestic chicken to Grey junglefowl (2.8 Mb, Chr 4: 76,429,662–79,206,200 bp), b Ceylon junglefowl to domestic chicken (600 kb, Chr 3: 108,325,801–108,925,700 bp), c domestic chicken/Red junglefowl to Ceylon junglefowl (100 kb, Chr 5: 49,333,700–49,433,700 bp), and d Green junglefowl to domestic chicken (100 kb, Chr 5: 9,538,700–9,638,700 bp), based on GRCg6a reference. (*) introgressed haplotypes. The targetGreyJ, targetDom, and targetCeylon in the Twisst are the introgressed, as revealed by the network, Grey junglefowl, domestic chicken, and Ceylon junglefowl haplotypes, respectively