The origin and genetic variation of domestic chickens with special reference to junglefowls Gallus g. gallus and G. varius

Abstract

It is postulated that chickens (Gallus gallus domesticus) became domesticated from wild junglefowls in Southeast Asia nearly 10,000 years ago. Based on 19 individual samples covering various chicken breeds, red junglefowl (G. g. gallus), and green junglefowl (G. varius), we address the origin of domestic chickens, the relative roles of ancestral polymorphisms and introgression, and the effects of artificial selection on the domestic chicken genome. DNA sequences from 30 introns at 25 nuclear loci are determined for both diploid chromosomes from a majority of samples. The phylogenetic analysis shows that the DNA sequences of chickens, red and green junglefowls formed reciprocally monophyletic clusters. The Markov chain Monte Carlo simulation further reveals that domestic chickens diverged from red junglefowl 58,000+/-16,000 years ago, well before the archeological dating of domestication, and that their common ancestor in turn diverged from green junglefowl 3.6 million years ago. Several shared haplotypes nonetheless found between green junglefowl and chickens are attributed to recent unidirectional introgression of chickens into green junglefowl. Shared haplotypes are more frequently found between red junglefowl and chickens, which are attributed to both introgression and ancestral polymorphisms. Within each chicken breed, there is an excess of homozygosity, but there is no significant reduction in the nucleotide diversity. Phenotypic modifications of chicken breeds as a result of artificial selection appear to stem from ancestral polymorphisms at a limited number of genetic loci.

Figure 1. The average-difference tree based on 1,000 concatenated sequences of randomly selected diploid sequences.

The proportion supporting a cluster is shown at each node as the realization of that cluster in the 1,000 individual trees. The TURKEY and QUAIL sequences are used as outgroups. The boxed RedDB indicates that the sequences were taken from the database of red junglefowl. Significant contributions of the domestic chicken genome to this database sequence are evident. The scale shown below the figure is a branch length corresponding to a per-site number of substitutions of 0.01 (1%). Abbreviations for samples are as follows. SHAMO: Shamo, WL: White leghorn, UKO: ukokkei, KOSHA: Koshamo, RJF: red junglefowl, GJF: green junglefowl.

Figure 2. Nucleotide divergence among mtDNA D-loop (y axis) and nuclear intron sequences (x axis).

The multiple-hit substitutions were corrected by the method of Jukes and Cantor and Kimura . Group A and A′ comprise comparisons of QUAIL and TURKEY, respectively vs. Gallus samples. Group B comprises comparisons of GJFs vs. RJFs and chickens. Group C represents inter- and intra-group comparisons of RJFs and chickens. The dotted line indicates d _mt = d _nuc. Each individual data point represents the comparison of a single species pair. Abbreviations for samples are the same as in Figure 1.

Figure 3. The proportion of shared haplotypes at 30 introns.

The 30 intron numbers in Table 2 are shown on the left. Different colors indicate different patterns of shared haplotypes as specified by the key on the right margin. CHICKENs in this Figure include only UKO and KOSHA samples. Abbreviations for samples are the same as in Figure 1.

Figure 4. ‘Structure’ graph for individual proportions of shared ancestry.

Ancestry was estimated from diploid intron sequences in the samples from four KOSHAs, four UKOs, four RJFs, and four GJFs. Predefined populations are shown on the abscissa. Different colors within each block indicate different ancestries. Abbreviations for samples are the same as in Figure 1

Figure 5. The three species and demographic parameters as estimated by MCMC and TSL methods.

With the TSL method, only pairs of species are taken into account at once, such that one of the three consecutive subscripts of a demographic parameter is shown in parentheses in the text. The symbols of θ and τ stand for the nucleotide divergence due to the extent of polymorphism and the species divergence, respectively. The subscript G, R, C means the three species, green junglefowl, red junglefowl and domestic chickens, respectively.