The domesticated chicken, Gallus gallus domesticus, is the most numerous domestic animal and a preferred source of animal protein. Chicken domestication has been thought (based on traditional measures) to have arisen in the Holocene (beginning ~11,650 years ago) from related species subspecies of wild jungle fowl, including five subspecies of red jungle fowl (RJF): G. g. gallus, G. g. spadiceus, G. g. jabouillei, G. g. murghi, and G. g. bankiva, using traditional morphological methods of comparison. But these methodologies have been stymied (with regard to a definitive determination regarding which of these subspecies was the progenitor) because there are no features of the bone morphology that distinguish one subspecies from another.
Recently, an international group of researchers published a paper entitled "863 genomes reveal the origin and domestication of chicken" in Cell Research (2020). This paper provides data consistent with modern domestic chickens being descendants of one of these subspecies, Gallus gallus spadiceus, which today exists in Southwestern China, northern Thailand and Myanmar. However, these studies also showed that as chickens were "translocated" through South and Southeast Asia in association with human dispersal there arose interbreeding with local red jungle fowl subspecies and other species. As a consequence, the White Leghorn chicken (the predominant commercially important breed) is a genetic mosaic of ancestries from other RJF subspecies.
Prior studies of domesticated chicken ancestry were based on mitochondrial DNA that suggested chickens were domesticated multiple times in different cultures. Because the domestic chicken can interbreed with wild subspecies relatives, including ones never domesticated, misleading results can be (and according to this work, were) obtained when based on mtDNA (which acts like a single genetic marker). The methodologies used in these studies, whole genome sequencing (WGS), provides a more robust source of genetic information, and accordingly has been performed in previous studies in other species, in plants as well as animals. Such studies have been performed on chickens, but as the authors explain, these studies have been limited to domestic chickens and did not include genetic information from putative ancestor species, which information is necessary to do the comparisons needed to elucidate the genetic consequences of chicken domestication. This paper provides that information.
The authors report that they performed WGS on 627 domestic chickens, 142 RJFs encompassing all five subspecies, 12 green jungle fowls (G. varius), 2 gray jungle fowls (G. sonneratii), and 4 Ceylon jungle fowls (G. lafayettii). These genomes analyzed along with 76 previously published genomes (69 chickens and 7 RJF).
Genetic comparison of 149 RJF genomes clustered them into 5 clades, with G. g. bankiva, being basal to all RJF subspecies. Statistical analysis indicated that there was "a long history of gene flow between RJF subspecies." Nevertheless, these authors' analyses "indicate[d] that all RJF subspecies are genetically differentiated, which generally correspond to their geographic ranges and taxonomic classifications," these authors report. They conclude from these results that:
G. g. bankiva is the most divergent subspecies and has a time to the most recent common ancestor (TMRCA) with the other RJF subspecies prior to 500 kya. . . . The TMRCA of the four other RJF subspecies was between 50 and 125 kya [thousand years ago]. These analyses indicate that all of the RJF subspecies diverged from one another substantially earlier than the advent of chicken domestication.
The paper next considered the geographic origin of domestic chickens. "The phylogeny constructed with all 149 RJFs and 696 domestic chickens supports a monophyletic clade composed of some wild G. g. spadiceus specimens and all but two of the 696 domestic chickens." All domestic chicken populations are most closely related to wild G. g. spadiceus, with the split of G. g. spadiceus from domestic chickens having taken place ~9500 ± 3300 years ago.
Geographically, the authors report two clades:
Clade I includes chickens from Europe and the Americas (including European broiler and egg layer chickens of White Leghorn, White Plymouth, Rhode Island Red and Cornish breeds), Iran, Pakistan, India, Bangladesh and northwestern China (i.e., Tibet and Xinjiang provinces bordering India). Clade II contains mostly northern, central, and southern Chinese village chickens (i.e., from Shanxi and Jiangxi provinces). Branches basal to the two clades, but within the total diversity of chickens, include 128 chickens sampled almost exclusively from the Yunnan province of China, Thailand, Vietnam and Indonesia. These individuals may represent the earliest domestic lineages or have admixed with local RJF subspecies.
This is illustrated as follows:
Starting from this origin (which contradicts earlier estimates that domestic chickens arose during the Neolithic in northern China), the authors further report that specimens from alternative locales (such as the Indus Valley in what is now Pakistan) "showed a deeper divergence from chickens than the remaining birds of G. g. murghi collected from northeastern India." These data were consistent with mtDNA analyses and with the congruence of the estimated divergence time (54,800 +/- 5,100 years ago) between G. g. murghi and G. g. spadiceus subspecies and the estimated divergence time between G. g. spadiceus and domestic chickens (i.e., the two subspecies diverged prior to divergence of either subspecies with domestic chickens). However, due to introgression after domestication, these authors determined that G. g. murghi contributed 3.8-22.4% of the genome of modern White Leghorn domesticated chickens. These analyses also supported earlier studies suggesting that three additional species (green jungle fowl with Indonesia chicken, Ceylon jungle fowl with Sri Lankan chicken, and the gray jungle fowl) contributed to the modern domesticated genome, although contributions from the former two species occurred at low frequencies.
Turning to specific genetic features related to adaptation of domestic chickens that were subjected to positive selection therefore, these authors report that these included "genes bearing signal of selection are associated with development of nervous system, muscle and bone as well as regulation of growth, metabolism and reproduction." Specifically, these genes included "multiple genes with evidence of selection are found in the neural crest development pathway, including FGFR1 (fibroblast growth factor receptor 1), MYC-l, ERBB4, and BMPs." Of particular significance was detection of positive selection of the FGFR1 gene, which is known to be involved in the regulation of embryonic development and skeletogenesis and has been found in other domesticated animals including horses and carp. The involvement of these and other genes (including GNRH-I (gonadotropin-releasing hormone 1) and KIF18A (kinesin family member 18A)), involved in embryogenesis, may be related to the domesticated chicken phenotypes of increased fertility and increased egg production compared with their wild relatives.
Finally, these researchers report that a missense mutation in thyroid stimulating hormone receptor, previously thought to be a genetic marker for domestication, was fixed in the ancestral G. g. spadiceus (but only in this subspecies).
The authors close by stating:
The novel findings from this study provide new insights into the origin and evolutionary history of domestic chickens. The identification of unique genomic landscapes of all RJF subspecies and three additional jungle fowl species suggests that conservation efforts should be made to safeguard them from extinction. These rich genomic resources will pave the way to facilitate ongoing explorations into the biocultural history of the relationship between humans and chickens as well as the development of fast-growing, high-quality and cost-effective lineages.
Image of "A cock and a hen roosting together" by Andrei Niemimäki, from the Wikimedia Commons under the Creative Commons Attribution-Share Alike 2.0 Generic license.