The origin and history of genetic diversity of local chickens in the Middle East and Africa

Among the various livestock animals, chickens and their products (meat and eggs) are becoming increasingly important in sustaining human livelihood. They also represent an important model species in evolutionary studies. Today, four main types of domestic chicken may be recognised, chicken commercial breeds, fancy breeds, inbred research lines and indigenous village chicken breeds or populations. The latter are supplying high-quality protein to poor communities, particularly in Africa and Asia, contributing to food security, poverty alleviation and the management of natural resources. The importance of chicken arises from many features (e.g short generation time, facility to breed them in captivity) that make them an ideal model species in different areas including embryology, physiology and medicine (e.g. vaccine development). Closely associated with human society, they represent an important proxy for the understanding of the history of human communities. The two aims of this thesis were (i) to evaluate different genetic markers for the understanding and unravelling of chicken history and (ii) to trace the migration routes of village chickens outside the probable domestication centre on the Indian subcontinent. The study involved analysis of samples of domestic chickens from Iraq, Ethiopia, Algeria, Libya, Pakistan and Saudi Arabia, together with samples of the four junglefowl species (Ceylon, Grey, Green and Red junglefowl). All our domestic chicken populations originate from the West and North-West of the Indian subcontinent, a putative centre of domestication for the species. We used full genome sequence information of high coverage (30 X) with all samples used in this study mapped against the reference genome Galgal 5.0. The first marker investigated (Chapter 2) was the mitochondrial (D-loop) sequences, which is the hypervariable part of the mtDNA control region. This marker has been used in several studies, and it is today our main source of information to reconstruct the history of the species. In this part, 706 samples from the six countries, including countries where we were lacking any information regarding the diversity of this marker so far were used. The results support an Indian subcontinent origin for the populations investigated as well as both a terrestrial and a more recent maritime, across the Indian Ocean, dispersal route. These two routes of migration have affected today’s genetic diversity of the chicken populations examined, although in different proportions. Furthermore, in some countries, there was evidence of a decline in the maternal population effective size following expansion, while others showed a recent expansion without any decline. However, this genetic marker barely shows any within-country phylogeographic signal. The next chapter (Chapter 3) examined if two other types of markers, the full mtDNA sequence and the W chromosome, may provide us with more information. As for the D-loop, they are maternally inherited. In this part, 243 full mtDNA and 157 W chromosome samples were analysed. The mtDNA samples included three countries (Iraq, Ethiopia and Saudi Arabia), while the W chromosome samples included just two (Iraq and Ethiopia), as only data from males were available for Saudi Arabian samples. As expected, the full mtDNA sequence data analysis provided us with more polymorphisms and more evidence for the presence of two routes of migration, terrestrial and maritime. In particular, for Ethiopia, it indicates that different populations may have witnessed different histories. It also shows a greater resolution of genetic diversity at the population level and suggests a decline in effective population size following an expansion in two countries (Iraq and Ethiopia). In contrast, data from the W chromosome had low variation to add any information on the origin of samples and their genetic diversity level. But we did observe some unexpectedly divergent haplotypes in some Ethiopian populations, which require further investigations. In Chapter 4, 315 whole-genome sequences of domestic chickens from three countries (Iraq, Ethiopia and Saudi Arabia) were used together with genome sequence information of four Gallus species (Ceylon, Green, Grey and Red junglefowl) and the common pheasant as an outgroup, to detect signals of introgression in domestic chicken. We also aim to assess if markers of introgression may help us to understand the history of the domestic chicken. The results showed no sign of gene flow from Ceylon and Green junglefowl into village chicken populations examined here. In contrast, there were many identified candidate genome regions of gene flow between Grey junglefowl and the domestic chicken populations. Building on previous work, six candidate introgressed genomic regions were further investigated. They all show evidence of Grey junglefowl introgression within domestic chicken as well as signs of gene flow in the opposite direction. These regions have different frequency levels of introgression in each country and also within each country. The highest level of gene flow is present in the north, central-east and western parts of Ethiopia, while the lowest levels of introgression were observed in Iraq, southern Ethiopia and Saudi Arabia. This variation in gene flow frequencies provided us with new information regarding the past movement of chicken into Africa and, in particular, led us to conclude that the chicken diversity observed in Ethiopia today were brought from the southern part of the Indian subcontinent, while the ones from Iraq and Saudi Arabia originate from the Northern part of the Indian subcontinent. In conclusion, the results presented here strongly advocate the use of both full mitochondrial DNA sequence information and markers of introgression to unravel the past history of the domestic chicken. However, the information obtained can only provide a window on such history, they allow us to build hypothesis which may be further investigated through the analysis of more populations over large geographic areas and, as much as possible, ancient chicken DNA studies