4. Discussion
This study has used world-wide ancient and modern goat genomes to shed light on the evolutionary events that have shaped the present-day SWA goat populations, and to characterize adaptive introgression and genetic changes after domestication in this region. Descriptive findings from the ADMIXTURE, PCA and TreeMix analyses suggested an excess of allele sharing of SWA and EAFR populations. Furthermore, patterns of allele sharing in outgroup f 3, D and f b statistics confirmed that SWA samples have a higher genetic affinity with EAFR than with other Asian goat groups. By exploring the genetic affinities of ancient samples from northern and southern parts of IRN with those from different periods of Levant and also present-day EAFR, we observed a remarkable genetic continuity between individuals from Chalcolithic period of IRN (7100-5700 YBP) and Levant/EAFR groups. The geographic distance of EAFR and SWA is considerable, but the EAFR influence may very well reflect the influence of the more proximate goats from the Levant region or the Saudi-Arabian Peninsula, which were not sampled for this study.
The higher level of allele sharing between ancient samples from IRN and Levant in the Chalcolithic time period coincides with known transitions to more arid conditions in the Middle East during the period of 6.5–5 kyr BP (Sun et al. 2021). It also agrees with the high genetic continuity and reduced genetic differentiation of farmers from southern Levant (Israel and Jordan) and Zagros Mountains (Iran) (Harney et al. 2018, Lazaridis et al. 2016). Thus, we propose extensive gene flow from Levant lineages into SWA populations after domestication time, dating between ~7,000 and 5,000 YBP, which suggested a North-Eastern path of gene flow from Levant into eastern parts of the Fertile Crescent. Given that the timing of this gene flow concurrences with a wet-to-dry transition in western parts of IRN regions such as Lakes Zeribar and Mirabad (Sun et al. 2021), we hypothesize that changing precipitation patterns and temperature have favored the introgression of adaptive introgression genes from the Levant genetic resource into the SWA region. The same climate transition is proposed to have driven the migration of heat-resistant indicine cattle to SWA after 4,200 BP (Verdugo et al. 2019).
Recent studies support a major role of adaptive introgression in the evolution of livestock animals, acting during periods of range expansion and contraction (Bangs et al. 2018, Zheng et al. 2020). For example, it has been shown that introgression signals of alleles in olfactory-related genes from wild relatives are associated with climatic adaptation in domestic sheep (Cao et al. 2021). A recent study has reported that an introgressed locus, harbors the MUC6 gene, from West Caucasian tur-like species into domestic goat confers pathogen resistance (Zheng et al. 2020).
In the current study, the strongest signals of adaptive introgression implicated a skin pigmentation (KITLG ) on chromosome 5 region (Yang et al. 2018, Deng et al. 2018). This gene encodes the ligand for the receptor tyrosine kinase protein KIT, which plays essential roles in the development and differentiation of different cell types in the body, such as melanocytes, blood cells and germ cells (Graham and Takahashi 1993). A regulatory region of the human KITLG contains an enhancer that regulates expression of hair follicles (Guenther et al. 2014). Due to that the frequency of the adaptive KITLG alleles are fixed in Nubian ibex and nearly fixed in AFR-ASA populations, we demonstrate that this gene has likely been introgressed from this wild species. The Nubian ibex is distributed around the northern Africa and the Arabian Peninsula, geographically close to the goat domestication center in SWA. It inhabits in a dry, deserts environment with intense solar radiation and extreme ambient temperatures (Castelló et al. 2016, Chebii et al. 2020). As several hair/wool characteristics are directly related to heat loss and therefore improving the adaptive flexibility of livestock animals to extreme environmental conditions (McManus et al. 2020), we hypothesise that KITLG gene likely has played a role in the evolution of goat lineages in the SWA during past history.
Based on the results from haplotype analysis of KITLG -selected region, we suggest two possible scenarios to explain the high similarity between the haplotypes AFR-ASA and Nubia ibexes. The first hypothesis is that there has been introgression from Nubian ibex into the ancestral goat populations around the northeast African and Levant regions. This scenario is conceivable since we identified extensive ancient gene flow from Levant populations into SWA region. Furthermore, in this scenario, the high frequency of the adaptive KITLG alleles in west African goats could be explained by previously documented gene flow from North-eastern to the west and central parts of Africa continent during the Holocene times, which was closely related with the expansion of herders (Schlebusch 2019). A second possibility would be that there have been multiple separate introgression events between Nubian ibexes and domestic goats in different geographical regions. However, due to limited sample size in our study, this data does not allow any strong conclusions.