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.