Discussion
One of the benefits of the current availability of WGS datasets is the
access to an abundance of sequence variants, which allow a comparison of
individuals or populations for several purposes. This is especially
useful for the analysis of Y-chromosomal diversity, which used to be
restricted by the availability of Y-chromosomal markers. The
male-specific part of the Y-chromosome constitutes the longest haplotype
in the mammalian genome and may serve as marker for mammalian paternal
lineages. Here, we combined the dataset of the VarGoats project with
published data and genotyped diagnostic SNPs in male goat samples from
several sources.
The Y-chromosomal phylogeny of wild and domestic goats is in agreement
with the Y-chromosomal tree on the basis of AMELY and ZFYgene fragments (Pidancier et al. 2006) and with a phylogeny of WGS
sequences (Grossen et al., 2020; Cai et al., unpublished). MtDNA trees
confirm the close relationship of markhor (Capra falconeri ) with
bezoar and domestic goat, but do not show the separation of these
species and the other wild goats. In addition, mitochondrial DNA (mtDNA)
sequences of some, but not all East-Caucasian turs (Capra
cylindricornis ) cluster with the mtDNAs of markhor, bezoar and domestic
goat, illustrating a separate history of maternal and paternal lineages
in cross-fertile species (Chen et al., 2018; Marín et al., 2017;
O’Connell et al., 2014; Zhang et al., 2020; Zhang et al., 2016).
On the basis of WGS data, Zheng et al. (2020) and Xiao et
al. (2021) reproduced the divergence of the domestic Y1 and Y2
haplogroup previously found on the basis of SNPs within or near
Y-chromosomal genes (Lenstra et al., 2005). Here we report a further
differentiation of haplogroups, resulting in a phylogeny supported by a
largely independent preliminary dataset (Fig. S1) and two phylogenetic
algorithms. We found that the major haplogroups corresponds with
haplotypes defined by SNPs (Çinar Kul et al., 2015; Lenstra & Econogene
Consortium, 2005; Pereira et al., 2009; Tabata et al., 2018, 2019; Vidal
et al., 2017; Waki et al., 2015), but Y1A haplotypes belong to either
haplogroup Y1AA or haplogroups Y1AB.
The phylogeny also indicates that these haplogroups diverged after the
split of the markhor and the cluster of the wild bezoar and the domestic
goats. The domestic goats and the two bezoar populations from Anatolia
and Iran do not share haplotypes, whereas the bezoar haplotypes are
attached to deep nodes in the tree of domestic haplotypes. This suggests
an absence of male gene flow between the bezoar populations and between
the bezoar and domestic goats from the same region. Thus, domestic
goats, which possibly were derived from bezoar populations not sampled
in this study, maintained their paternal lineages during the migration
from the Fertile Crescent via Anatolia to Europe, this in spite of
indications of management of wild goats in central Anatolia (Stiner et
al., 2022).
Geographic plots of domestic haplogroup frequencies show a considerable
spatial differentiation, which resonates with the strong phylogeography
displayed by autosomal SNPs (Colli et al., 2018), but is in clear
contrast with the weak phylogenetic structure displayed by the major
mtDNA haplogroups (Luikart et al., 2001; Naderi et al., 2007, 2008; Zhao
et al., 2014b, 2014a, Colli et al., 2015). Remarkably, Y-chromosomal
haplotypes from all five haplogroups have been found in ancient DNA
samples from Southwest Asia or Southeast Europe. The locations of
ancient Y1AA, Y1B and Y2B samples are well outside the range of the
corresponding domestic haplogroups (Fig. 3). This indicates that during
the Neolithic and later worldwide migrations a series of bottlenecks and
expansions in the domestic male lineage created a strong geographic
differentiation of the haplogroup distribution (Fig. 4):
- The dominance of haplogroup Y1B in central and northern Europa may
very well reflect population bottlenecks during the Neolithic
introduction of agriculture via the Danube route (Cymbron et al.,
2005; Rivollat et al., 2015; Tresset & Vigne, 2007)
- Y2A and Y1AA are almost the only haplogroups in Africa south of the
Sahara. The two African Y1AA haplotypes are related to those of Asian,
indicating that only Y2A expanded during the first introduction of
domesticated goats in central and southern Africa
- Y2B has been found in two Neolithic Iranian samples whereas related
CaYB2 haplotypes are present in Iranian and Anatolian bezoars.
However, by population bottlenecks during the global spreading of
domestic goats Y2b now only occurs in Asia east of the Indus River and
in one goat from Madagascar (see below).
- Y1AA was found in Neolithic samples in southeast Europe, but now has a
low frequency in Europe. In Asia it expanded together with Y2B and
later came to South Africa when Asian goats were used to breed the
Boer goat (see below).
- Y1AB is the most frequent haplogroup in north China. The distributions
of Y1AB and Y1AA/ Y2B in East Asia correspond to ranges of the
north-Chinese cashmere goats and the small Southeast Asian ‘katjang’
type, respectively (Porter et al., 2016). This obviously reflects the
large difference of climate between northern and southern China, which
determined a similar distribution of taurine and indicine cattle.
These two types of cattle are supposed to have entered China via a
northern and southern migration route, respectively (Chen et al.,
2018; K. Zhang et al., 2020), which support the separate eastern
expansions of the Y1AB and Y1AA/Y2B goats, respectively.
Exceptions to these geographic patterns follow from close relationships
between haplotype from different continents, which are most likely
explained by later major introgressions. Interestingly, in the
phylogenetic trees and networks (Figs. 2 and S2) the Y2A haplotypes on
Madagascar are closely related to Asian haplotypes and one Diana goat
from northern Madagascar even has an eastern-Asian Y2B haplotype.
However, autosomal DNA shows that the Malagasy goats are more related to
the southern and eastern African continental goats (Colli et al., 2018;
Denoyelle et al., 2021). This parallels a recent finding that Malagasy
cattle combines Indian and admixed African zebu ancestry (Magnier et
al., 2022). The Malagasy language has an Austronesian origin, which
testifies the colonization of Madagascar by immigrants from southeastern
Asia about 500 CE. Thus, it is likely that these immigrants brought
Austronesian goats, cattle and possibly also other livestock from their
region of origin to Madagascar.
Other introgressions are more recent. The exceptional Y1AA and Y2A in
the English Anglo-Nubian is explained by the documented import during
the 19th century of Indian and African goats to
England. These served on the ships as source of milk and meat, but
surviving males were crossed with English goats, which resulted in the
emergence of a popular transboundary breed.
The worldwide popular Boer goat also is of mixed origin (Porter et al.,
2016; Vidal et al., 2017) and carries exclusively Y1AA haplotypes. This
breed is supposed to be a crossbred of local African and Indian goats,
possibly mediated by incrossing of Anglo-Nubian males (Porter et al.,
2016). The crossbred origin is consistent with the results of Colliet al. (2018): a separate phylogenetic position of the Boer
relative the other African and Asian goats and the K=3 pattern of
model-based clustering showing African and west-Asian ancestry. The
Indian ancestry is entirely in agreement with a close clustering of the
Boer and Pakistani Y1AA haplotypes (Figs. 1B and 2).
Subsequently, the Boer became itself a source of introgression. The same
Y1AA haplotypes are closely related to Y1AA haplotypes in local breeds
in Uganda, Malawi, Mozambique and Zimbabwe. In these countries
crossbreeding with Boer goats from Africa is popular because of its
excellent meat production (Banda et al., 1993; Garrine, 2007; Lu, 2011;
Onzima et al., 2018). Therefore, it is most likely that the Y1AA in
eastern and southern African goats originates from the Boer.
There were three out-of-range findings of Y1B, in the Ugandan Karamonja,
in the Korean native goat and in the indigenous goats kept on the
Chongmin Island in Shanghai. Because of the popularity of Swiss dairy
goats in both Uganda (NAADS, 2005) and Korea (Kim et al., 2019),
crossbreeding again is the most likely explanation. There are no data on
European admixture in the Chongmin goats (Gao et al., 2020). Thus,
exotic occurrence of Y chromosomal variants are direct and sensitive
indicators of admixture events, but are to be complemented with
quantitative admixture tests, such as model-based clustering, thef 3 and f 4 test or,
ideally, identification of introgressed segments across the genome.
The latter approach may also lead to clues on the phenotypic
consequences of the introgression via the identification of the admixed
genes (Chen et al., 2018; Lv et al., 2014; Wang et al., 2015; Zheng et
al., 2020). A more direct link with the Y-chromosomal variation would be
provided if this can be linked to male phenotypic traits, but even in
human genetics this has scarcely be investigated (Matsunaga et al.,
2021; Yang et al., 2018; X. Zhang et al., 2021). Breeds in which
different Y-chromosomal haplogroups occur may allow to study an
association of haplogroups with typically male traits such as male
fertility and dominance behavior. It would be interesting if
Y-chromosomal variants can be related to the climate or other
environmental features, because this would imply that the geographic
differentiation of the Y-chromosomal variation is driven by regional
adaptation.
Most introgressions described in this study contribute to the expansion
of popular breeds at the expense of the original local breeds. On the
one hand, depending on the extent of the gene flow this may decrease the
diversity of the genetic resources; on the other hand, it does not
necessarily disrupt the environmental adaptation, arguably one of the
most consequential components of the phenotypic repertoire. If properly
managed, admixture of productive breeds may also contribute to the
sustainable conservation of local populations and illustrates that
genetic diversity has never been a static phenomenon.
We conclude that the Y-chromosomal
variation of goats reveals bottlenecks, expansions and introgressions,
illustrating the power of Y-chromosomal markers for inferring the
genetic origin of mammalian populations.