Introduction
Goat (Capra hircus ), sheep (Ovis aries ), cattle (Bos taurus ) and pigs (Sus scrofa ) are four major livestock species, which after their domestication in southwest Asia about 10,000 BP (Larson & Fuller, 2014; Stiner et al., 2022) spread to all inhabited continents. Because of their relatively small size, sheep and goats were the earliest domesticates, but have become less important than cattle and pigs as suppliers of food. However, sheep and goat are suitable for extensive management by smallholders or hobby breeders with goats being favored in conditions of poverty (Peacock, 2005). Whereas the high-quality goat cashmere wool and mohair fibres do not attain the volume of sheep wool, the demand of goat milk and cheese has increased considerably since the 1960s (Dubeuf, Morand-Fehr, & Rubino, 2004; Miller & Lu, 2019). During the last four decades, this has doubled the global number of goats to around 1 billion heads (Utaaker, 2021), which now approaches the numbers for sheep and cattle (Hegde, 2019).
As for other livestock, genetic isolation, adaptation and selection have created numerous local goat populations, whereas a restricted number of high-performing breeds play a major role in the agricultural production. The genetic diversity of goat breeds has been studied extensively (Ajmone-Marsan et al., 2014; Amills et al., 2017; Deniskova et al., 2021; Zheng et al., 2020). This demonstrated for autosomal DNA a geographic partitioning of the diversity (Colli et al., 2018), which is in sharp contrast to similar studies of sheep (Belabdi et al., 2019; Ciani et al., 2020; Kijas et al., 2012), but has been confirmed by similarities of ancient and modern DNA samples from the same regions (Cai et al., 2020; Daly et al., 2018, 2021). However, the goat Y-chromosome as a marker for the paternal lineages has not yet been studied at a worldwide scale.
Because of its absence of recombination, the male-specific part of the mammalian Y-chromosomes is by far the longest haplotype that is stably transmitted across generations (Hughes et al., 2015). In many species, males have a relatively small male effective population size, which makes Y-chromosomal variants highly informative markers for paternal origin that generally show a much stronger phylogeographic differentiation than mitochondrial or autosomal variants. This is now widely exploited in population-genetic studies of humans (Batini & Jobling, 2017; Jobling & Tyler-Smith, 2017; Kivisild, 2017), cattle (Edwards et al., 2011; Ganguly et al., 2020; Xia et al., 2019), horse (Felkel et al., 2019; Wallner et al., 2017; Wutke et al., 2018), water buffalo (Zhang et al., 2016), sheep (Deng et al., 2020; Meadows & Kijas, 2009; Zhang et al., 2014), camel (Felkel et al., 2019), llamas and alpacas ((Marín et al., 2017) pigs (Choi et al., 2020; Guirao-Rico et al., 2018) and dogs (Natanaelsson et al., 2006; Oetjens et al., 2018).
A preliminary analysis of the Y-chromosomal diversity in European and Turkish goats defined the three haplotypes Y1A, Y1B and Y2, which had a strong geographic differentiation (Lenstra & Econogene Consortium, 2005). The same haplotypes were found in goats from Portugal and North-Africa (Pereira et al., 2009), Turkey (Çinar Kul et al., 2015), eastern and southern Asia (Waki et al., 2015; Tabata et al., 2018, 2019) and Switzerland and Spain (Vidal et al., 2017) with the additional haplotypes Y2B in east Asia, Y2C in Turkish Hair and Kilis goats, and Y1B2 as well Y1C mainly in Switzerland (Table S1). However, these haplotypes are based on a low number of SNPs in or near DDX3Y, SRY and ZFY and genotyping in a limited number of domestic goat breeds. Thus, it is not clear if the haplotypes represent major haplogroups or local variants or if other major haplogroups exist. Nor does it inform us on the Y-chromosomal variants that existed in the earlier domestic goats or in their wild ancestor, the bezoar (Capra aegagrus ) (Amills et al., 2017). Whole-genome sequences (WGSs), however, has confirmed the differentiation of the Y1 and Y2 haplogroups (Xiao et al., 2021; Zheng et al., 2020).
In this study, we used WGS data for a large panel of goat breeds (Denoyelle et al., 2021) to systematically characterize the SNP-level variation in the single-copy male-specific part of the caprine Y-chromosome. In addition, we determined the Y-chromosomal haplogroups in goats originating from several European, Asian or African countries, in ancient goat DNA samples and in the wild bezoar (Alberto et al., 2018; Cai et al., 2020; Daly et al., 2018, 2021; M. Zhang et al., 2014; Zheng et al., 2020). We sought to answer the following questions (1) How are the WGS- based haplogroups related to the previously reported haplotypes? (2) How are the domestic paternal lineages related to those of bezoars from Iran and Anatolia, respectively? (3) How strong is the phylogeographic structure of the caprine male lineages? (4) What does the pattern of diversity tell us about Neolithic and later migrations? (5) Can we also infer other gene flows between or within continents? Answering these questions will contribute to our understanding of the genetic background of the domestic goat, which is relevant for breed management and conservation.