The assembly of caprine Y chromosome sequence reveals a unique paternal phylogenetic pattern and improves our understanding of the origin of domestic goat

Abstract

The mammalian Y chromosome offers a unique perspective on the male reproduction and paternal evolutionary histories. However, further understanding of the Y chromosome biology for most mammals is hindered by the lack of a Y chromosome assembly. This study presents an integrated in silico strategy for identifying and assembling the goat Y-linked scaffolds using existing data. A total of 11.5 Mb Y-linked sequences were clustered into 33 scaffolds, and 187 protein-coding genes were annotated. We also identified high abundance of repetitive elements. A 5.84 Mb subset was further ordered into an assembly with the evidence from the goat radiation hybrid map (RH map). The existing whole-genome resequencing data of 96 goats (worldwide distribution) were utilized to exploit the paternal relationships among bezoars and domestic goats. Goat paternal lineages were clearly divided into two clades (Y1 and Y2), predating the goat domestication. Demographic history analyses indicated that maternal lineages experienced a bottleneck effect around 2,000 YBP (years before present), after which goats belonging to the A haplogroup spread worldwide from the Near East. As opposed to this, paternal lineages experienced a population decline around the 10,000 YBP. The evidence from the Y chromosome suggests that male goats were not affected by the A haplogroup worldwide transmission, which implies sexually unbalanced contribution to the goat trade and population expansion in post-Neolithic period.

Keywords: RH map; Y chromosome assembly; demographic history; goat; phylogenetic.

FIGURE 1

Identified scaffolds of the goat Y sequence. (a) AD ratios of X‐linked (blue), autosomal (red), Y‐linked (green), and unassigned scaffolds (black). (b) The enlargement of the box in (a), scaffolds below the threshold of 0.4 are classified as Y origin, and unassigned scaffolds are shown in black. (c) Identification of Y‐linked scaffolds through the YGS. Each dot represents one scaffold in all unplaced scaffolds. Red dots are scaffolds previously confirmed to be Y‐linked. Abscissa denotes the proportion of scaffold sequence not matched by female short reads; ordinate denotes scaffold size. The filtering cutoff was set to 90%. (d) The count of scaffolds identified by the AD ratio, the YGS, the similarity search, and the comparison of overlaps among all approaches

FIGURE 2

(a) The organization of the goat Y assembly. The assembly consists of two separate sections representing a low‐copy gene region and ampliconic and/or heterochromatic region. The single‐copy genes are blue, and the multicopy genes are gray. The haplotypes of 24 male bezoars, 67 male domestic goats, and five other male Capra species corresponding to the above organization are shown. The reference allele is blue and alternative allele is yellow. (b) The comparison of coverage of several major types of repetitive elements among the autosomes and Y sequences in cattle and goats. (c) The distribution and median size of protein‐coding genes

FIGURE 3

Population and relationship of goats based on the Y chromosome results. (a) The geographic map of 96 modern individuals, five outgroup samples were not shown due to the lack of geographic information. (b) The enlargement of the box in (a), exhibiting different distribution of two goat lineages, where lineage one is marked with a red triangle, and lineage two is marked with a red circle. (c) PCA constructed using Y SNP data. Colors reflect the geographic regions of sampling. Outgroup samples were not shown due to a high divergence from other goat samples

FIGURE 4

Phylogenetic tree of 96 modern goats. (a) Y chromosome haplotypes constructed using BEAST software. (b) mtDNA SNPs constructed using MEGAX software. Colors reflect the geographic regions of the samples

FIGURE 5

Comparison of Bayesian skyline plot for domestic goats using (a) Y SNP data (b) mtDNA sequence. The dark blue and red solid lines correspond to the Y chromosome and mtDNA median estimate of the effective population size (Ne). The shadow area shows the upper and lower limits of the estimation