In mammals the male-specific region of the Y chromosome (MSY) is passed from father to sons without recombination. As a result it reflects the migratory and demographic history of males. Due to this is it possible to compare the demographic history of males and females using the mitochondrial DNA as the female counterpart. A clear contrast can be seen between the demographic histories of the two sexes when this is applied to the horse. The MSY shows extremely low diversity in the horse in contrast to that of the female mtDNA.
The low MSY diversity cannot be explained by a low mutation rate, as the Y chromosome lineages of modern horses are distinct from those of the Przewalski’s horse. The presence of only 6 Y chromosome haplotypes in modern horses breeds does suggest an extremely low effective population. A genetic bottleneck during the domestication process about 5,500 years ago is a likely cause of the lack of Y chromosome diversity. Subsequently, most ‘modern horse breeds’ are the result of centralised and organised horse breeding over the past few hundred years. The entire horse population has also been strong affected by the popularity of inbreeding and line-breeding concepts during this period.
A particularly important trend in the history of the Y chromosome is the import of foreign stallions to improve local herds with started in Europe in the 16th century. The European horse population was influenced by the introduction of ‘oriental stallions’ up until the end of the 18th century, in particular Turkoman stallions, from the steppes of central Asia, and Arabian stallions from the Arabian Peninsula. The English Thoroughbred resulted in a peak in stallion mediated improvement in the 19th and 20th century. The studbook of the English Thoroughbred has been closed since 1793. It was founded through the introgression of oriental stallions which were bred to local mare. The breeding history of the English Thoroughbred has led to only a small number of founder lineages remaining in modern horse breeds.
The work carried out by Wallner et. al, was undertaken to resolve the first Y chromosome genealogy of modern horses by screening a 1.46 Mb of the MSY in 52 horses from 21 breeds. Wallner et. al, estimated the de novo mutation rate of the horse MSY and showed that various modern horse Y chromosome lineages split much later than the domestication of the species. Wallner et. al, aimed to unravel the origin of influential founder stallions and to determine their genetic influence on modern horse populations by using high-resolution MSY haplotyping. Wallner et. al, show that the English Thoroughbred MSY was derived from the Turkoman lineage and that English Thoroughbred stallions are largely responsible for the predominance of the Turkoman haplotype in modern horses.
Methods and Results
Wallner et. al, generated a horse MSY reference sequence and then used it for variant calling using short-read data from multiple individuals. Wallner et. al, enriched for male-specific reads by mapping paired-end Illumina reads from the genome of three male Lipizzan stallions to the published female horse reference to generate the reference sequence. A de novo assembly of all unmapped reads was then carried out by Wallner et. al and contigs with a total length of 13.6 Mb was obtained. To extract male specific sequences filtering criteria were applied. Wallner et. al mapped Illumina reads from 27 males of different breeds and from 5 females to the de novo assembled contigs and obtained 2,794 preliminary MSY contigs covering 1.67 Mb. 100% of the MSY contigs were found to be male-specific when Wallner and colleagues scrutinised their work.
To detect MSY variants, Wallner et. al mapped whole-genome next-generation sequencing data from 52 domestic male horses from 21 different breeds to the nonrepMSY reference and used a Przewalski’s horse and donkey as outliers. In total 53 domestic and 284 Przewalski’s horse variants were categorised as ‘true’ variants after passing several filtering steps.
Wallner et. al then constructed a maximum-parsimony tree based on inferred domestic horse haplotypes using the Przewalski’s horse and donkey sequence as outgroups. Two deep splits in the MSY ancestry were observed with separated northern European samples into two well-supported branches; one for Shetland pony and Norwegian Fjord horse and the other for Icelandic horse. A crown group was defined by two sequences variations, within which Wallner et. al observed a polytomy with four branches (A, L, S and T). Included in branch A were the Arabian horse, two Arabian-influences Trakehner stallions, a south German draft horse and Connemara ponies. Branch L and S covered Iberian stallions including Lipizzan sire lineages and a Sorraia male. Branch T contained more than two-thirds of the sample used by Wallner et al, of which all have documented English Thoroughbred parental ancestry, except the Franches-Montagnes. Wallner et al found that nucleotide diversity was extremely low between all the samples, which suggests a recent common ancestor for all the haplotypes. Wallner et all assumed a mean generation time of 7 years, which suggests that the most recent common ancestor of the crown group dates to 647 ± 229 years ago and that the entire tree consolidated about 1,328 ± 380 years ago.
Maximum-Parsimony Tree of the Horse MSY for 52 Individuals
Wallner et al then evaluated the MSY haplotype distribution by genotyping 56 MSY variants from 363 males representing 57 modern breeds to see whether the observed phylogeny covers the male breeding stock of modern breeds. Wallner et all used a pedigree-based sampling strategy to cover the influential lines of a given breed and to avoid oversampling of relatives. Even in the larger samples, Wallner et al show the haplotypes N and I were restricted to northern European breeds and that all remaining modern horse breeds cluster within the A-L-S-T crown group.
MSY markers specific to particular founder lines can be used to identify the origin of founder studs and to determine their influence on the global horse population and Wallner et al used this to show that the English Thoroughbred MSY was derived from the Turkoman lineage. While the sub-branches of Tb can be attributed to English Thoroughbred stallions, the basal haplotype Tb was also found in breeds with no documented English Thoroughbred influence. Wallner et all extended their sample to identify the origin of Tb. Wallner et al found that Tb is the most frequent haplotype among 78 Akhal-Teke males, and so believe that Tb is likely to be of Turkoman origin. The presence of Tb in many European breeds with no documented influence of Turkoman stallions shows their influence. This also corresponds to the geopolitical development of the region.