Crucial selective horse-breeding decisions around 3000 years ago are most likely responsible for the lack of variability in DNA inherited down the male line, according to researchers.
Researcher Saskia Wutke and her colleagues from a range of European institutions say selective breeding just before and during the Iron Age is likely the reason for the lack of variability through male lines – a trait unique among livestock animals.
Their finding challenges the current assumption that high maternal DNA diversity and low paternal DNA diversity in modern horses is generally explained by unequal sex ratios – many mares and few stallions – at the beginning of horse domestication.
The estimated 56 million horses around the world today are immensely diverse in their maternally-inherited mitochondrial DNA.
Yet, modern horses show very little variation on their paternally inherited Y chromosome, a curious finding since recent studies suggest that Y chromosomal diversity among horses was much larger in the past.
When and why this diversity disappeared remains controversial, as does any possible influence of the horse domestication process.
For their research, the study team genotyped 16 Y chromosomal single-nucleotide polymorphisms in 96 ancient Eurasian stallion remains spanning roughly the last 5000 years (from the early domestication stages – Copper and Bronze Ages – to the Middle Ages).
This data set provides the first full-time series of Y chromosomal variation from early domestication stages until the Middle Ages.
Their results showed that lack of paternal diversity appeared to begin in the Late Bronze Age about 3500 years ago – a time when large-scale human migrations required horses for transportation – and became even more noticeable during the Iron Age.
Through several additional analyses, the authors found that deliberate selection for, or rejection of, certain stallions imposed by humans in breeding processes can explain the loss of paternal diversity.
Additionally, when the dominant stallion lineage that is present in modern horses took hold during the Iron Age, the Roman Empire changed the mode of animal breeding by shifting the focus from female-based to male-based selective breeding, which likely increased the reproductive success of a few selected stallions, and thus their lineages.
The researchers found that one particular haplotype – a set of genetic determinants located on a single chromosome – progressively replaced all other haplotypes except for one additional lineage restricted to Yakutian horses.
The trend in paternal diversity toward dominance of the modern lineage through this haplotype, dubbed Y-HT-1, appeared to start in the Bronze Age and became even more pronounced during the Iron Age.
“The Bronze Age was a time of large-scale human migrations across Eurasia, movements that were undoubtedly facilitated by the spread of horses as a means of transport and warfare.
“At that time, the western Eurasian steppes were inhabited by highly mobile cultures that largely relied on horses.
“The genetic admixture of northern and central European humans with Caucasians/eastern Europeans did correlate with the spread of the Yamnaya culture from the Pontic-Caspian steppe, an area that has repeatedly been suggested as the center of horse domestication.
“Given the importance of domestic horses, it appears that deliberate selection/rejection of certain stallions by these people might have contributed to the loss of paternal diversity.
“The spread of humans out of this region might also have resulted in the spread of Y-HT-1 from Asia to Europe.”
This scenario, they said, also agreed with recent findings that the low male diversity of modern-day horses was not caused by recruiting only a limited number of stallions during early domestication.
They said the fact that horses were basically fixed for Y-HT-1 already at the beginning of the Middle Ages would have prevented other haplotypes from rising again during medieval times.
Decline of genetic diversity in ancient domestic stallions in Europe
Saskia Wutke, Edson Sandoval-Castellanos, Norbert Benecke, Hans-Jürgen Döhle, Susanne Friederich, Javier Gonzalez, Michael Hofreiter, Lembi Lõugas, Ola Magnell, Anna-Sapfo Malaspinas, Arturo Morales-Muñiz, Ludovic Orlando, Monika Reissmann, Alexandra Trinks and Arne Ludwig.
Science Advances 18 Apr 2018: Vol. 4, no. 4, eaap9691, DOI: 10.1126/sciadv.aap9691