Naveed Khan: The genomic origins of modern horses revealed by ancient DNA: from early domestication to modern breeding

Naveed Khan’s PhD thesis may have upended previous theories (see David Anthony’s The Origin of Horseback Riding that horse domestication began in the Botai culture or even earlier in the Sredni Stog culture. His study concluded:

The ancient DNA work presented in this thesis led to many important discoveries regarding the origin and process of horse domestication, highlighting the power of multi-disciplinary lines of evidence in deciphering highly controversial and complex evolutionary processes. The major discoveries made in this study are:
1) Botai domestic horses only marginally contributed to the genetic makeup of modern domesticates (~2-3% of their overall genomic ancestry), and hence the latter are unlikely descendants of the earliest domestic horses known to the archaeological record (Outram et al., 2009). Therefore, the demic domestic expansion model, positing a single population expansion of domestic horses from Yamnaya to Afanasievo cultures (Anthony, 2007) through Botai cannot
be considered as valid. It is noteworthy that an independent ancient genomic study on humans, including individuals from both the Yamnaya and Botai cultures, also failed to retrieve any significant Yamnaya-related ancestory amongst Botai herders (de Barros Damgaard et al., 2018).
Altogether, this suggests that horses were ultimately re-domesticated in a second, independent centre, or that extensive introgression with local wild populations took place as the population expanded from the initial Botai-related domestication centre. Further work is needed to disentangle both scenarios.
2) Previously thought as only surviving true wild horse, the Przewalski’s horse, actually represent the feral descendants of Botai related domestic horses. However, D-statistics in the form of (outgroup, E. lenensis; modern domesticates, Botai horses) are balanced while those in the form
of (outgroup, E. lenensis; modern domesticates, Przewalski’s horses) are not. This indicate that significant shift in the ancestry of Przewalski’s horses took place during the feralization process, e.g. the introgression from another, yet un-identified, ghost population into the genome of Przewalski’s horse.
3) Ruling out Iberia as a major source for the genomic makeup of modern domesticates, despite previous suggestions based on paleo-climatic reconstructions, archeological data as well mtDNA and nuclear DNA studies from modern horse breeds (Jansen et al., 2002; Leonardi et al., 2018; Sommer et al., 2011; Warmuth et al., 2011).
4) A severe decline in autosomal nucleotide diversity took place in the last ~400 years and was accompanied by a ~16.4% median drop in individual heterozygosity within the last 200 years.
Together with the parallel increased mutational load detected, this indicates that the last few centuries of horse evolution and artificial selection mainly through close studs impacted overall levels of genetic diversity more than the previous five millennia of horse management.
5) Y chromosome diversity levels dropped down to the present-day levels after ~850-1,350 AD, which is compatible with the findings of another independent ancient DNA studies tracking the decline of Patrilineal diversity through time, although based on more-limited SNP information 159 (Wutke et al., 2018). This also echoes a study carried out by Wallner et al., 2017 showing that all
modern European stallion lines largely originated from a ~700-1,000 year-old, oriental haplogroup, and the growing influence of Persian like horses in European and Asian domestic horses detected after the 7th-9th century AD.
6) An archaic wild Siberian lineage, previously known as E. lenensis (Boeskorov et al., 2018) existed in Upper Paleolithic times and until around 5,000 years ago. Its range was not restricted to North Eastern Siberia, but also extended at least to South Western Siberia (i.e. the Tuva Republic). In contrast to earlier claims (Schubert et al., 2014), this lineage does not seem to have contributed significantly to the genetic makeup of modern domesticates.
Many of the findings listed above require further investigation before a complete understanding of the horse domestication process and recent evolutionary history can be fully understood. For instance, the now feral Przewalski’s horse still represents an important and unique source of morphological, behavioral and genetic attributes of past horse lineages. Therefore, ongoing conservative programmes should be re-inforced, regardless of its wild or feral status, and extra measures should be taken to prevent the most important threat in its reintroduction range, namely its dilution through cross-breeding with the numerically-dominant neighbouring domestic stocks. The finding that Botai domestic horses have not contributed significantly to the genetic makeup of modern horses also raises many questions, such as: were the horses also domesticated in independent domestication center(s)? On the contrary, could extensive admixture with local wild populations have virtually erased the Botai ancestry from the horse genome, after its spread out of Botai along with extensive Bonze Age populations’ movements (Allentoft et al., 2015;
Anthony, 2007; Anthony & Brown, 2011; Haak et al., 2015) (through a process called introgressive capture)? How many other, yet not sampled, ghost populations exist at the time of domestication and how many of these contributed, if at all, to the domestication process?
Answering such questions will require additional ancient DNA data from (and prior to) the 3rd millennium BCE and across the most likely geographic domestication candidates, mainly the Pontic Caspian steppes and Anatolia (Benecke, 2006a). Furthermore the extended range for the wild archaic Siberian lineage and the evidence for its survival well until after the time of domestication (Boeskorov et al., 2018), would require to screen currently not studied, domestic
horse population, specially the less focused non breed population, to see if they carry any possible introgression from this Siberian Archaic lineage.
These forthcoming ancient DNA studies on horses should be aimed at recovering whole genomes from high-quality samples whenever available, or at least genome-scale data through target-enrichment approaches (e.g. Haak et al. 2015, Cruz-Davalos et al. 2017), in case when DNA preservation is not sufficient (e.g. in the warm environments from Anatolia).