Authors Antoine Fages, Kristian Hanghøj, Naveed Khan, Alan K. Outram, Pablo Librado, Ludovic Orlando
Genome-wide data from 278 ancient equids provide insights into how ancient equestrian civilizations managed, exchanged, and bred horses and indicate vast loss of genetic diversity as well as the existence of two extinct lineages of horses that failed to contribute to modern domestic animals.
- Two now-extinct horse lineages lived in Iberia and Siberia some 5,000 years ago
- Iberian and Siberian horses contributed limited ancestry to modern domesticates
- Modern breeding practices were accompanied by a significant drop in genetic diversity
Fages et al., 2019, Cell 177, 1–17 May 30, 2019 ª 2019 The Author(s). Published by Elsevier Inc. https://doi.org/10.1016/j.cell.2019.03.049
Horse domestication revolutionized warfare and accelerated travel, trade, and the geographic expansion of languages. Here, we present the largest DNA time series for a non-human organism to date, including genome-scale data from 149 ancient animals and 129 ancient genomes (R1-fold coverage), 87 of which are new. This extensive dataset allows us to assess the modern legacy of past equestrian civilizations. We find that two extinct horse lineages existed during early domestication, one at the far western (Iberia) and the other at the far eastern range (Siberia) of Eurasia. None of these contributed significantly to modern diversity. We show that the influence of Persian-related horse lineages increased following the Islamic conquests in Europe and Asia. Multiple alleles associated with elite-racing, including at the MSTN ‘‘speed gene,’’ only rose in popularity within the last millennium. Finally, the development of modern breeding impacted genetic diversity more dramatically than the previous millennia of human management.
Part 2 of 4
The Choice of Stallions for Reproduction and Its Impact in the Last 2,000 Years
The Y chromosome diversity is extremely limited in modern horses (Lindgren et al., 2004) but was greater in the past (Librado et al., 2017; Lippold et al., 2011), indicating that specific stallion lines have become increasingly prominent. Previous work showed that this process started 900 BCE–400 CE, however, on the basis of only four polymorphic SNPs (Wutke et al., 2018). We thus leveraged our 105 stallions and the 1,500 orthologous polymorphic sites recovered at monocopy regions to gain further temporal resolution for this reduction in Y chromosome diversity (STAR Methods). We considered all past time intervals of 250 years represented by a minimum of 3 males in Asia and in Europe separately, to limit the impact of geographic structure. This revealed that Y chromosome nucleotide diversity (p) decreased steadily in both continents during the last 2,000 years but dropped to present-day levels only after 850–1,350 CE (Figures 2B and S2E; STAR Methods). This is consistent with the dominance of an 1,000- to 700-year-old oriental haplogroup in most modern studs (Felkel et al., 2018; Wallner et al.
(Figure 2A). However, diversity was larger in La Te` ne, Roman, and Gallo-Roman horses, where Y-to-autosomal p ratios were close to 0.25. This contrasts to modern horses, where marked selection of specific patrilines drives Y-to-autosomal p ratios substantially below 0.25 (0.0193–0.0396) (Figure 2A). The close-to-0.25 Y-toautosomal p ratios found in La Te` ne, Roman, and Gallo-Roman horses suggest breeding strategies involving an even reproductive success among stallions or equally biased reproductive success in both sexes (Wilson Sayres et al., 2014) 2017). Our data also indicate that the growing influence of specific stallion lines post-Renaissance (Wallner et al., 2017) was responsible for as much as a 3.8- to 10.0-fold drop in Y chromosome diversity.
We then calculated Y chromosome p estimates within past cultures represented by a minimum of three males to clarify the historical contexts that most impacted Y chromosome diversity. This confirmed the temporal trajectory observed above as Byzantine horses (287–861 CE) and horses from the Great Mongolian Empire (1,206–1,368 CE) showed limited yet larger-thanmodern diversity. Bronze Age Deer Stone horses from Mongolia, medieval Aukstaiciai horses from Lithuania (C9th–C10th [ninth through the tenth centuries of the Common Era]), and Iron Age Pazyryk Scythian horses showed similar diversity levels. (0.000256–0.000267) (Figure 2A). However, diversity was larger in La Te` ne, Roman, and Gallo-Roman horses, where Y-to-autosomal p ratios were close to 0.25. This contrasts to modern horses, where marked selection of specific patrilines drives Y-to-autosomal p ratios substantially below 0.25 (0.0193–0.0396) (Figure 2A). The close-to-0.25 Y-toautosomal p ratios found in La Te` ne, Roman, and Gallo-Roman horses suggest breeding strategies involving an even reproductive success among stallions or equally biased reproductive success in both sexes (Wilson Sayres et al., 2014).
Influence of Persian Lines Post C7th–C9th
We next tracked evidence for animal exchange between past cultures by mapping genetic variation through space and time. We included all samples belonging to a particular archaeological culture, as long as they collectively accumulated a minimal genome depth-of-coverage of 2-fold (n = 186, Table S5). TreeMix reconstructions (Pickrell and Pritchard, 2012) revealed that modern Shetland and Icelandic ponies were most closely related to a group of north European horses including pre-Viking Pictish horses from C6th–C7th Britain, Viking horses, and one C9th–C10th horse from Estonia (Saardjave) (Figure 3; STAR Methods). This is in line with the historical expansion of Scandinavian seafaring warriors in the British Isles and Iceland between the late C8th–C11th (Brink and Price, 2008). These horses formed a sister clade to mainland European horses spanning the Iron Age to the C7th and a number of cultures, including in the La Te` ne and (Gallo-) Roman periods. Other modern European native breeds (e.g., Friesian, Duelmener, Sorraia, and Connemara) were found to belong to yet another clade, first appearing in Europe at Nustar, Croatia in the C9th, but not present at that time in northern Europe (Aukstaiciai, Lithuania). This suggests the introduction of new domestic lineages to the south of mainland Europe between the C7th–C9th, a time strikingly coincident with the peak of Arab raids on the Mediterranean coasts, including Croatia (Skylitzes and Wortley, 2010). This, and the earliest identification of this clade within two Sassanid Persian horses from Shahr-I-Qumis, Iran (C4th–C5th), supports the growing influence of oriental bloodlines in mainland Europe following at least the C9th. Moving focus to Asia, steppe Iron Age Pazyryk Scythian and Xiongnu horses appear related to Karasuk horses, locally present in the Minusinsk Basin of South Siberia during the late Bronze Age (Mallory and Adams, 1997). This lineage of horses survived at least until the C8th in Central Asia at Boz Adyr, Kyrgyzstan. However, Mongolian horses from the Uyghur (C7th–C9th, Khotont_UCIE2012x85_1291) and the Great Mongolian Empire (C13th) clustered together with C9th horses from Kazakhstan (Gregorevka4_PAVH2_1192 and Zhanaturmus_ Issyk1_1143) within the group descending from the two Shahr- I-Qumis Sassanid Persian horses. Therefore, the population shift observed in Europe during the C7th–C9th was also mirrored in Central Asia and Mongolia.
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