Origin and history of mitochondrial DNA lineages in domestic horses

Abstract

Domestic horses represent a genetic paradox: although they have the greatest number of maternal lineages (mtDNA) of all domestic species, their paternal lineages are extremely homogeneous on the Y-chromosome. In order to address their huge mtDNA variation and the origin and history of maternal lineages in domestic horses, we analyzed 1961 partial d-loop sequences from 207 ancient remains and 1754 modern horses. The sample set ranged from Alaska and North East Siberia to the Iberian Peninsula and from the Late Pleistocene to modern times. We found a panmictic Late Pleistocene horse population ranging from Alaska to the Pyrenees. Later, during the Early Holocene and the Copper Age, more or less separated sub-populations are indicated for the Eurasian steppe region and Iberia. Our data suggest multiple domestications and introgressions of females especially during the Iron Age. Although all Eurasian regions contributed to the genetic pedigree of modern breeds, most haplotypes had their roots in Eastern Europe and Siberia. We found 87 ancient haplotypes (Pleistocene to Mediaeval Times); 56 of these haplotypes were also observed in domestic horses, although thus far only 39 haplotypes have been confirmed to survive in modern breeds. Thus, at least seventeen haplotypes of early domestic horses have become extinct during the last 5,500 years. It is concluded that the large diversity of mtDNA lineages is not a product of animal breeding but, in fact, represents ancestral variability.

Figure 1. Median-joining network based on 247 bp of the mitochondrial D-Loop from 207 ancient samples (colored) and 601 modern sequences of primitive breeds (white).

Eighty-seven haplotypes were found among the ancient samples; 103 different haplotypes among the primitive breeds and 36 haplotypes are shared (Table S5). Figure 1A shows haplotypes named after –, whereas Figure 1B shows the new nomenclature (Table S4). Haplogroups are signed by a color code.

Figure 2. Origin of mitochondrial lineages of modern horses.

Only mitochondrial lineages are shown which were/are present in domestic horses. Haplotypes in italic/underlined were so far only found in early-domestic remains. The striped zone indicates the postulated period of horse domestication.

Figure 3. Haplogroup distribution of Eurasian primitive breeds (n = 601 animals; Table S13).

(1: Asturcon (n = 12), Cartujano (n = 8), Garrano (n = 5), Losino (n = 10), Lusitano (n = 10), Marismeno (n = 12), Merens (n = 10), Pottoka (n = 13), Sorraia (n = 27); 2: Duelmener (n = 10), Exmoor (n = 17), Gotland (n = 3), Icelandic (n = 6), Norwegian Fjord (n = 11), Shetland (n = 18), Welsh (n = 1); 3: Arabian (n = 99), Barb (n = 37), Fulani (n = 9), Egyptian (n = 7); 4: Hucul (n = 11), Koonik (n = 5); 5: Anatolian (n = 17), Giara (n = 2), Mallorquina (n = 2), Pindos (n = 7), Sanfrantellano (n = 10), Sicilian Oriental (n = 1), Sicilian Ind. (n = 13), Skyros (n = 5); 6: Akhal Teke (n = 37), Caspian (n = 13), Vyatskaya (n = 18); 7: Tuva (n = 10); 8: Mongolian (n = 20), Przewalski (n = 2); 9: Debao (n = 24), Guan Mountains (n = 10), Guanzhong (n = 2), Wenshan (n = 2), XiNeHe (n = 1), Dali (n = 6), Yunnan (n = 1), Tibetan (n = 16); 10: Cheju (n = 25), Taishu (n = 2); 11: Yakut (n = 15)).

Figure 4. Mismatch distribution of mitochondrial haplotypes indicating population expansion (domestication) for all regions excluding Iberia during 3000 BC–600 AD.

Figure 5. This figure illustrates the chronology of geographic haplogroup distribution.

Size of circles represents haplogroup frequencies.