Review article
Domestication of the horse: Genetic relationships between domestic and wild horses

https://doi.org/10.1016/j.livsci.2008.03.002Get rights and content

Abstract

To date, a large amount of equine genetic data has been obtained regarding (i) extant domestic horses of various breeds from all over the world, (ii) ancient domestic horses, (iii) the extant Przewalski's wild horse, and (iv) the late Pleistocene wild horse from Eurasia and North America. Here, a review of mtDNA and Y chromosome marker analyses is presented in the context of horse domestication. High matrilineal (mtDNA) diversity, which can be found in both extant and ancient (domestic and wild) horses, has suggested that a high number of wild (and tamed) mares were domesticated. Alternatively, Y chromosome marker analysis revealed a single haplotype in all domestic horses analyzed; interestingly even a small population of extant Przewalski's wild horses showed two different Y chromosome haplotypes. It seems that an extreme male population bottleneck occurred due to domestication, while reduction in the female population was only moderate, leaving about 100 distinct haplotypes. For this reason, we speculate that domestication might have started when the appropriate stallion was found or was obtained by selection. Perhaps it had some unusual but special characteristics which could have accelerated the process of domestication. We doubt that only a single Y chromosome haplotype will be found in present-day domestic horses if there are no important differences between the founder stallion/s and the other stallions that were not included in the domestication. In the Eneolithic, tamed and wild mares have probably been spread all over Eurasia, although the number of animals was most likely very low and the populations were limited to a restricted area (e.g., taming centers). Only two subspecies of wild horses (Tarpan and Przewalski's wild horse) have survived up to recently. During the further process of domestication, mares (tamed or wild) were preferentially crossed to stallions having more desirable characteristics. We assume that mares from different regions varied in their morphology due to adaptation to their local environmental conditions. These data might explain rapid expansion of horse populations, as well as their rapid differentiation into various phenotypes during the early phase of domestication.

Introduction

During the late Pleistocene, large herds of wild horse were common on the open plains of Europe, Asia, and North America (Clutton-Brock, 1999). Evidence for the existence of wild horses in North Africa has also been found (Bagtache et al., 1984). By the end of the ice age, the range of all wild horses was very much reduced (Clutton-Brock, 1999). In North America, due to the climatic/vegetational shift, horses underwent a rapid decline in body size and became extinct around 10,500 BC (Guthrie, 2003). If humans played a role in their extinction, it occurred on top of other ecological changes (Guthrie, 2006). In Eurasia, only two subspecies of wild horses survived to historic times:

  • The Tarpan. Equus ferus ferus Boddaert, 1785. Synonyms: sylvestris Brincken, 1826; gmelini Antonius, 1912; silvaticus Vetulani, 1928 (Groves, 1986).

  • Przewalski's horse. Equus ferus przewalskii Poliakov, 1881. Synonyms: hagenbecki Matschie, 1903; typicus Hilzheimer, 1909; probably also equuleus Smith, 1841 (Groves, 1986).

The Tarpan (Fig. 1) was described in numerous references from the eighteen and nineteenth centuries as a small animal, having a mouse-dun coat with a light underbelly, sooty to black limbs from the knees and hocks down, a short, frizzled mane, and a tail with short dark hair (Olsen, 2006). Although the last Tarpan went extinct in Poland in 1918 or 1919, the only available skeletal material consists of one complete skeleton and a cranium lacking a mandible from another individual. There are many accounts of Tarpans stealing domestic mares and forming harems, thus many Tarpans may simply have been feral horses or hybrids (Olsen, 2006). Exmoor ponies of Britain which are often claimed to be directly descended from British Pleistocene stocks may also represent a population of feral ponies (Clutton-Brock, 1999).

Przewalski's horse (Fig. 2) would also be extinct today if a small number had not been captured in the Mongolian steppes in the first years of the 20th century and brought to Europe, where they have multiplied in zoos and wildlife parks (Clutton-Brock, 1999). Like the Tarpan, Przewalski's stallions were notorious for stealing mares from Mongol horse herds (Olsen, 2006). The karyotypes of a Przewalski's horse (2n = 66) and a domestic horse (2n = 64) differed by one Robertsonian translocation (ECA 5 = EPR23 + EPR 24); the direction of evolution – fusion or a fission – cannot be concluded (Benirschke et al., 1965, Ryder et al., 1978, Ahrens and Stranzinger, 2005). The hybrids (2n = 65), however, are fertile (Koulischer and Frechkop, 1966). Przewalski's horse is considered as a sister taxon of wild progenitors of domestic horses, mainly due to the differences in chromosome number. The existing populations of Przewalski's horses, however, are derived from very limited number of individuals, and only descendants of these animals were karyotyped. If a translocation occurred recently (i.e., up to several thousand years ago), some other Asian populations of Holocene wild horses might still have 64 chromosomes.

The questions of when, where and why horses were first domesticated, are still hotly debated. It is generally accepted that domestication should be considered a process that flows through our arbitrary classes of wild, captive, tame, and domesticated horses (Olsen, 2006). Horse-keeping, perhaps just for food, might have begun in a limited way in the European steppes during the Early Eneolithic, about 5000 BC, when horses were first included with cattle and sheep in graveside ritual deposits like those at Khvalynsk on the Volga river (Brown and Anthony, 1998, Anthony and Brown, 2000).

Horseback riding, which might be a good indicator of horse domestication, first appeared in the steppes east of the Ural Mountains. Here, bit wear (a dental pathology that occurs regularly among bitted horses) has been found on the lower second premolars (P2's) of at least four horses at the sites of Botai and Kozhai 1 in northern Kazakhstan, both dated around 3500-3000 BC (Brown and Anthony, 1998). It is possible that 85-90% of the horses butchered at Botai were never bitted. Perhaps the Botai hunters rode horses to hunt wild horses (Brown and Anthony, 1998, Anthony and Brown, 2000). Another indirect evidence for horse domestication was found in the way of circle and semicircular horse corrals that have been uncovered in Eneolithic Botai settlements (Olsen, 2006, Stiff et al., 2006). However, population structure analysis for Botai (the age and sex structure of horse populations) fit the hunting model (Levine, 2005). Levine (2005) suggested that horse taming probably first arose as a by-product of horse hunting for meat. Wild horses, particularly as foals, can be captured and tamed and, as such, ridden or harnessed and, at the end of their lives, if necessary, slaughtered and eaten. Considering the problems encountered by modern collectors trying to breed Przewalski's horses, it seems likely that horse-keeping would have had to have been relatively advanced before controlled breeding over successive generations, and thus domestication, would have been possible (Levine, 2005).

The earliest direct evidence for horse domestication – using dateable textual and artistic evidence – only dates back to the end of the third millennium BC (Levine, 2005). Evidence of horses in graves, accompanied by artifacts unambiguously associated with riding or traction, is even more recent, dating to no later than the beginning of the second millennium BC. By the middle of the second millennium, horses were widely used to pull chariots, e.g., in the Near East, Greece and on the Eurasian steppe (Levine, 2005).

Reduction in overall animal size on the one hand and an increase in variability on the other are classic indicators of domestication (Uerpmann, 1990). It seems, however, that domestication has little impact on the equine anatomy; there are no indisputable osteological differences between wild and domesticated horses (Levine, 2006). In addition, horse populations exhibited high variability throughout the Pleistocene into the post-Pleistocene (Levine, 2006). The systematic classification of the remains of wild horses from an enormous geographic area, say from Western Europe to Siberia, that includes a wide range of habitats and a long temporal span, is very difficult to perform. This is due in large part to the fact that in Quaternary horses, adaptive and non-adaptive traits combine to form a reticular pattern, a mosaic of characters that represent changes in different places and times (Eisenmann, 1996). Even within an assemblage from a single locality, multiple forms have been detected (Olsen, 2006).

The wild horses of the mid-Holocene varied naturally in size. The horses of the central Eurasian steppes in Kazakhstan were somewhat larger than those of the western steppes in central Ukraine, which were larger than those of the steppe/forest-steppe border in Western Ukraine and Romania. All the horses of the steppes were significantly larger than the pony-sized wild horses of central and Western Europe (Anthony, 2007). There is a range of variation in both wild and domestic animals, and concerning most characteristics, there is considerable overlap (Olsen, 2006). Nevertheless, the increase in variation that began about 2500 BC and continued thereafter has often been taken as an indicator of domestication, although increased variation is sensitive to sample size (Anthony, 2007).

By 1500 BC during what would have been the early phase in the domestication of the horse, there seems already to be definition into northern pony and Arabian types (Clutton-Brock, 1999). One group consisted of the small “Celtic” ponies of Britain, Western Europe and Greece, while the second group consisted of larger horses from Scythia and the Russian steppes (Clutton-Brock, 1999). “Celtic” ponies were very small, some being less than a meter high at the withers; the Scythian horses were characteristically large and resembled Arabian horses in their conformation (Clutton-Brock, 1999).

Two models of horse domestication have been suggested (Clutton-Brock, 1999):

  • Model I

  • The wild stock, from which all domestic horses were bred, inhabited the plains of southern Russia, from the Ukraine to the region of Turkestan. The earliest domesticated horses spread out from this arc and all the different types and breeds of horses that are known today were developed as a result of artificial selection in combination with natural selection for adaptation to local environmental conditions.

  • Model II

  • The alternative model is based on the possibility that there was a geographical cline in the population of wild horses: those in the northern part of the range being smaller and sturdier than those found in the south. The reason for believing this is that even in the earliest findings of the domestic horse there are considerable differences in the size and proportions of the bones from different regions.

Recent research suggests, however, that the natural distribution of the Holocene horse was much wider than what has been formerly believed, particularly in Western and central Europe (Levine, 2005). Neolithic remains from putatively wild horses have, for example, been found in Sweden, Denmark, the Netherlands, France, Spain, Italy, Germany, Switzerland, Hungary and Serbia – in addition to Ukraine, Russia and Kazakhstan. These results are underlying the assumption that the earliest domestication must have taken place in Eastern Europe or central Asia. The fact that wild horses were more common in those regions does not definitely prove that they were first domesticated there (Levine, 2005).

According to Levine (2005), horse domestication would have taken a relatively long time to develop and might well have been dependent upon arbitrary genetic changes that would have predisposed some horses to breed in captivity. Even if the earliest assays into domestication had been relatively restricted – either temporally or spatially – until their extinction, wild horses could, and probably would have been introduced into domestic herds (Levine, 2006). Historical records of horses, described as wild, in Eurasia – in the post Iron Age – do suggest that they were widely distributed at least until the medieval period. Thus wild genes could have been introduced into domestic stock until relatively recent times (Levine, 2006).

Section snippets

Genetic data

In horses, three types of genetic data have been studied extensively during the last decade:

  • Nucleotide sequences of mitochondrial DNA (mtDNA), which can be used for the reconstruction of past events regarding female populations

  • Y chromosome markers (nucleotide sequences, microsatellites and single-nucleotide polymorphisms (SNP)) - for reconstruction of past events in male populations

  • Microsatellites of nuclear autosomal DNA - for estimation of the relationship (or the differentiation) among horse

mtDNA markers

Due to the maternal inheritance of mtDNA and lack of recombination, mtDNA has been widely used for studying the history of maternal lines. If no mutations occur, progeny show the same mtDNA nucleotide sequence (haplotype or mtDNA type) as their mother. Occasionally, mutations occur and become fixed in the maternal (female) lines. By examining these mutations, we can follow distinct maternal lines back into the population history (Fig. 3). The majority of mtDNA genetic data concern the

Y chromosome markers

Y chromosome markers are specific for males and therefore have been widely used to examine patrilineal relationships. In domestic horses, stallion lines have been studied by three, highly polymorphic sets of markers: Y-specific sequence (Wallner et al., 2003), microsatellite loci (Wallner et al., 2004) and SNPs (Lindgren et al., 2004). A single haplotype was detected by examining Y-specific sequences (Wallner et al., 2003) and by genotyping six Y chromosome-specific microsatellite loci in 49

Reconstruction of the process of horse domestication

All extant domestic horses can be traced back to one founder stallion, or to closely related stallions having the same Y haplotype (Lindgren et al., 2004). Therefore the presence of low patrilineal and high matrilineal diversity might suggest that the process of horse domestication (not taming) started when the “appropriate male” was found or obtained by selection. Perhaps it had some unusual special characteristics which could accelerate the process of domestication. We doubt that only one Y

Acknowledgements

The authors would like to acknowledge three anonymous reviewers and Dr. Simona Sušnik for useful comments. Thanks to the late Dr. Ann T. Bowling, who encourage us at the beginning of our work on horse genetics.

References (53)

  • Clutton-BrockJ.

    A natural history of domesticated mammals

    (1999)
  • Di BernardoG. et al.

    Genetic characterization of Pompeii and Herculaneum Equidae buried by Vesuvius in 79 AD

    J. Cell. Physiol.

    (2004)
  • EisenmannV.

    Quaternary horses: possible candidates to domestication

  • FelsensteinJ.

    PHYLIP (Phylogeny Inference Package) version 3.6

    (2005)
  • GrovesC.P.

    The taxonomy, distribution and adaptations of recent Equids

  • GuthrieD.

    Rapid body size decline in Alaskan Pleistocene horses before extinction

    Nature

    (2003)
  • GuthrieD.

    New carbon dates link climatic change with human colonization and Pleistocene extinctions

    Nature

    (2006)
  • HigginsD. et al.

    CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice

    Nucleic Acids Res.

    (1994)
  • IshidaN. et al.

    Polymorphic sequence in the D-loop region of equine mitochondrial DNA

    Anim. Genet.

    (1994)
  • JansenT. et al.

    Mitochondrial DNA and the Origins of the Domestic Horse

    Proc. Natl. Acad. Sci. U.S.A.

    (2002)
  • KavarT. et al.

    Mitochondrial D-loop sequence variation among the 16 maternal lines of the Lipizzan horse breed

    Anim. Genet.

    (1999)
  • KavarT. et al.

    History of Lipizzan horse maternal lines as revealed by mtDNA analysis

    Genet. Sel. Evol.

    (2002)
  • KavarT. et al.

    Rodovi lipicancev slovenske reje glede na haplotip mitohondrijske DNK

    Acta agr. slov.

    (2004)
  • Keyser-TracquiC. et al.

    Mitochondrial DNA analysis of horses recovered from a frozen tomb (Berel site, Kazakhstan, 3rd Century BC)

    Anim. Genet.

    (2005)
  • KimK.I. et al.

    Phylogenetic relationships of Cheju horses to other horse breeds as determined by mtDNA D-loop sequence polymorphism

    Anim. Genet.

    (1999)
  • KimuraM.

    A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences

    J. Mol. Evol.

    (1980)
  • Cited by (45)

    • Konik, Tarpan, European wild horse: An origin story with conservation implications

      2021, Global Ecology and Conservation
      Citation Excerpt :

      It is likely that such a reproductive behavior added to the extent of gene flow between domestic and wild horses. Further, since horses are very mobile animals, considerable displacements must have been characteristic of wild populations (Kavar and Dovč, 2008). Such mobility results in gene flow, which may partly explain the lack of phylogeographic structure found in the mitochondrial DNA of current domestic horses (Kavar and Dovč, 2008).

    • Aspects of Breeding Stallion Management with Specific Focus on Animal Welfare

      2021, Journal of Equine Veterinary Science
      Citation Excerpt :

      Approximately 5000 years ago, the horse was domesticated [11,14,15]. Initially serving as a source of milk, meat, and leather [16,17] the horse was subsequently transferred to the function of pulling loads, being stronger and faster than a bovine [18]. As time went by, humans realized that they could accommodate horses and use them for support in the day-by-day work [11].

    • Impacts of Feral Horse Use on Herbaceous Riparian Vegetation within a Sagebrush Steppe Ecosystem

      2017, Rangeland Ecology and Management
      Citation Excerpt :

      During the Pleistocene, the range of a variety of species of wild horses (Equus sp.) covered much of Europe, Asia, North America, and perhaps North Africa (Kavar and Dove, 2008).

    • The Trojan Horse reconstruction

      2015, Mechanism and Machine Theory
    View all citing articles on Scopus
    View full text