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Abstract

Domestication entails control of wild species and is generally regarded as a complex process confined to a restricted area and culture. Previous DNA sequence analyses of several domestic species have suggested only a limited number of origination events. We analyzed mitochondrial DNA (mtDNA) control region sequences of 191 domestic horses and found a high diversity of matrilines. Sequence analysis of equids from archaeological sites and late Pleistocene deposits showed that this diversity was not due to an accelerated mutation rate or an ancient domestication event. Consequently, high mtDNA sequence diversity of horses implies an unprecedented and widespread integration of matrilines and an extensive utilization and taming of wild horses. However, genetic variation at nuclear markers is partitioned among horse breeds and may reflect sex-biased dispersal and breeding.
DOI: 10.1126/science.291.5503.474
, 474 (2001); 291Science
et al.Carles Vilà,
Widespread Origins of Domestic Horse Lineages
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during the study; and the personnel of Canadian Forces
Station Alert for logistical support. We are especially
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29 August 2000; accepted 6 December 2000
Widespread Origins of
Domestic Horse Lineages
Carles Vila`,
1
* Jennifer A. Leonard,
2
Anders Go¨therstro¨m,
3
Stefan Marklund,
4
Kaj Sandberg,
4
Kerstin Lide´n,
3
Robert K. Wayne,
2
Hans Ellegren
1
Domestication entails control of wild species and is generally regarded as a
complex process confined to a restricted area and culture. Previous DNA se-
quence analyses of several domestic species have suggested only a limited
number of origination events. We analyzed mitochondrial DNA (mtDNA) con-
trol region sequences of 191 domestic horses and found a high diversity of
matrilines. Sequence analysis of equids from archaeological sites and late
Pleistocene deposits showed that this diversity was not due to an accelerated
mutation rate or an ancient domestication event. Consequently, high mtDNA
sequence diversity of horses implies an unprecedented and widespread inte-
gration of matrilines and an extensive utilization and taming of wild horses.
However, genetic variation at nuclear markers is partitioned among horse
breeds and may reflect sex-biased dispersal and breeding.
The domestication of the horse has profoundly
affected the course of civilization. Horses pro-
vided meat, milk, and enhanced transportation
and warfare capabilities that led to the spread of
Indo-European languages and culture and the
collapse of ancient societies (1, 2). Horse re-
mains become increasingly common in archae-
ological sites of the Eurasian grassland steppe
dating from about 6000 years ago, suggesting
the time and place of their first domestication
(3–5). Two alternative hypotheses for the origin
of the domestic horse from wild populations
can be formulated. A restricted origin hypoth-
esis postulates that the domestic horse was de-
veloped through selective breeding of a limited
wild stock from a few foci of domestication.
Thereafter, domestic horses would have been
distributed to other regions. Under this hypoth-
esis, domestication is a complex and improba-
ble process requiring multigeneration selection
on traits that permit stable coexistence with
humans. Another alternative could be that
domestication involved a large number of
founders recruited over an extended time period
from throughout the extensive Eurasian range
of the horse. In this multiple origins scenario,
horses may have been independently captured
from diverse wild populations and then increas-
ingly bred in captivity as wild numbers dwin-
dled. Consequently, early domestic horses may
not represent a stock highly modified by selec-
tive breeding.
These two hypotheses for the origin of the
domestic horse make distinct predictions with
regard to genetic variation in maternally in-
herited mtDNA. The restricted origin hypoth-
esis predicts that mitochondrial diversity of
the horse should be limited to a few founding
lineages and those added subsequently by
mutation. In contrast, a multiple origins hy-
pothesis predicts diversity greater than that
typically found in a single wild population
and divergence among lineages that well pre-
cedes the first evidence of domestication.
Phylogenetic analysis of 37 different
mtDNA control region sequences from domes-
tic horses deposited in GenBank, 616 base pairs
(bp) in length (6), revealed at least six divergent
sequence clades (clades A to F, Fig. 1A). After
correcting for multiple hits and ignoring indels,
the mean divergence observed between se-
quences was 2.6% (range: 0.2 to 5%). The
average divergence between donkey (Equus
asinus) and horses was 16.1% (range: 14.3 to
19.1%). Assuming that horses diverged from
the lineage leading to extant stenoid equids
(zebras and asses) at least 2 million years ago
(Ma), as the fossil record suggests (7), or about
3.9 Ma, according to molecular data (8), we can
estimate an average rate of equid mtDNA se-
quence divergence of 4.1% or 8.1% per million
years. Therefore, modern horse lineages coa-
lesce at about 0.32 or 0.63 Ma, long before the
first domestic horses appear in the archaeolog-
ical record (4). Even clade D, having a more
recent coalescence time, has a mean sequence
divergence of 0.8% (range: 0.2 to 2.0%), which
predicts an origin at least 0.1 Ma. These results
show that domestic horse lineages have an an-
cient origin. Thus, given the 6000-year origin
suggested by the archaeological record, numer-
ous matrilines must have been incorporated into
the gene pool of the domestic horse.
To expand the representation of modern and
ancient breeds, we sequenced 355 bp of the left
domain of the mtDNA control region in 191
horses from 10 distinct breeds (9), including
some that are very old such as the Icelandic
pony, Swedish Gotland Russ, and British Ex-
moor pony. A Przewalski’s horse was also se-
quenced. We found 32 different sequences, and
a search of GenBank provided 38 additional
haplotypes for the same region. We compared
all these sequences with those obtained from
DNA isolated from long bone remains of eight
horses preserved frozen in Alaskan permafrost
deposits from a locality near Fairbanks, Alaska,
dated 12,000 to 28,000 years ago (10, 11).
Additionally, we sequenced DNA of eight
1
Department of Evolutionary Biology, Uppsala Uni-
versity, Norbyva¨gen 18D, S-75236 Uppsala, Sweden.
2
Department of Organismic Biology, Ecology and Evo-
lution, University of California, Los Angeles, CA
90095–1606, USA.
3
Archeological Research Laborato-
ry, Stockholm University, S-10691 Stockholm, Swe-
den.
4
Department of Animal Breeding and Genetics,
Swedish University of Agricultural Sciences, S-75007
Uppsala, Sweden.
*To whom correspondence should be addressed. E-
mail: carles.vila@ebc.uu.se
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horse remains from archaeological sites in
southern Sweden and Estonia, dated to 1000 to
2000 years ago (11).
The additional sequences affirm the ancient
and diverse origin of domestic horse mtDNA
lineages (Fig. 1B). Six of eight permafrost se-
quences cluster in a group ancestral to modern
sequences (Pleist2, Pleist3, Pleist4, Pleist6,
Pleist7, and Pleist8), possibly representing a
sister taxon of the domestic horse or a lineage
not present in modern domestic horses (Fig.
1B) (12). However, the other two permafrost
sequences cluster with those of clade C (Pleist1
and Pleist5). These sequences differ by as little
as 1.2% from modern counterparts. Similarly,
four complete and four incomplete sequences
found in archaeological remains are distributed
throughout the tree defined by modern horse
sequences and are closely related to them (Fig.
1B). Finally, in the most primitive (4) and
chromosomally distinct horse (13), the Prze-
walski’s horse, only a single haplotype has been
found [EC13B, Fig. 1B; cf. (14 )]. The low
variability of the Przewalski’s horse is not un-
expected because the captive population was
founded from only 13 individuals (14 ). This
haplotype is not directly ancestral to any se-
quence cluster. Therefore, because sequences
from ancient specimens and Przewalski’s hors-
es are very similar to those in modern horses,
our results contradict the possibility that a high
mutation rate explains the haplotype diversity
observed in modern horses. Moreover, modern
horse sequences do not define monophyletic
groups with respect to wild progenitors, as
would be expected if they were founded from a
limited wild stock (15–17). The lack of well-
supported phylogenetic clades and the presence
of numerous matrilines whose divergence ex-
Fig. 1. Mitochondrial control
region sequence trees. (A)
Neighbor-joining tree of
modern horse haplotypes
based on 616 bp of mito-
chondrial control region se-
quence. Letters A to F indi-
cate sequence clades consis-
tently supported with differ-
ent tree-building methods.
Support values are indicated
at nodes when found in at
least 50% of 1000 bootstrap
neighbor-joining trees, in a
consensus tree of 1000 steps
based on the quartet puz-
zling algorithm, and in a 50%
majority rule consensus tree
of 26,113 most parsimoni-
ous trees. (B) Neighbor-join-
ing tree of modern and an-
cient horse haplotypes based
on 355 bp of control region
sequence. Bootstrap support
is indicated at nodes if found
in more than 50% of 1000
bootstrap trees. Letters A to
F correspond to sequence
clades in (A). The sequence
identification codes refer to
GenBank accession numbers,
except for the sequences ob-
tained in this study. Modern
horses are indicated with the
prefix EC, late Pleistocene
sequences from permafrost
deposits near Fairbanks,
Alaska, with a dot and the
prefix Pleist, and archaeolog-
ical sequences from northern
Europe with a triangle and
the prefix Anc. The sequence
obtained from Przewalski’s
horses is indicated with an
asterisk. For some archaeo-
logical samples, only partial
sequences were obtained:
Anc4, 262 bp were se-
quenced, most similar to se-
quences in clade C; Anc5,
241 bp, identical to sequenc-
es related to clade B; Anc7,
259 bp, identical to sequenc-
es in clade A; and Anc8, 223
bp, most similar to sequenc-
es in clade A.
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ceeds that between late Pleistocene and modern
sequences suggest a massive and unprecedent-
ed retention of ancestral matrilines. The obser-
vation that the sequences obtained from the late
Pleistocene Alaskan horses cluster in two dis-
crete groups indicates that the diversity of
mtDNA lineages in single natural populations
might have been limited. Consequently, the
high diversity of matrilines observed among
modern horses suggests the utilization of wild
horses from a large number of populations as
founders of the domestic horse. A single geo-
graphically restricted population would not suf-
fice as founding stock.
Although the initial founding of the domes-
tic horse involved incorporation of multiple ma-
trilines, the development of phenotypically dis-
tinct breeds may be a different process charac-
terized by a limited founding stock and restrict-
ed breeding (18). Consistent with limited
genetic exchange among breeds, we found that
haplotype frequencies differed significantly in
all but one of 45 pairwise breed comparisons
(exact test, P 0.05) (19). However, the se-
quences found in the 10 sampled modern and
ancient breeds never defined monophyletic
groups as might be expected if they were de-
rived from a limited founding stock (Fig. 2A).
Additionally, genetic diversity within breeds is
high; on average, 7.4 haplotypes occurred per
breed (range: 3 to 9), and the nucleotide diver-
sity per breed averaged 0.022 (range: 0.012 to
0.027), comparable to that found in large wild
ungulate populations (20). Moreover, genetic
diversity within breeds is not a recent phenom-
enon, because Viking Age horse bones 1000 to
2000 years old and from a restricted area in
northern Europe also show a diversity of control
region lineages (Fig. 1B). The high haplotypic
diversity of ancient horse breeds and of a Viking
Age population suggests that domestic horse
populations were founded by a diversity of ma-
trilines that, as suggested by the archaeological
record, was augmented by trade (21, 22).
High levels of mtDNA variation within
and between horse breeds may reflect a bias
toward females in breeding and trade. Con-
sequently, we assessed variation in 15 hyper-
variable, biparentally inherited, microsatellite
loci (23–27 ). The observed microsatellite
heterozygosity was moderately high for all
breeds, varying from 49.4% 5.7% to
62.6% 5.8%, and the mean number of
alleles per locus varied from 3.6 0.3 to
4.5 0.4. Allele frequencies differed signif-
icantly between breeds (exact test, P 0.01).
The microsatellite divergence between breeds
was more marked than observed with
mtDNA sequences. Individuals from the
same breed generally clustered together in a
neighbor-joining tree based on allele sharing
distance (Fig. 2B), and 95% of individuals
could be classified correctly to breed with an
assignment test (28). These results show that
maternal gene flow has dominated the genetic
exchange between breeds and/or that female
effective population size within breeds is
larger than that of males. A sex bias in an-
cient breeding is consistent with modern
Fig. 2. Genetic diversity in horse breeds. (A) Distribution of haplotypes
found in 10 horse breeds and in horses of the Orient from GenBank. This
distribution is superimposed on a neighbor-joining tree of modern horse
haplotypes based on the same 355 bp of the control region sequence, as
in Fig. 1B. Each one of the observed haplotypes is indicated by a colored
symbol corresponding to its position in the relationship tree. (B) Un-
rooted neighbor-joining tree of horses from 10 breeds as in (A) based on
the proportion of shared alleles between individuals.
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breeding practices in which select breeding
males are used as stud for 15 to 20 or more
females (29).
Wild horses were widely distributed
throughout the Eurasian steppe during the Up-
per Paleolithic [35,000 to 10,000 years before
present (B.P.)], but in many regions, they dis-
appeared from the fossil record about 10,000
years ago (3, 4). Horse remains became in-
creasingly frequent in archaeological sites of
southern Ukraine and Kazakhstan starting
about 6000 years ago, where limited evidence
from bit wear on teeth suggests that some hors-
es could have been ridden (29, 30). By the
beginning of the Iron Age, wild horse popula-
tions had declined, and today, only one putative
wild population, the Przewalski’s horse, re-
mains (4). Therefore, a scenario consistent with
the archaeological record and genetic results
posits that, initially, wild horses were captured
over a large geographic area and used for nu-
trition and transport. As wild populations dwin-
dled because of exploitation or environmental
changes (31), increased emphasis was placed
on captive breeding, allowing for multiple ma-
trilines of a single ancestral species to be inte-
grated into the gene pool of domestic horses.
This contrasts with previous notions of domes-
tication as a complex multigeneration process
that begins with relatively few individuals se-
lected for behavioral characteristics, such as
docility and sedentary habits, as a prerequisite
to coexistence with humans.
Domestic species such as dogs, cattle,
sheep, and goats were established several thou-
sand years before the horse was domesticated
(4). The geographic spread of these species was
a likely result of their expansion from a limited
number of domestication centers. In the horse,
the extensive and unparalleled retention of an-
cestral matrilines suggests that widespread uti-
lization occurred primarily through the transfer
of technology for capturing, taming, and rearing
wild caught animals (29, 30). In contrast, the
export of domesticated horses from a geograph-
ically restricted center of origin would have
resulted in a more limited diversity of matri-
lines. Consequently, in the history of the do-
mestic horse, transfer of technology rather than
selective breeding may have been the critical
innovation leading to their widespread utiliza-
tion. Moreover, the high value of horses in
primitive societies (1, 2) placed a premium on
the rapid acquisition of this technology from
neighboring communities.
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den, Late Viking Age; Anc7, EstP61, tooth, from Pada,
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32
P and were separated in 6%
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(38). An assignment test that uses likelihood ratios to
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ij
1 P
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, where P
ij
is the
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39. Supported by the Swedish Research Council for Ag-
riculture and Forestry, the Swedish Royal Academy of
Sciences, the NSF, and the Bank of Sweden Tercen-
tenniary Foundation. We thank the American Muse-
um of Natural History in New York and the Historical
Museum in Stockholm for permission to sample their
collections; L. Luoˆgas for providing archaeological
horse samples from Estonia; H. Persson for assisting
in the microsatellite typing; and J. Diamond, B. Van
Valkenburgh, M. Kohn, and K.-P. Koepfli for com-
menting on the manuscript.
12 October 2000; accepted 13 December 2000
R EPORTS
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Supplementary resources (52)

... The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript." targeted small portions of the mitochondrion, focusing particularly on clarifying the early phylogenetic history of horse domestication [20][21][22][23]. These studies revealed a weak geographic structure among mitochondrial haplogroups, the highest diversity of which are found in Asian horses, and also show that European and Middle Eastern horses lack genetic representation of the most ancestral lineages, suggesting an Asian origin [23]. ...
... Bootstrap support is on the nodes (10,000 iterations). Letters on the right correspond to the equine haplogroups defined by Achilli et al. [22]. (TIF) S1 Table. ...
... Samples from GenBank that were included in the phylogeographic analysis. Except for NC001788 (Equus asinus) all are published in Achilli et al. [22]. (DOCX) S1 File. ...
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Unlike other European domesticates introduced in the Americas after the European invasion, equids (Equidae) were previously in the Western Hemisphere but were extinct by the late Holocene era. The return of equids to the Americas through the introduction of the domestic horse ( Equus caballus ) is documented in the historical literature but is not explored fully either archaeologically or genetically. Historical documents suggest that the first domestic horses were brought from the Iberian Peninsula to the Caribbean in the late 15 th century CE, but archaeological remains of these early introductions are rare. This paper presents the mitochondrial genome of a late 16 th century horse from the Spanish colonial site of Puerto Real (northern Haiti). It represents the earliest complete mitogenome of a post-Columbian domestic horse in the Western Hemisphere offering a unique opportunity to clarify the phylogeographic history of this species in the Americas. Our data supports the hypothesis of an Iberian origin for this early translocated individual and clarifies its phylogenetic relationship with modern breeds in the Americas.
... Methodological and bioinformatics tools have recently been developed, allowing for increased accuracy in the analysis of high-throughput genomes, and over last decades, the equine research community has aimed to reconstruct the evolutionary paths that can still be detected in their genomes [8]. Genetic evidence has pinpointed multiple horse domestication events occurring across Eurasia 5000-6000 years ago [2,[9][10][11][12][13][14][15][16]. After this evidence emerged, the history of the horse domestication process was revised. ...
... In contrast to the high mtDNA variability reported in previous studies [2,8,9,115,116], which was already present immediately after their domestication [17,19,117], the Y chromosome shows a very low level of genetic polymorphism in modern horse populations [91,118]. Despite a large diversity of domestic male founders contributing to their early domestication [117], the Y chromosome variability considerably decreased in the last 200 years because of selective pressures and the reduction in the stallion population size operated by breeders [19]. ...
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... However, archaeological data are fragmented, and many characteristic differences may have already existed between domesticated animals and their wild ancestors in the early domestication phase, including coat color, temperament, and reproductive ability, which cannot be discovered through skeletal archaeology. The other method analyzes the genome of modern domesticated animals to obtain temporal and geographic information on domestication and to discover the genetic basis of domestication (Luikart et al., 2001;Vilà et al., 2001;Pedrosa et al., 2005;Naderi et al., 2008), including inferring the initial domestication centers based on the genetic diversity generated by geographical differences. A large amount of phenotypic diversity exists among and within species of modern domesticated animals, and genomic analysis can reveal the influence of specific loci on phenotypes, including coat color, body size, fat content, biological clock, and behavior (Wright, 2015). ...
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Background: The domestication of horses has played critical roles in human civilizations. The excavation of ancient horse DNA provides crucial data for studying horse domestication. Studies of horse domestication can shed light on the general mechanisms of animal domestication. Objective: We wish to explore the gene transcription regulation by long noncoding RNAs (lncRNAs) that influence horse domestication. Methods: First, we assembled the ancient DNA sequences of multiple horses at different times and the genomes of horses, donkeys, and Przewalski horses. Second, we extracted sequences of lncRNA genes shared in ancient horses and sequences of lncRNA genes and the promoter regions of domestication-critical genes shared in modern horses, modern donkeys, and Przewalski horses to form two sample groups. Third, we used the LongTarget program to predict potential regulatory interactions between these lncRNAs and these domestication-critical genes and analyzed the differences between the regulation in ancient/modern horses and between horses/donkeys/Przewalski horses. Fourth, we performed functional enrichment analyses of genes that exhibit differences in epigenetic regulation. Results: First, genes associated with neural crest development and domestication syndrome are important targets of lncRNAs. Second, compared with undomesticated Przewalski horses, more lncRNAs participate in the epigenetic regulation in modern horses and donkeys, suggesting that domestication is linked to more epigenetic regulatory changes. Third, lncRNAs’ potential target genes in modern horses are mainly involved in two functional areas: 1) the nervous system, behavior, and cognition, and 2) muscle, body size, cardiac function, and metabolism. Conclusion: Domestication is linked to substantial epigenetic regulatory changes. Genes associated with neural crest development and domestication syndrome underwent noticeable lncRNA-mediated epigenetic regulation changes during horse domestication.
... Among the segregating sites, we also identified four mutational hotspots previously described located at positions 15585, 15597, 15650, and 15659 [29], and these positions were not included in phylogenetic analysis (Table 2A,B). ...
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