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C. R. Biologies 334 (2011) 247–254
Contents lists available at ScienceDirect
Comptes Rendus Biologies
www.sciencedirect.com
Review/Revue
Conservation genetics of cattle, sheep, and goats
Génétique de la conservation de la vache, du mouton, et de la chèvre
Pierre Taberlet *, Eric Coissac, Johan Pansu, François Pompanon
CNRS UMR 5553, laboratoire d’écologie alpine, université Joseph-Fourier, BP 53, 38041 Grenoble, France
A R T I C L E I N F O
A B S T R A C T
Article history:
Available online 1 February 2011
Cattle, sheep and goats were domesticated about 10,000 years ago, spread out of the
domestication centers in Europe, Asia, and Africa during the next few thousands years, and
gave many populations locally adapted. After a very long period of soft selection, the
situation changed dramatically 200 years ago with the emergence of the breed concept.
The selection pressure strongly increased, and the reproduction among breeds was
seriously reduced, leading to the fragmentation of the initial gene pool. More recently, the
selection pressure was increased again via the use of artificial insemination, leading to a
few industrial breeds with very high performances, but with low effective population
sizes. Beside this performance improvement of industrial breeds, genetic resources are
being lost, because of the replacement of traditional breeds by high performance industrial
breeds at the worldwide level, and because of the loss of genetic diversity in these
industrial breeds. Many breeds are already extinct, and genetic resources in cattle, sheep,
and goats are thus highly endangered, particularly in developed countries. The recent
development of next generation sequencing technologies opens new avenues for properly
characterizing the genetic resources, not only in the very diverse domestic breeds, but also
in their wild relatives. Based on sound genetic characterization, urgent conservation
measures must be taken to avoid an irremediable loss of farm animal genetic resources,
integrating economical, sociological, and political parameters.
ß 2011 Académie des sciences. Published by Elsevier Masson SAS. All rights reserved.
Keywords:
Bos
Breeds
Capra
Domestication
Genetic diversity
Ovis
Selection
R É S U M É
Mots clés :
Capra
Bos
Diversité génétique
Domestication
Ovis
Races
Sélection
La vache, le mouton et la chèvre ont été domestiqués il y a environ 10 000 ans. Ils se sont
ensuite répandus en Europe, Asie, et Afrique durant les quelques milliers d’années qui ont
suivi, et ont donné de nombreuses populations bien adaptées aux conditions locales. Après
une très longue période de sélection non intensive, la situation a changé il y a 200 ans avec
l’émergence de la notion de race. La pression de sélection a fortement augmenté et la
reproduction entre races a été sérieusement réduite, conduisant à la fragmentation du
pool génétique initial. Plus récemment, la pression de sélection a augmenté à nouveau par
l’utilisation de l’insémination artificielle, donnant quelques races industrielles très
performantes, mais avec de faibles tailles efficaces de population. Le revers de cette
amélioration des performances des races industrielles est que les ressources génétiques
sont en voie de disparition, en raison d’une part du remplacement au niveau mondial des
races traditionnelles par des races industrielles à haute performance et, d’autre part, de la
perte de diversité génétique chez ces races industrielles. De nombreuses races sont déjà
éteintes et les ressources génétiques chez la vache, le mouton et la chèvre sont donc très
* Corresponding author.
E-mail address: pierre.taberlet@ujf-grenoble.fr (P. Taberlet).
1631-0691/$ – see front matter ß 2011 Académie des sciences. Published by Elsevier Masson SAS. All rights reserved.
doi:10.1016/j.crvi.2010.12.007
Author's personal copy
P. Taberlet et al. / C. R. Biologies 334 (2011) 247–254
248
menacées, en particulier dans les pays développés. La mise au point récente de nouvelles
technologies de séquençage d’ADN ouvre de nouvelles perspectives pour une meilleure
caractérisation des ressources génétiques, non seulement dans les diverses races
domestiques, mais aussi chez les espèces sauvages proches. Sur la base de caractérisations génétiques fiables, des mesures de conservation urgentes doivent être prises pour
éviter une perte irrémédiable des ressources génétiques chez les animaux domestiques,
en intégrant des paramètres économiques, sociologiques et politiques.
ß 2011 Académie des sciences. Publié par Elsevier Masson SAS. Tous droits réservés.
1. Introduction
Conservation biology is a relatively new field of
research that emerged in the seventies with the goal of
preserving ecosystems, species and genes [1]. Within this
field, conservation genetics deals with the application of
genetic concepts and tools to conservation problems. At
first glance, highlighting conservation problems in domestic ungulates may appear as a paradox [2], as the census
population sizes of farm animals are extremely high (Table
1). Potential conservation issues in domestic animals were
already spotted by the Food and Agriculture Organization
of the United Nations (FAO) in the seventies [3] with the
objective of long-term conservation of genetic resources
for future use. Such a goal can be achieved by preserving
the widest possible spectrum of genetic diversity because
future needs are unpredictable. This FAO document [3] also
emphasized the conflict between immediate improvement
and conservation, indicating that ‘‘the best way of
conservation would be the development of a management
system which would both maintain genetic variability of
existing livestock resources and at the same time permit
continuous improvement in productivity and adaptability
of that resource’’. Unfortunately, despite this very early
warning, the investments toward conservation aspects
were far behind those for improving the productivity of a
few industrial breeds. As a consequence, traditional
indigenous breeds are still disappearing (Table 1) and
the effective population size of many cattle breeds is far
below a threshold that would ensure long-term sustainability. The last FAO survey [4] considered that 16, 13 and
3% of the cattle, sheep, and goat breeds already disappeared, respectively. In such a context, it is becoming more
and more urgent to implement sound conservation
strategies for farm animals [5].
In this paper, we first aim to review the current
knowledge about the origin and the history of cattle, sheep,
and goats. Such knowledge is of prime importance for
properly assessing the risk concerning the loss of genetic
diversity and for designing sound conservation guidelines.
We also examine the current practices that lead to massive
Table 1
Population sizes, current number of breeds, and number of extinct breeds
for cattle, sheep, and goats at the worldwide level (statistics concerning
169 countries [4]).
Population size (’000)
Number of breeds
Number of extinct breeds
Cattle
Sheep
Goat
1,367,335
1311
209
1,060,606
1409
180
710,381
618
19
loss of genetic resources. Then, we highlight the potential
genetic resources, obviously including domestic breeds but
also including wild relatives. Finally, we provide conservation guidelines for long-term sustainability based on the
current situation and on the availability of new genomic
tools.
2. The origin of cattle, sheep and goats
Data about cattle, sheep, and goat domestication first
came from osteometry and morphometry evidence collected in archaeological sites [6]. More recently, these data
were completed by extensive genetic studies [7] using
both modern and ancient samples, thus allowing producing more precise scenarios of the domestication processes.
The first archaeological evidence of the domestication of
these three species traces back to around 10,500 BP
(calibrated) in the Fertile Crescent (Fig. 1). It seems that
goat and sheep were domesticated first [8,9], immediately
followed by cattle [10].
The wild ancestor of all domesticated cattle was the
auroch (Bos primigenius) [11] that is now extinct. Aurochs
had a very wide geographic distribution, from East Asia to
Europe and North Africa. The common usage accepts two
taxa for the domestic cattle, namely Bos taurus and
B. indicus that fully interbreed. B. indicus differs from
B. taurus by the presence of a prominent hump. The
presence of two mtDNA haplogroups (Fig. 2) is interpreted
as an indication of two main domestication events, the one
in the Fertile Crescent leading to B. taurus and the other in
the Indian subcontinent leading to B. indicus [12–14].
Extensive hybridization occurred in Africa, leading to a
complex intermixing of these two mitochondrial haplogroups in the field [13].
The systematics of the genus Ovis is controversial. The
number of species that have been recognized within this
genus varies from one [15] to seven [16]. Recently, an
extensive mitochondrial and nuclear DNA survey including
all taxa of the genus was carried out [17], confirming the
presence of seven monophyletic clades corresponding to
the seven species described by Nadler et al. [16]. Based on
another extensive study of the mitochondrial DNA
(mtDNA) of putative ancestors (O. orientalis, the Asiatic
mouflon; O. vignei, the urial; O. ammon, the argali), it
clearly appeared that the wild ancestor is O. orientalis [18].
Both archaeological [8] and genetic data spot the
domestication center in eastern Anatolia and North-west
Iran. To date, the number of mtDNA haplogroups described
for the domestic sheep varies as no standard criteria are
used for defining them [19,20]. However, authors agree on
three main haplogroups (i.e. A, B and C in Fig. 1).
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P. Taberlet et al. / C. R. Biologies 334 (2011) 247–254
249
Fig. 1. The main events in cattle, sheep, and goat domestication.
Goat domestication is well documented by archaeological evidence and also by several genetic studies. The goat
wild ancestor is the bezoar, Capra aegagrus [21–23]. A
large-scale analysis of current bezoar mtDNA polymor[()TD$FIG]phism over its whole geographic distribution has recently
been performed [23]. All the six current mitochondrial
haplogroups found in the domestics (Fig. 2) were also
found in its wild ancestor, suggesting that the domestication process occurred over a very large area encompassing
eastern Anatolia and North-West Iran.
Fig. 2. Unrooted neighbor-joining trees illustrating the mtDNA polymorphism of cattle, sheep, and goats [2,51].
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P. Taberlet et al. / C. R. Biologies 334 (2011) 247–254
The cattle mtDNA polymorphism [12,13,24] seems
compatible with the domestication of only two mtDNA
haplotypes, leading to B. taurus and B. indicus. Such an
observation is in favor of a population bottleneck at the
domestication time. On the opposite, the goat mtDNA
polymorphism of the A haplogroup (representing more
than 90% of the haplotypes) is by far too high for
originating from a single haplotype at the domestication
time. A detailed analysis of this A haplogroup suggested an
initial number of haplotypes higher than 1000 [23],
strongly supporting the absence of bottleneck at the
domestication time in goats. The sheep mtDNA polymorphism also seems to support an absence of bottleneck.
How can the differences between cattle on one hand, and
goat and sheep on the other hand, be explained? If we
assume that a sustainable domestication must be based on
a very high gene pool, we may elaborate the following
scenario. As the geographic distribution of sheep and goat
wild ancestors was quite restricted around the domestication centres, only a large-scale domestication event
involving thousands of individuals can produce a population that will not suffer from inbreeding depression later
on, during the dispersal out of the domestication centres.
The cattle domestication might have followed a different
trajectory, with first a bottleneck at the domestication
time, followed by extensive introgressions from the
aurochs later on, over large geographic areas as the wild
ancestor was very widely distributed [25]. Such introgressions were able to enlarge the nuclear DNA gene pool of
cattle until the extinction of the aurochs in the sixteen
century. We can also imagine that these introgressions
were strongly biased toward male aurochs mating with
domestic females, explaining why cattle mtDNA only
transmitted by female does not show significant auroch
contribution. However, aurochs’ mtDNA have been found
at a very low percentage in Italian cattle breeds [26,27].
Recent studies [28] suggest that introgressions from
aurochs into domestics may have been even more
widespread than expected. This might partly explain the
relatively large cattle gene pool despite a likely bottleneck
at the time of domestication.
3. Dispersal from the domestication centres
During the 3000–4000 years following the initial
domestication events in the Fertile Crescent, the Neolithic
culture diffused over Europe, Africa and Asia. Archaeological evidence showed that agriculture colonized Europe by
two main routes, the Mediterranean route and the
Danubian route. Due to successive founder effects during
the spread of agriculture, we can hypothesize a clinal
decrease in genetic diversity with increasing distance to
the domestication centre. Such a decrease has been
demonstrated for cattle mtDNA, for which populations
in Western Europe exhibit lower polymorphism than those
in the Near East [14,24]. This might not be initially the case
for cattle nuclear DNA if introgressions from aurochs were
common. However, the pattern of variation observed may
also be the result of recent selective processes; it has been
recently shown that traditional cattle breeds closer to the
domestication centre in Middle East show a higher nuclear
polymorphism than more heavily selected breeds in
Western Europe [29]. Several secondary migrations
accompanied human migrations in more recent historical
times and contributed to a more complex shaping of local
gene pools. For example, it has been shown that Iberian
cattle breeds have been introgressed by African breeds
[30–33]. Also, a close genetic relationship was discovered
between Tuscan cattle breeds and Near Eastern breeds,
possibly linked to the sailing and docking in Tuscany of
Middle Eastern people in the late Bronze Age and to the
onset of the Etruscan civilization in Central Italy [34].
Surprisingly, despite potential serial founder effect during
the agriculture spread, the nuclear DNA polymorphism
based on microsatellites is still relatively high in the three
species [35–38], comparable to what is found in wild
species. Such a result suggests a large effective population
size during most of the period since the colonization.
4. Influence of the breed concept on genetic diversity
Fig. 1 summarizes the history of cattle, sheep, and goats.
During about 10,000 years, farmers controlled the reproduction of their farm animals by favoring the reproduction
of individuals with better phenotypes. As a result, farm
animals slowly became adapted to local environments and
fulfilled the needs of farmers in a sustainable way. At that
time, gene flow among different phenotypes was possible,
resulting in relatively high effective population sizes,
preventing genetic drift at the regional scale. The situation
dramatically changed about two hundred years ago with
the emergence of the breed concept. Since that time, much
stronger selection pressures have been applied to local
populations followed by standardization of the morphology and the performance. All animals from the same breed
began to exhibit the same phenotypic characteristics,
including the same coat color. Most importantly, the gene
flow among different phenotypes (i.e. among different
breeds) was seriously reduced. To summarize, as illustrated on Fig. 3, the populations of farm animals that
underwent relatively soft selection pressures during about
98% of their common history with humans were suddenly
fragmented into many well-defined breeds, with much
higher selection constraints. Population fragmentation is
known to have deleterious consequences in the long term
by increasing genetic drift and inbreeding, and by reducing
the fitness [39]. Fragmentation is also one of the most
important factors leading to extinction in wild species [39].
5. The current loss of genetic resources
The current loss of genetic resources concerns not only
the extinction of traditional breeds, but also the loss of
genetic diversity within breeds. With the development of
artificial insemination during the last 50 years, only a few
males were involved in reproduction schemes and
consequently industrial breeds underwent another important step toward the reduction of their effective population
size. For example, at the worldwide level, the Holstein
cattle has an effective population size of about 50 (Table 2),
leading inexorably to genetic drift and loss of alleles. All the
genetic diseases observed in this breed [40], as well as the
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251
Fig. 3. Different phenotypes in the past now replaced by a homogenous breed.
strong reduction in fertility [41] may be linked to such a
low effective population size. Based initially on data from
livestock, conservation biologists proposed the 50/500 rule
of thumb for managing wild species [42]: in the short term,
the effective population size should not be less than 50 to
avoid extinction risk due to genetic effects; in the long
term, the effective population should not be less than 500.
Surprisingly, such low effective population sizes in many
cattle industrial breeds did not warn scientists in charge of
the management of these breeds, maybe because a low
effective population size is an advantage for short-term
genetic selection and performance improvements.
Traditional breeds are threatened by the success of
industrial breeds via two processes. First, the high
performance of industrial breeds tends to impose the
replacement of traditional breeds by more productive
ones. In many areas, farmers have a strong economic
pressure to switch to industrial breeds. Such a phenomenon can be very fast, and a valuable traditional breed can
Table 2
Example of effective population sizes in the cattle Holstein breed.
Country
Period
Census
population
size
Effective
population
size (Ne)
Reference
USA
France
Denmark
Germany
1999
1988–1991
1993–2003
1999
8,500,000
2,500,000
3,700,000
2,200,000
39
46
49
52
[52]
[53]
[54]
[55]
be lost within a decade. Second, autochthonous breeds are
often crossbred to a more productive breed from
elsewhere, most often a high production breed. Adaptive
traits may be rapidly lost by poorly designed crossbreeding
leading to dilution of important adaptive loci of traditional
breeds. Traits such as resistance to local infectious and
parasitic diseases, adaptation to poor forage, homing and
gregarious behavior can be rapidly lost and difficult to
rescue. They represent key traits for the survival and the
management of herds in extensive farming. In developing
countries, many examples illustrate this introgression
threat, where indiscriminate repeated crossbreeding
quickly disrupted generations of selection for adaptation
to harsh environments (see examples in [2]).
6. The potential genetic resources
A basic approach for characterizing these resources can
simply be to record phenotypic characters in all the very
diverse breeds adapted to different environments and
management systems. Then the genetic resources can be
identified based on these phenotypic characters, assuming
that phenotypes are strongly linked to genetics. An
alternative approach consists to employ genetic markers.
However, the characterization of genetic resources with
molecular markers suffers two difficulties: the ascertainment bias of the markers used, and the problem of neutral
versus adaptive markers.
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252
Table 3
Wild species representing potential genetic resources for cattle, sheep, and goats (only the most closely related species are presented for sheep and goats).
Common name
Scientific name
Geographic distribution
Domestic form
Conservation
status [56]
Gaur
Banteng
Bos gaurus
Bos javanicus
Bos frontalis
Bali cattle
Vulnerable
Endangered
Kouprey
Bos sauveli
–
Yak
Bos mutus
Bos grunniens
Critically endangered
(possibly extinct)
Vulnerable
Asiatic Mouflon
Urial
Argali
Bezoar
Ovis orientalis
Ovis vignei
Ovis ammon
Capra aegagrus
Ovis aries (sheep)
–
–
Capra hircus (goat)
Least concern
Vulnerable
Near threatened
Vulnerable
Markhor
Capra falconeri
South and southeast Asia (largest populations in India)
South Asia (Java, Borneo, Myanmar, Thailand, Cambodia,
Laos, Vietnam)
Northern Cambodia, southern Laos, Western Vietnam,
eastern Thailand
Himalayan region of south Central Asia (Tibetan Plateau,
Mongolia, Russia)
Caucasus, northern Iraq, northwestern Iran, Anatolia
Asia minor
Central Asia
Central Afghanistan, southern Pakistan, Iran, western
Turkmenistan, northern Iraq, Caucasus region, Turkey
Northeastern Afghanistan, Gilgit-Balistan, Hunza-Nagar
Valley, northern and central Pakistan, Kashmir, southern Tajikistan,
southern Uzbekistan
–
Endangered
The ascertainment biases are due to the adjustment of
genetic markers (microsatellites or single nucleotide
polymorphisms) with the constraint of being as polymorphic as possible in the breeds under study, i.e. industrial
breeds in most cases. As a consequence, the genetic
diversity estimates for traditional breeds when using such
markers will be biased toward low values and the
estimation of heterozygosity is particularly affected [43].
Such an ascertainment bias has also been clearly shown in
wild species where only the most polymorphic microsatellites are selected for further investigations [44].
Genome-wide analyses based on single nucleotide polymorphisms (SNP) are now widely used in farm animals
[45], but also suffer from the same ascertainment bias
[46,47]. In such a situation, only sequencing many regions
of the genome would give a reliable estimate of the genetic
diversity [44] and is appropriate for properly characterizing genetic resources.
The second difficulty for characterizing genetic
resources is linked to an ongoing debate about the relative
importance of neutral versus adaptive variations for
identifying the populations to prioritize for protection
purposes. The neutral variation, an indicator of global
genetic diversity, can be used for assessing conservation
values, based on the idea that we do not know future
selection pressures and that more diverse populations at
the genome-wide level will better adapt [48]. The opposite
point of view claims that only adaptive variation is
relevant for conservation purpose [49].
Should we include wild ancestors as potential genetic
resources when they still exist? The answer to this
question is not straightforward, as no extensive study
has been carried out so far to properly assess the potential
of wild populations as genetic resources. The value of wild
ancestors will be inversely linked to the proportion of
genetic diversity that has been captured during the
domestication process. Within each of the Capra and Ovis
genera, many species can hybridize and produce fertile
offspring. As a consequence, beside the wild ancestor,
several other species within these two genera can also be
considered as genetic resources (e.g. Capra falconeri for
goats, Ovis vignei and O. ammon for sheep; Table 3). For
cattle the situation is different, as the wild ancestor is
extinct. Nevertheless, four or five wild species of the genus
Bos are still alive and can produce fertile hybrids with
cattle. Thus, they might also be considered as genetic
resources (Table 3).
7. Conclusion
The effective management of farm animal genetic
resources is primordial to ensure global and sustainable
food security. The erosion of genetic resources has been
clearly documented for farm animals [4]. Within a few
decades, we might lose most of the highly valuable farm
animal genetic resources that humanity has gradually
selected over the past 10,500 years [2]. Urgent conservation measures must be taken to avoid such an irremediable
loss [5]. These genetic resources are even not properly
characterized due to the problem of ascertainment bias of
the molecular markers used up to now. Fortunately, with
the development of the next generation DNA sequencing
technology [50], it will be possible to resequence whole
genomes and to properly assess the genetic diversity and
the conservation value of the different breeds, avoiding the
ascertainment bias due to the use of microsatellites or
single nucleotide polymorphisms. There is clearly a race
between the characterization of genetic resources and
their loss. In the same way, the development of genomic
tools will allow to optimize the breeding strategies for
ensuring the improvement of performance together with
the preservation of genetic diversity.
If the integration of wild relatives in conservation
planning is common in plants, it is not the case for
domestic animals. Most of the wild relatives of cattle,
sheep, and goats are endangered (Table 3), and no ongoing
actions were implemented to preserve them based on the
fact that they have the potential of representing valuable
genetic resources for agriculture. Thus, it is now urgent to
properly assess their potential as genetic resources.
The first step toward an efficient conservation strategy
for cattle, sheep, and goat genetic resources is the proper
characterization of the conservation value of the different
breeds and of the wild relatives. This step relies on genetic
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P. Taberlet et al. / C. R. Biologies 334 (2011) 247–254
technologies, and we can be optimistic at that level
according to the current revolution in DNA sequencing.
However, the implementation of the subsequent steps is
more puzzling, as conservation strategies for farm animal
genetic resources must integrate economical, sociological,
and political parameters.
Conflict of interest statement
The authors have not declared any conflict of interest.
Acknowledgements
The European Commission provided funding via the FP7
NextGen project (‘‘Next generation methods to preserve
farm animal biodiversity by optimizing present and future
breeding options’’; Grant agreement no. 244356).
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