doi:10.1111/j.1365-2052.2010.02038.

Genetic diversity in farm animals – a review

L. F. Groeneveld*, J. A. Lenstra†, H. Eding‡, M. A. Toro§, B. Scherf¶, D. Pilling¶, R. Negrini**,
E. K. Finlay††, H. Jianlin‡‡, E. Groeneveld*, S. Weigend* and The GLOBALDIV Consortium
*Institute of Farm Animal Genetics, Friedrich-Loeffler-Institut, Hoeltystr. 10, 31535 Neustadt, Germany. †Department of Infectious Diseases
and Immunology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 2, 3584 CM, Utrecht, The Netherlands. ‡Animal Evaluations
Unit, CRV, PO Box 454, 6800 AL, Arnhem, The Netherlands. §Departamento de Producción Animal, ETS Ingenieros Agrónomos,
Universidad Politécnica de Madrid, 28040 Madrid, Spain. ¶Animal Production and Health Division, Food and Agriculture Organization of the
United Nations, Viale delle Terme di Caracalla, 00153 Rome, Italy. **Istituto di Zootecnica, Facoltà di Agraria, Università Cattolica del Sacro
Cuore, Via Emilia Parmense 84, 29122 Piacenza, Italy. ††Smurfit Institute of Genetics, Trinity College, Dublin 2, Ireland. ‡‡CAAS-ILRI Joint
Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS),
Beijing 1000193, China

Summary Domestication of livestock species and a long history of migrations, selection and adaptation
have created an enormous variety of breeds. Conservation of these genetic resources relies
on demographic characterization, recording of production environments and effective data
management. In addition, molecular genetic studies allow a comparison of genetic diversity
within and across breeds and a reconstruction of the history of breeds and ancestral
populations. This has been summarized for cattle, yak, water buffalo, sheep, goats, camelids,
pigs, horses, and chickens. Further progress is expected to benefit from advances in mole-
cular technology.
Keywords databases, domestication, farm animal genetic resources, genetic diversity,
livestock, production environment recording.

and communication systems have led to uniform and

Introduction
strictly controlled production environments. As a result,
Domestication of animals was an essential step in human highly productive breeds have replaced local ones across the
demographic and cultural development. Together with the world. This development has led to growing concerns about
domestication of plant species it laid the foundation of the erosion of genetic resources (Food and Agriculture
agriculture as we know it today (Diamond 2002). During Organization of the United Nations, FAO 2007b). As the
the subsequent history of livestock, the main evolutionary genetic diversity of low-production breeds is likely to con-
forces of mutation, selective breeding, adaptation, isolation tribute to current or future traits of interest (Notter 1999;
and genetic drift have created an enormous diversity of local Bruford et al. 2003; Toro et al. 2008), they are considered
populations. In the last centuries, this has culminated in the essential for maintaining future breeding options. According
formation of many well-defined breeds used for a variety of to the FAO, 20% of the roughly 7600 breeds reported
purposes with differing levels of performance. During the worldwide, belonging to 18 mammalian species and 16
last decades, development of and increased focus on more avian species, are at risk, and 62 breeds became extinct
efficient selection programmes have accelerated genetic within the first 6 years of this century (FAO 2007b).
improvement in a number of breeds. Artificial insemination Effective management of farm animal genetic resources
and embryo transfer have facilitated the dissemination of (FAnGR) requires comprehensive knowledge of the breeds‘
genetic material. In addition, progress in feed technology characteristics, including data on population size and
has allowed optimal nutrition, while enhanced transport structure, geographical distribution, the production envi-
ronment, and within- and between-breed genetic diversity.
Integration of these different types of data will result in the
Address for correspondence
most complete representation possible of biological diversity
S. Weigend, Institute of Farm Animal Genetics, Friedrich-Loeffler- within and among breeds, and will thus facilitate effective
Institut, Hoeltystr. 10, 31535 Neustadt, Germany. management of FAnGR. These objectives are addressed
E-mail: steffen.weigend@fli.bund.de under one of the four Strategic Priority Areas of the Global
Accepted for publication 28 October 2009 Plan of Action for Animal Genetic Resources adopted by

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 Genetic diversity in farm animals 7

109 countries at the first International Technical Confer- geographical distribution of the population. A more con-
ence on Animal Genetic Resources, held in Interlaken, centrated population is more vulnerable to localized disas-
Switzerland in 2007, and endorsed by the FAO Conference, ters, such as disease epidemics, than a widespread
(FAO 2007a). population. Demographic data obtained at the national level
It is widely accepted that detailed molecular data on need to be considered in the context of the global demo-
within- and between-breed diversity are essential for effec- graphics of the breeds in question. A breed that is common
tive management of FAnGR (e.g. Weitzman 1993; Hall & in other countries is likely to be a lower priority for national
Bradley 1995; Barker 1999; Ruane 2000; Bruford et al. conservation. A basic requirement is to know whether a
2003; Simianer 2005; Toro & Caballero 2005; Toro et al. given national breed is genetically distinct or whether it is
2008). However, to date molecular methods only provide a part of a larger population spread across several countries.
fraction of the data needed to make informed management In a recently developed classification (FAO 2007b), breeds
decisions. Many mechanisms controlling biological diversity present in only one country are termed Ôlocal breedsÕ and
are not understood. For instance, the link between func- those present in more than one country are termed Ôtrans-
tional diversity and diversity as assessed by neutral markers boundary breedsÕ, the latter being further differentiated into
is not clear. Data on the environment in which breeds are ÔregionalÕ and ÔinternationalÕ transboundary breeds
raised may be informative regarding their adaptations depending on the extent of their distribution. In 2008, 7040
and facilitate comparisons of their performance levels. local breeds, 500 regional transboundary breeds and 551
Furthermore, demographic data, compiled across political international transboundary breeds were recorded in FAOÕs
borders, are needed to assess a breedÕs risk status (FAO Domestic Animal Diversity Information System (DAD-IS;
2007b). http://www.fao.org/dad-is/) (FAO 2009).
Here, we review the current state of knowledge regarding The country, species and breed coverage of DAD-IS is
the evaluation of biological diversity of the main farm ani- described below. In the case of demographic data, much
mal species. The sections on demographic characterization remains to be done to improve coverage. For approximately
and production environment recording focus on data 53% of avian national breed populations and 48% of
requirements and outline the current state of the avail- mammalian national breed populations recorded in DAD-IS
ability of these data. This is followed by a review of breed the data necessary to provide even a basic assessment of risk
description databases, which briefly describes the available status are unavailable.
infrastructure for data management and summarizes the Monitoring of trends in population size and structure is
types of publicly accessible phenotypic and demographic hampered by a lack of regular updates of demographic data.
data. The section on genetic characterization in livestock To allow effective monitoring, data should be collected at
briefly reviews current knowledge regarding domestication least once per generation of the species in question, partic-
processes and breed diversity at the global and local level for ularly for breeds classified as at risk: about 8 years for
cattle, water buffalo, goats, sheep, horses, pigs, camelids, horses and donkeys, 5 years for cattle, buffalo, sheep and
yak and chickens. The available databases for storage and goats, 3 years for pigs and 2 years for poultry species. The
management of molecular data are the subject of a sub- required frequency is also affected by the reproductive
sequent section. We conclude with an assessment of the technology being used, which should be recorded as part of
adequacy of the infrastructure necessary for comprehensive the monitoring process. For many breeds, particularly in
analyses of global livestock diversity and outline prospects developing countries, even if demographic data are avail-
for the future. able, they have not recently been updated. The methods
used to collect the data affect their reliability, but consid-
eration also needs to be given to the costs involved. Analysis
Demographic characterization
of population data in DAD-IS shows that 87% of entries are
Demographic data are fundamental to the assessment of the based on a census or survey at breed level, while 11% are
risk status of livestock breeds – a key step in the strategic estimates based on a census at species level.
planning of FAnGR management. Risk status depends on Data on the geographical distribution of breed popula-
several factors. First, it is linked to the size and structure of tions are also limited. However, efforts to improve the sit-
the population. Effective population size (Ne) is the preferred uation are underway – textual data describing breed
measure for the assessment of risk status (FAO 1992; distribution that have been entered into DAD-IS are being
Gandini et al. 2004); it is approximated on the basis of the converted into georeferenced coordinates; more compre-
size of both the female and the male breeding populations. hensive georeferencing is regarded as a priority as part
Knowing the Ne allows the rate of inbreeding, and hence the of the implementation of set production environment
loss of genetic diversity within the population, to be inferred. descriptors (see below) within DAD-IS (FAO/WAAP 2008).
Second, risk status depends on current and predicted future Key challenges for the future include the development of
population trends. For instance, a rapid downward trend methods for representative sampling of national animal
indicates a high level of risk. The third relevant factor is the populations to estimate their total population sizes and

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8 Groeneveld et al.

other demographic data in a cost-effective manner. Another First, breed societies maintain websites to describe their
problem is the lack of measures that capture the genetic populations, with the intention of advertising their own
dilution caused by crossbreeding (FAO 2007b). It is not genetic resources. Perceived strong points of a breed are
always clear whether, and to what degree, historic or recent emphasized, although not always substantiated through
interactions between breeds have affected their uniqueness. facts and figures. However, the websites give a useful and
This applies especially to so-called non-descript local popu- informative overview of a certain set of breeds, usually
lations, which often merge gradually into neighbouring including images, while their outreach may be limited by
populations. Molecular characterization studies help to the use of the national language. The website of the Devon
unravel such relationships, but need to be better coordi- Cattle BreedersÕ Society may serve as an example (http://
nated and the results better combined. redrubydevon.co.uk). It hosts information on the breedÕs
history, the breed society and lists perceived strong points of
the breed such as ÔHigh Daily Weight GainsÕ or ÔLongevityÕ.
Production environment recording
Interested readers find contact addresses for further
Descriptions of breedsÕ production environments are information.
important for many aspects of FAnGR management. They Second, after the ÔConvention on Biological DiversityÕ was
can be used to make inferences regarding the breedsÕ adopted at the United Nations Conference on Environment
characteristics, based on the assumption that being exposed and Development held in Rio de Janeiro in 1992, national
to particular climates, feed resources and pathogens will websites have been put in place by each country, with a
over time have led to genetic differences in adaptation to complete coverage of those breeds considered to be part of
environmental conditions. A comprehensive description of their national heritage. An English version or at least an
the production environment is also vital for meaningful English introduction is sometimes available. Two examples
evaluation and comparison of the performance of different are the German ÔCentral Documentation of Animal Genetic
breeds. More broadly, a deeper understanding of production ResourcesÕ (TGRDEU; http://www.tgrdeugenres.de/) and
environments – including socio-economic aspects such as the French ÔBureau des Ressources GenetiquesÕ (BGR; http://
markets – can help in the planning of the future use and www.brg.prd.fr). Again, visually appealing presentation
development of the breeds. may get more emphasis than inclusion of hard facts.
While descriptions of the production environments of Third, at the international level, only a few websites are
individual breeds – varying in their focus and level of detail available. The ÔBreeds of LivestockÕ website run by the
– can be found, comparisons are difficult; and too often University of Oklahoma (http://www.ansi.okstate.edu/
breeds are considered in isolation from their production breeds/) describes a respectable number of breeds of live-
environments. Efforts have therefore been made to develop a stock, including cattle, goats, horses, sheep, pigs, buffalo,
recognized set of Ôproduction environment descriptorsÕ to be camelids and poultry, with differing degrees of detail. A
used throughout the world as a common framework for similar website, solely for cattle, has been compiled by a
describing production environments and to provide a basis South African company (http://www.embryoplus.com/
for recording more detailed production environment data cattle_breeds.html). It contains phenotypic descriptions for
within DAD-IS (FAO 1998; FAO/WAAP 2008). Under the about 140 of 950 listed breeds. As both websites are in
proposed framework, a production environment is divided English, they are useful for a wide audience.
into two main domains, the management environment and While the above websites tend to address only within-
the natural environment. These domains are further broken country biodiversity with little or no factual data on
down into a hierarchy of criteria. Most of the measures performances and census data, the EAAP (European Asso-
required for the natural environment domain (with the ciation for Animal Production) database – initiated in the
exception of the distribution of diseases and parasites) are 1980s – is based on a questionnaire and contains a large
now available on global high-resolution maps. Overlaying number of factual data items on breeds from all over Europe
these data with georeferenced breed distributions will allow (Simon 1990). It was the basis of FAOÕs DAD-IS, which was
more comprehensive descriptions and analyses of the redesigned to become FABISnet, a worldwide network
production environments. As noted above, georeferencing consisting of communicating national and regional data-
breed distributions is therefore a priority. bases (Groeneveld et al. 2006).
These information systems target true global coverage, as
all FAO member countries have agreed to report their breed
Breed description databases
data to DAD-IS, now the FAO node of FABISnet, through
Creating awareness through information dissemination is their officially appointed National Coordinators for the
considered an important component in conservation and Management of Animal Genetic Resources. In contrast to
utilization of genetic resources. Accordingly, a number of other databases, factual information is stored in more than
websites try to address this issue, often from different per- 200 clearly defined fields, allowing targeted database
spectives. Three groups of databases can be identified: searches.

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 Genetic diversity in farm animals 9

Furthermore, its multiple language capability and net- A comparison of European, Southwest-Asian and Indian
working allows the setup of national databases, while cattle reveals a gradual autosomal indicine-taurine cline
ensuring seamless integration into the worldwide network from India to Anatolia and a sharper cline of the mtDNA
headed at the FAO in Rome. Currently, a network of 13 and Y-chromosomal markers (Loftus et al. 1999; Troy et al.
national systems (Austria, Cyprus, Georgia, Estonia, Ice- 2001; Kumar et al. 2003; Edwards et al. 2007a). A meta-
land, Ireland, Italy, The Netherlands, Poland, Slovakia, analysis of different microsatellite datasets revealed patterns
Slovenia, Switzerland and the United Kingdom) all over of diversity and taurine–zebu admixture over Europe,
Europe is linked to the European EFABIS node (http://efa- South-West Asia and Africa (Freeman et al. 2006a).
bis.tzv.fal.de), which in turn is connected to FAOÕs DAD-IS In Asia, zebu and taurine cattle dominate in the south
(http://www.fao.org/dad-is/). This regional setup can serve and the north respectively. This again established central
as a model for other regions of the world, and FABISnet will hybrid zones in China (Cai et al. 2006, 2007; Lai et al.
likely expand in the near future. 2006; Zhang et al. 2007a) and Central Asia (Kantanen et al.
Compared with others, the FABISnet databases are the 2009). More to the north, indicine mtDNA was found in
most comprehensive, with data from 198 countries and Mongolia (20%), but Japanese and Korean cattle are com-
territories for more than 14 000 populations from 37 spe- pletely taurine (Mannen et al. 2004). Kikkawa et al. (2003)
cies, including descriptions of morphology, performance, described male taurine introgression in zebus from Bangla-
reproduction and demographic data. A unique feature is desh and Nepal. Interestingly, of six Nepalese zebus, five
that the degree of endangerment is automatically computed carried the expected zebu mtDNA, but one animal originated
from the number of male and female breeding animals, or if via the maternal lineage from yak (Bos grunniens).
this is not available, from the total population size. While a Following the European discovery of America in 1492,
large number of breeds have been entered, the completeness cattle were brought over from Spain and Portugal. Later,
of the information still needs improvement. Indian zebu cattle were imported to Central and South
FABISnet goes well beyond breed descriptions as it is also America because of their adaptation to hot and dry condi-
a repository of documents related to the breeds, their con- tions. Because mainly bulls were imported and crossed with
servation and utilization. While being far from exhaustive in Creole cattle, the Brahman zebu breed carries taurine
all aspects, these websites provide a wealth of information mtDNA, while Brazilian Nellore and Gir carry both taurine
on the breeds of the world. and indicine haplotypes (Meirelles et al. 1999). The hump-
less Creole cattle are thought to be descendants of Iberian
imports, but depending on the breed 40–100% of the bulls
Genetic characterization in livestock
harbour the zebu Y-chromosome (Giovambattista et al.
2000; Ginja et al. 2010). For Argentinean and Bolivian
Cattle
Creole cattle, autosomal microsatellites indicate 2–5% zebu
Traditionally, taurine cattle (Bos taurus) and zebu (Bos in- admixture (Liron et al. 2006b). A network analysis of mi-
dicus) are considered as separate species despite their com- crosatellite-based genetic distances and model based clus-
plete interfertility (Lenstra & Bradley 1999). One of the first tering showed an intermediate position of five Brazilian
contributions of DNA research to a reconstruction of the Creole breeds between modern taurine and Brazilian zebu
domestication of cattle was a comparison of the mitochon- breeds with 10–20% zebu introgression (Egito et al. 2007).
drial DNA (mtDNA) of taurine and indicine cattle (Bradley Crosses of zebu and taurine with banteng (Bos javanicus),
et al. 1996). The divergence of their control regions implied which are wild cattle from Southeast Asia, yield fertile female
separate domestications, which most likely started and sterile male offspring (Lenstra & Bradley 1999).
c. 8000 years BC in Southwestern Asia and the Indus valley Domestic cattle in Southeast Asia and Indonesia are thought
respectively (Zeder et al. 2006). to be of hybrid origin via crossing of zebu with Bali cattle,
Zebus were probably imported into Africa after the Arabian which is a domestic form of the banteng. Indeed, Kikkawa
invasions in the 7th century (Bradley et al. 1998). Interest- et al. (2003) and Mohamad et al. (2009) found banteng
ingly, the discovery that African zebus carry taurine mtDNA mtDNA in Indonesian zebus, most notably in the Madura
implies that African zebus were the result of crossing zebu (56%) and Galekan (94%) breeds. The mixed species origin of
bulls with taurine cows (Bradley et al. 1998). The resulting Indonesian zebus was confirmed by microsatellite analysis
distribution of taurine, indicine and mixed phenotypes (Mohamad et al. 2009). Analysis of mtDNA, Y-chromosomal
correlates with the Y-chromosomal INRA124 microsatellite DNA and microsatellites indicated a purely banteng origin of
alleles (Hanotte et al. 2000), satellite DNA polymorphism and Indonesian Bali cattle. However, mtDNA and nuclear DNA in
AFLP patterns (Nijman et al. 1999). Microsatellite genotypes a Bali cattle population kept in Malaysia was of mixed
allowed a reconstruction of zebu migration routes (Hanotte zebu-banteng origin (Nijman et al. 2003).
et al. 2002). In West Africa, zebu introgression is counter- The wild ox or aurochs (Bos primigenius), which is the
acted by the tsetse resistance of the native taurine breeds ancestor of both taurine and indicine cattle, lived in the
(Freeman et al. 2004, 2006b; Ibeagha-Awemu et al. 2004). European forests until its extinction in 1627, so hybridization

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10 Groeneveld et al.

with domestic cattle originating from Southwestern Asia were most likely introduced during the Middle Ages (Felius
(Troy et al. 2001) is an obvious possibility. In 59 fossil aur- 1995).
ochs bones, Edwards et al. (2007b) found one mtDNA ha- Second, the T1 haplogroup has appreciable frequencies in
plogroup (P) in all except one sample, which had a different several Spanish and Portuguese breeds (Cymbron et al.
haplotype (E). Both P and E are distinct from the taurine 1999; Miretti et al. 2004; Beja-Pereira et al. 2006; Cortés
haplogroup T. This would exclude a recruitment of aurochs et al. 2008; Ginja et al. 2010), indicating migration from
cows for use as livestock, but exceptions seem to confirm the Africa to the north. This may have occurred either during
rule: the P haplotype is present in less than 0.1% of modern the Neolithic movement of cattle or later, for instance dur-
cattle samples (Achilli et al. 2009; Stock et al. 2009), while ing the Islamic occupation. Importation of Iberian cattle
the related Q and R haplotypes are also found sporadically into the newly discovered American continent explains the
(Achilli et al. 2008, 2009). relatively high frequency of the T1 haplogroup in Caribbean
However, the extent to which aurochs contributed to and South American cattle (Magee et al. 2002; Carvajal-
modern cattle via male introgression is not yet clear. Gö- Carmona et al. 2003; Mirol et al. 2003; Miretti et al. 2004;
therström et al. (2005) defined a Y1 haplotype in most Liron et al. 2006a,b; Ginja et al. 2010).
North-European breeds and a Y2 haplotype in most other Autosomal protein polymorphisms (Medjugorac et al.
European cattle and in Southwest Asia. Y1 was also found 1994), microsatellite data (Cymbron et al. 2005; Li et al.
in fossil aurochs remains, but this was not in agreement 2007; Medugorac et al. 2009) and AFLP fingerprinting
with later findings (Svensson & Götherström 2008). Bol- (Negrini et al. 2007) are in line with a demic expansion of
longino et al. (2008) found Y2 haplotypes in several Euro- agriculture from southeastern to northwestern Europe.
pean samples for which the aurochs origin was verified via Cymbron et al. (2005) observed that the correlations be-
the mtDNA P-haplotype, which raises the possibility that Y2 tween genetic and geographical distances are different for
carrying bulls have also descended from aurochs bulls. Mediterranean and Northern breeds; it is proposed that this
Mitochondrial DNA, as well as nuclear polymorphisms, reflects the separate Neolithic migrations along the Medi-
have revealed several other aspects of the early differentia- terranean coasts and the Danube respectively. A larger set
tion of taurine cattle. The predominance of one taurine of microsatellite data (Lenstra et al. 2006b; Lenstra 2008)
mtDNA haplogroup (T1) in Africa (Troy et al. 2001) and a indeed indicates a separate position of Mediterranean cattle,
new haplogroup in Eastern Asia (T4: Mannen et al. 2004; but divides the Transalpine cattle into two different clusters
Kantanen et al. 2009) suggested two other regions of of breeds: Central-European (Alpine, Southern-French) and
domestication. However, complete mtDNA sequences Northern European. The separate position of Central-Euro-
showed that T1 and T4 are closely related to the major T3 pean cattle was also indicated by AFLP data (Negrini et al.
haplogroup, so their predominance probably reflects foun- 2007). Strikingly, the Northern-European cluster largely
der effects in Africa and Eastern Asia respectively (Achilli coincides with a high diversity of milk protein genes (Beja-
et al. 2009). Pereira et al. 2003), the distribution of the human lactase
The T3 mtDNA haplogroup is predominant in most persistence alleles and the location of Neolithic cattle
European breeds and Northern Asia (Kantanen et al. farming sites. This led to the suggestion of a gene-culture
2009) and is one of the four major haplogroups (T, T1, T2 co-evolution between cattle and humans (Beja-Pereira et al.
and T3) in Southwestern Asia. By contrast, in the African 2003).
taurine cattle haplogroup T1 is dominant, which is rare in Predictably, SNP data (e.g. Gautier et al. 2007; Svensson
Southwestern Asia. These observations are in line with a et al. 2007; McKay et al. 2008; The Bovine HapMap Con-
Southwest-Asian origin of European cattle, confirming the sortium et al. 2009) will reveal more about the history of
paleontological evidence of a gradual introduction of European cattle. AFLP polymorphisms, as proxy for SNP
domestic cattle in Europe from Southwestern Asia (Zeder diversity, suggested that relative to microsatellites SNPs
et al. 2006). There are two interesting exceptions to the emphasize the zebu-taurine divergence and hence also the
T3 dominance in Europe. First, four ancient breeds from difference between Podolian and other European cattle
Tuscany have almost the same mtDNA diversity as found (Negrini et al. 2007). Large-scale SNP analysis (Gautier
in Southwestern Asia, suggesting an ancient maternal et al. 2007; The Bovine HapMap Consortium et al. 2009)
origin and a direct link between Tuscan and Western- indicated that in several breeds linkage disequilibrium (LD)
Asian cattle (Pellecchia et al. 2007). For the Chianina extends further than in humans, but is hardly detectable at
breed this was confirmed by microsatellite data (European distances over 200 kb. These data also suggested a rapid
Cattle Genetic Diversity Consortium, unpublished results). recent decrease of the effective population size of domestic
Microsatellites also indicated that two other Tuscan cattle. Also promising is the differentiation of several Y1 and
breeds, the Maremmana in the south and the Cabannina Y2 haplotypes that as markers of paternal lineages will be
in the north have been subject to Podolian and Brown informative for introgression and upgrading (Svensson &
Mountain breed introgression respectively. Cattle east of Götherström 2008; Ginja et al. 2009; Ginja et al. 2010;
the Appennines and on Sicily are of the Podolian type and Kantanen et al. 2009).

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 Genetic diversity in farm animals 11

Molecular data have also generated information on the unique livestock species on the Qinghai-Tibetan Plateau of
history of individual breeds. A major determinant of the western China, in the Mongolian and Russian steppes and
genetic constitution of a breed is its degree of isolation from in other Himalayan countries (Wiener et al. 2003; Wiener &
other breeds. For instance, the Jersey is a typical island Jianlin 2005). The state of development of molecular
breed that has been kept isolated since 1789. This has led to markers and genetic research on the yak was reviewed by
a limited degree of inbreeding (Chikhi et al. 2004), but has Jianlin (2003).
also preserved unique features. Inbreeding has gone further Recently, the genetic diversity of yak has been examined.
in two Balearic Island breeds, in a Betizu subpopulation mtDNA cytochrome b and D-loop sequences revealed two
(Martin-Burriel et al. 2007), and in the Spanish Lidia halogroups within domestic yak, which diverged at least
(fighting cattle: Cañón et al. 2008). The most extreme 100 000 years ago (Guo et al. 2006; Lai et al. 2007).
inbreeding has been observed in English Chillingham cattle, Haplotypes of both groups were found in a single, small,
which have become almost completely homogeneous by wild yak population, thus indicating that the domestic
strict isolation of one herd for hundreds of years (Visscher Chinese yak were derived from a single wild gene pool. A
et al. 2001). Often, but not always, genetic isolation has led domestication event was estimated to have taken place
to phenotypic uniqueness. This has also been the case for around the early Holocene, within 10 000 years before
the Italian Chianina (see above) and is an obvious argument present (YBP) in Qinghai and Tibet. No pattern of phylo-
for conservation. geographical distribution of major clades in Chinese yak
At the other end of the scale are the several breeds that sampled from different localities in south-western and
have been shaped by gene flow from other breeds. For in- north-western China was found (Guo et al. 2006; Lai et al.
stance, Northern-Russian cattle have been influenced 2007). A study with intensive sampling of domestic yak
heavily by modern commercial cattle (Li et al. 2007; from all the yak-keeping countries, including China,
Kantanen et al. 2009). On a comparable scale, several Bhutan, Nepal, India, Pakistan, Kyrgyzstan, Mongolia and
Scandinavian breeds have been upgraded by the Scottish Russia, revealed a third, less frequent, haplogroup (Qi et al.
Ayrshire (Tapio et al. 2006a). A rustic Spanish breed, Serr- 2008). Geographical clines in the haplogroup diversity
ana di Teruel, was clearly influenced by brown mountain indicated that a single domestication on the Eastern Qing-
cattle (Martin-Burriel et al. 2007). Several other introgres- hai-Tibetan Plateau was followed by a westward migration
sions have been indicated by a Europe-wide microsatellite passing through the Himalayan and Kunlun mountain
dataset (European Cattle Genetic Diversity Consortium, ranges, and northward migration through South Gobi and
unpublished results). This has been rather extreme for the the Gobi Altai mountains to Mongolia and Siberia.
Portuguese Minhota, which has been upgraded with Cross-species amplification of 136 bovine microsatellite
German Yellow bulls (Felius 1995) to the point that it has markers revealed a high success rate up to 95% (Minqiang
become virtually identical to the German breed. et al. 2003; Nguyen et al. 2005; Xuebin et al. 2005). Sev-
Genotypes from 30 microsatellites for 69 European breeds eral of these are included in the list of markers recom-
were used for testing formal criteria for conservation (Len- mended by the ISAG/FAO working group for yak (Hoffmann
stra & the European Cattle Genetic Diversity Consortium et al. 2004). Using 15 microsetellites, Xuebin et al. (2005)
2006a). The popular Weitzman method, based on genetic found high genetic diversity within the Mongolian and
distances, favours highly inbred populations even if these Russian yak populations. The Gobi Altai, south Gobi and
have been derived recently from other populations. Ranking north Hangai populations in Mongolia are closely related, as
of conservation priorities on the basis of marker-estimated are the Hovsgol and the Buryatia populations in Mongolia
kinships was less influenced by inbreeding, and favoured and Russia respectively. These groups of populations should
Mediterranean breeds (Lenstra & the European Cattle therefore be considered as distinct genetic entities for con-
Genetic Diversity Consortium 2006a). These breeds indeed servation and breeding programmes.
have a relatively high degree of molecular diversity, which Cross-species amplification of bovine Y-chromosome spe-
next to phenotypic uniqueness is an obvious argument for cific markers now allows the analysis of paternal lineages
conservation. Moreover, the Busa and Anatolian breeds (Xuebin et al. 2002). In addition, a complete yak mtDNA
were considered to be valuable genetic resources on the genome sequence (Gu et al. 2007) and several bovine SNPs
basis of their high genetic diversity (Medugorac et al. 2009). that are also polymorphic in yak will contribute further to
Conservation priorities of Nordic cattle were analysed by the understanding of the genetic constitution of yak popu-
Bennewitz et al. (2006) and Tapio et al. (2006a). lations.

Yak Water buffalo

Yak (Poephagus grunniens) is a bovine species that can The domestic water buffalo Bubalus bubalis is thought to
hybridize with taurine and zebu cattle and produce fertile have been domesticated in the Indus and Yangtze valley
females but sterile males (Lenstra & Bradley 1999). It is a civilizations 5000 years ago (Cockrill 1981). Domestication

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12 Groeneveld et al.

was also proposed to have occurred in China as early as (Tanaka et al. 1996). A study of 30 microsatellites found a
7000 years ago (Chen & Li 1989). However, this was not in river-swamp differentiation of 30.2% (Zhang et al. 2007b),
agreement with mtDNA sequences of ancient remains of the and studies of mtDNA found an average sequence diver-
endogenous Bubalus mephistopheles, which did not establish gence of 8.6% for D-loop and 2.6% for cytochrome b (Ku-
a link with the modern domestic water buffalo (Yang et al. mar et al. 2007a), of the same order as the differentiation
2008). Representations of buffalo appear on seals of the between Bos taurus and Bos indicus in cattle.
Indus valley and Mesopotamia from the third millennium BC Initial analyses of a short region of the mitochondrial D-
(Zeuner 1963). The ancestral wild water buffalo Bubalus loop found haplotypes shared between river and swamp
arnee was common across the Indian subcontinent, but buffalo, which is consistent with a single domestication
numbers have decreased because of environmental pres- event (Lau et al. 1998; Kierstein et al. 2004). However,
sures and hybridization with domestic populations. The wild studies of longer regions of the D-loop and of cytochrome b
form is now listed as endangered and is thought to survive all support the hypothesis of separate domestications of river
only in a few areas of India, Nepal, Bhutan and Thailand and swamp buffalo, probably in the Indus and Yangtze
(Scherf 2000). valley civilizations in the second millennium BC (Kumar
Water buffalo have historically been divided into swamp et al. 2007b; Lei et al. 2007). Research into Chinese swamp
and river buffalo based on morphological, behavioural and buffalo populations revealed two maternal lineages: Swamp
geographical criteria. The two types also differ in chromo- A and B. The more common lineage A was found in 81.5%
some number: swamp 2n = 48, river 2n = 50 (Ulbrich & of samples, but lineage B was present in five of the seven
Fischer 1967; Fischer & Ulbrich 1968), because of a telo- populations sampled, with no clear geographical pattern of
mere-centromere tandem fusion between two chromosomes A and B distribution. The estimated time of divergence of
in river buffalo (Di Berardino & Iannuzzi 1981). River and the two lineages was 18 000 YBP, and while both show
swamp buffalo will only mate if reared together from calf- indications of population expansion, lineage A appears to be
hood and while first generation hybrids are fertile it has not a more recent expansion (Lei et al. 2007).
been confirmed whether fertility persists in subsequent Microsatellite analyses in buffalo have focused on the
generations (Fischer & Ulbrich 1968). They are sometimes defined river breeds of India and local swamp populations of
referred to as different subspecies; river as Bubalus bubalis China. Most genetic diversity in buffalo lies within breeds,
bubalis and swamp as Bubalus bubalis carabenesis. Swamp and estimates of the percentage of diversity between popu-
buffalo bear a closer morphological resemblance to wild lations vary between 2.8% in Chinese swamp populations
buffalo than do river buffalo. (Zhang et al. 2007b), 3.4–9.69% in Indian river breeds and
Swamp buffalo are found throughout Southeast Asia and local populations (Kumar et al. 2006; Vijh et al. 2008), and
China. There are no recognized breeds, although some 5.7% in Italian, Greek and Egyptian river breeds (Moioli
geographical populations have local names and have been et al. 2001). Most of these values are low compared with
shown to differ in morphology and environmental adapta- other species [7.11% for cattle (MacHugh et al. 1998), 8%
tion (Chen & Zu 2004). River buffalo are mainly found in in horses (Cañón et al. 2000), 13% in pigs (Martinez et al.
the Indian subcontinent and westwards through South- 2000)]. This may be because buffalo have not undergone
western Asia and Mediterranean countries. Buffalo have the same degree of isolation and rigorous selection and
recently been introduced to Africa, South America and widespread use of artificial insemination in the creation of
Australia. Well-recognized and morphologically defined established breeds. Mean expected heterozygosity also varies
river buffalo breeds exist in India and Pakistan, but 70% of between studies; it was 0.535 in Chinese swamp popula-
river buffalo do not belong to any named breed and are tions (Zhang et al. 2007b), 0.506 in Southeast-Asian
classified as non-descript (Arora et al. 2004). The geo- swamp populations (Barker et al. 1997a), 0.71–0.78 and
graphical ranges of river and swamp buffalo overlap in East 0.63–0.73 in Indian river populations (Kumar et al. 2006;
India and Bangladesh. Sri Lankan buffalo are morphologi- Vijh et al. 2008), and 0.577–0.605 in river buffalo of
cally similar to swamp buffalo but analyses of chromosome Mediterranean countries (Moioli et al. 2001).
number, microsatellites and mtDNA identify them as river The previous systems of grouping buffalo breeds based on
buffalo (Barker et al. 1997b; Lau et al. 1998). Genetic dif- morphology and geography (Cockrill 1981) do not correlate
ferentiation of both river and swamp populations is of the well with genetic diversity patterns. AMOVA analysis of mi-
same order of magnitude as that between well-recognized crosatellite data found that, when Indian breeds were di-
breeds of other domestic species (Barker et al. 1997b). vided by either geography or morphology, <1% of the
Estimates of the time of divergence of river and swamp genetic diversity lay between groups (Kumar et al. 2006).
buffalo vary widely, but all predate the domestication of However, a DA distance tree and principal component and
buffalo. The estimates range between 10 000–15 000 YBP STRUCTURE analyses of microsatellite genotypes in Chinese
(Barker et al. 1997a), 28 000–87 000 YBP (Lau et al. swamp buffalo populations revealed several geographical
1998), more than 700 000 YBP (Tanaka et al. 1995), clusters: in the upper and middle reaches of the Yangtze
1 million YBP (Amano et al. 1994) and 1.7 million YBP valley, in the lower reaches of the valley, in Southern China

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 Genetic diversity in farm animals 13

and in Southwestern China. The first two components of the found in Portugal, Turkey, the Caucasus and China (Tapio
principal component analysis also divided populations on et al. 2006b). Haplotype D, present in Rumanian Karachai
North/South and East/West axes (Zhang et al. 2007b). The and Caucasian animals, is possibly related to the A haplo-
genetic distances between Chinese populations also corre- type. Haplotype E, which is intermediate between A and C,
lated with the geographical distance between them; one is also rare and has only been found in two Turkish animals.
study of Indian populations found no such correlation and This mtDNA diversity with distinct haplogroups is com-
another only found it after the removal of a population and parable with what is observed in goats and cattle, although
several loci, which were out of Hardy–Weinberg equilibrium the divergence of sheep haplogroups is less pronounced
(Kumar et al. 2006; Zhang et al. 2007b; Vijh et al. 2008). than the taurine–zebu divergence (Bruford et al. 2003).
Most analyses of river buffalo have focused on the minority Furthermore, in contrast to the taurine cattle haplotypes,
that form recognized breeds. Inclusion of two local non-de- the sheep haplogroups hardly correlate with geographical
script populations in a microsatellite study showed similar origin. Different lineages might reflect multiple regions of
levels of within- and between-population diversity as the origin, but another obvious possibility is a coexistence of
recognized breeds (Vijh et al. 2008). Such local populations different maternal lineages in the predomestic population.
may be valuable reservoirs of genetic diversity, which is By contrast, little variation has been observed in the
threatened by modern breeding practices. Murrah buffalo are paternal lineage. One SNP in the Y-chromosomal SRY
a popular breed, and increased use of Murrah sperm for mutation has a high frequency in European breeds (Mead-
artificial insemination is decreasing the genetic diversity ows et al. 2004) and is probably of European origin. The
between buffalo populations (Sethi 2001). In a multidimen- microsatellite SRYM18 defines other haplotypes (Meadows
sional scaling analysis of microsatellite data, Murrah buffalo et al. 2006), but except for the major haplotypes, these were
cluster with several other breeds of northern, central and of low frequency and dispersed over different continents.
western India, possibly because of this ongoing admixture. A recent study of retrovirus integrations (Chessa et al.
The Toda breed is reared by the Toda tribe in the Nilgiri hills 2009) has provided additional information on the intro-
of South India and is both culturally and religiously signifi- duction of sheep into Europe. A high frequency of one
cant to the tribe, and is also endangered as a result of its low integration or the lack of other integrations indicated an
numbers. Microsatellite and mtDNA studies identified the early arrival of the primitive sheep populations (European
Toda breed as genetically distinct from other recognized mouflons, North-Atlantic Island breeds). Another informa-
breeds and in need of conservation, but Vijh et al. (2008) tive retrovirus copy is present in most other European breeds
found that the geographically close local population of and probably indicates the later arrival of wool-producing
Kalasthi buffalo cluster with the Toda breed, demonstrating sheep. This study also indicated an interesting genetic link of
the importance of considering local populations as well as English Jacob sheep with Asian or African populations.
breeds when deciding on conservation priorities. Although several groups have studied the diversity of
sheep as revealed by microsatellites, this has provided rel-
atively little insight into the relationship between breeds.
Sheep
One drawback is the unfortunate use of different microsat-
Sheep (Ovis aries) were domesticated in Southwestern Asia ellite panels, which precludes the combination of datasets
about 12 000 years ago and thus represent one of the (for an overview, see http://www.globaldiv.eu/docs/Micro-
earliest livestock animals (Zeder et al. 2006). As with other satellite%20markers.pdf). Another drawback is that there is
domestic animals (Bruford et al. 2003), relationships with only little phylogeographical structure; this in contrast to
ancestor species have been investigated via comparison of the clear correlation of genetic and geographical structure
mtDNA data. Hiendleder et al. (2002) found two haplo- observed in cattle and goats. In a study of 20 European
groups A and B, which both were different from the se- breeds, AMOVA analysis showed that only 1% of the variation
quences in any extant Ovis species. The European mouflon is between regions and less than 3% is between seven types
(Ovis musimon) carries haplogroup B, but this is a feral form of breed (Lawson Handley et al. 2007). In Baltic breeds,
of early European domesticates. Most likely, sheep descend Tapio et al. (2005a) found a general lack of differentiation
from one or more Asiatic mouflon (Ovis orientalis) popula- at the breed level.
tions (Hiendleder et al. 2002). On the other hand, with eight microsatellites, Buchanan
Several reports have further analysed the geographical et al. (1994) observed a clustering of three English breeds
distribution of haplotypes. The most relevant information relative to Merino-type breeds and to Awassi. So far, most
has been summarized by Meadows et al. (2007). The main data on phylogeographical relationships of breeds came from
haplotypes A and B are both found in Asia, while B domi- the EU Econogene project, which analysed 57 breeds with 31
nates in Europe (see also Bruford et al. 2003; Meadows et al. microsatellites (Peter et al. 2007). Separate positions were
2005). A high frequency of A in New Zealand resulted from observed for three clusters of breeds: Southwest-Asian,
early imports of Indian animals into Australia (Hiendleder Southeast-European and Central- and Western-European.
et al. 2002). Haplotype C is less frequent, but has been Within the last group, there was a weak differentiation of

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14 Groeneveld et al.

Merino and Alpine breeds. There was also a clear decline of diversity of the C-haplogroup indicated a second domestica-
the heterozygosity and allelic richness from Southwestern tion on the Central Iranian plateau and in the Southern
Asia and Southeastern Europe to the west and the north-west Zagros, but this domestication centre probably did not con-
(Peter et al. 2007), reflecting repeated founder effects during tribute significantly to the current domestic goat gene pool.
the gradual introduction of domestic sheep into Europe. Mitochondrial DNA haplotypes suggested a genetic link
In another study, independent coordination analysis between Southwest-Asian and Iberian goats (Pereira et al.
suggested a separate position of Northern-European short- in press) and between Southern/Central American goats
tailed sheep, which could be divided into a north-western, and Canarian goats (Amills et al. 2009), both via maritime
northeastern and a heterogeneous Swedish-Norwegian transport.
cluster (Tapio et al. 2005b). Santos-Silva et al. (2008) The prevalent notion that the geographical structure of
studied the relationships of Portuguese sheep, which were goats is weaker than for cattle and sheep (Luikart et al.
clearly different from the imported Assaf breed. Cinkulov 2001) rests mainly on the worldwide prevalence of haplo-
et al. (2008) analysed genetic differentiation of the Pra- group A. However, the dispersal of A haplotypes seems to be
menka, an indigenous mountain sheep breed of the Balkans. predomestic, and Y-chromosomal data show considerable
Furthermore, Gizaw et al. (2007) observed a partial differ- geographical partitioning. Three Y-chromosomal haplo-
entiation of three breed groups that had been successively types belong to two haplogroups, Y1 and Y2 (Lenstra 2005;
introduced to Ethiopia: thin tailed, short- and long-fat-tailed Pereira et al. in press). Y2 has not been found in Switzerland
and thick-rumped breeds. and Germany and is scarce in Italy, while it is predominant
The differentiation of European and Asian sheep and the elsewhere.
weak geographical structure of European sheep were con- Microsatellites also reveal a high degree of geographical
firmed by analysis of a 1536-SNP dataset (Kijas et al. 2009). structuring, although incompatibility of datasets again
This study also showed a difference between Asian and limits the scope of most studies to the regional scale. Barker
African populations and a separate position of the North- et al. (2001) found a clear correlation of tree topology and
Atlantic Soay sheep. genetic distance for Southeast Asian goats. The largest
The diversity pattern of European sheep breeds, which is dataset described so far (Cañón et al. 2006) comprises 45
clearly more panmictic than observed for cattle and goats, breeds from Europe and the Middle East. Four discrete
probably reflects a history of cross-breeding promoted by groups were found: Middle East, central Mediterranean,
commercial interests (Lenstra 2005). From the 17th cen- western Mediterranean and central/northern Europe. Again
tury onwards, Merino sheep from Spain were exported to there was a decline in allelic richness from south-east to
several European countries (Wood & Orel 2001), while north-west, presumably the result of founder effects that
English or Texel rams were also popular sires. also explain the distribution of Y-chromosomal alleles (Ca-
ñón et al. 2006). Geographical structuring of microsatellite
genotypes was also reported for goat populations from
Goats
Burkina-Faso (Traoré et al. 2009), India (Rout et al. 2008)
Goats (Capra hircus) were domesticated about 10 000 years and northern Vietnam (Berthouly et al. 2009). Conserva-
ago in Southwestern Asia, thus in the same period and in tion value of Swiss goat breeds on the basis of microsatellite
the same region as sheep. Although the species are of a diversity was explored by Glowatzki-Mullis et al. (2008).
similar size, goats found their own use because of their The clear phylogeographical structure of European goats
adaptation to marginal conditions. Goats most likely des- probably reflects the style of husbandry. In contrast to the
cend from the wild bezoar, Capra aegagrus, (Naderi et al. situation of sheep and cattle and with the exception of the
2007, 2008). The information available on mtDNA haplo- widespread use of Swiss dairy animals, goats are of more
groups has been summarized by Naderi et al. (2007). More limited economic importance, and breeding has remained
than 90% of goats worldwide carry haplogroup A. Haplo- largely a local affair.
group B has so far been found mainly in Asia and South In the Econogene dataset, Western Europe was only
Africa, C in Southern Europe, D in Asia, F only in the partially represented. Comparison with Asian and African
Sicilian Girgentata breed, and G in Southwestern Asia and breeds will probably define additional clusters of breeds. We
Northern Africa. Subgroup B1 is restricted to China and conclude that further molecular analyses of autosomal and
Mongolia. Another subgroup of B is reported to be specific to Y-chromosomal diversity of goats offer excellent perspec-
the Canary Islands, which is possibly due to their genetic tives to retrieve the history of their domestication and
isolation since their arrival 3000 years ago (Amills et al. subsequent migrations.
2004). Data on African goats are relatively scarce.
Haplogroups A–G are all present in the bezoar goat (Naderi
Camelids
et al. 2008). The distribution of the haplogroups suggested
that eastern Anatolia and possibly Northern and Central The Camelidae family comprises four domesticated species
Zagros were the most important domestication centres. The belonging to three genera. The Bactrian camel (Camelus

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 Genetic diversity in farm animals 15

bactrianus) is found throughout Central Asia, and the dis- with the Mewari breed being differentiated from the Bika-
tribution of the dromedary (Camelus dromedarius) ranges neri, Kutchi and the Jaisalmeri breeds.
from Central Asia and Southwestern Asia to Northern For the New World camelids, Rieder et al. (2000) found
Africa. The llama (Lama glama) and alpaca (Vicugna pacos) high genetic variation at six microsatellite loci within Swiss
are found in the Andean mountains in South America New World camelid breeds. Sarno et al. (2001) observed
(Jianlin 2005a,b). All species of the family have the same much less variation in an island guanaco population than
conservative karyotype (2n = 74) and can produce fertile in the mainland population and a significant genetic dif-
hybrids between species, both within and even between ferentiation between the two populations in southern Chile.
genera (Skidmore et al. 1999; Potts 2004; Mengoni Bustamante et al. (2002) and Maté et al. (2005) reported a
Goñalons & Yacobaccio 2006; Wheeler et al. 2006). high level of genetic diversity in Argentine llamas and
mtDNA sequences and nuclear microsatellite markers sup- guanacos, indicating the Patagonian guanaco to be an
port a clear genetic differentiation of wild guanaco (Lama important genetic resource for conservation or economic
guanicoe) from wild vicuña (Vicugna vicugna) (Stanley et al. utilization programmes. Sarno et al. (2004) detected higher
1994; Kadwell et al. 2001; Palma et al. 2002). They also levels of microsatellite allelic diversity in V. v. mensalis than
provide genetic evidence for two geographically isolated in V. v. vicugna in Bolivia and Chile.
wild subspecies of the guanaco (L. g. cacsilensis and The structure and organization of the D-loop region of
L. g. guanicoe) (Palma et al. 2002; Gonzalez et al. 2006) and four South American camelid species in Argentina were
the vicuña (V. v. vicugna and V. v. mensalis) (Palma et al. reported by Maté et al. (2004, 2007), and a high degree of
2002; Marı́n et al. 2007). Independent domestications of heteroplasmy was found. Complete mtDNA sequences and
the llama from L. g. cacsilensis and the alpaca from structure are available for alpacas (Ursing et al. 2000;
V. v. mensalis have subsequently been demonstrated (Palma Arnason et al. 2004), a dromedary (16 643 bp) and
et al. 2002; Wheeler et al. 2006). These occurred 4000– domestic and wild Bactrian camels (Cui et al. 2007). Geno-
4500 YBP for llama in the South-Central Andes (Mengoni mic sequence data with 2· coverage (OÕBrien et al. 2008)
Goñalons & Yacobaccio 2006) or 6000–7000 YBP for both and the identification of 1516 microsatellite loci (Reed &
alpaca and llama in the Central Andes (Wheeler et al. Chaves 2008) as well as 750 000 SNP markers of alpaca
2006). mtDNA analyses recognize the extant wild Bactrian will facilitate further studies of the diversity of camelids.
camel as a separate lineage (Jianlin et al. 1999; Ji et al.
2009). Combined mtDNA and microsatellite data further
Pigs
support the recognition of the wild Bactrian camel as a
separate subspecies (Camelus gobi or Camelus bactrianus gobi), Molecular data have shed light on pig domestication by
and suggest different ancestors and separate domestication tracing mtDNA. Initial mtDNA studies showed that Euro-
events for the dromedary and the Bactrian camel (H. Jianlin pean and Chinese pigs were domesticated independently
et al. unpublished data). For the Bactrian camel, this took from European and Asian subspecies of wild boar (Giuffra
place 4000 YBP in the eastern part of Central Asia (Mason et al. 2000), but later studies suggested at least seven
1984; Peters & von den Driesch 1997; FAO 2007b). For the domestication events across Eurasia (Larson et al. 2005)
dromedary, this occurred 4500–5000 YBP in the Southern and East Asia (Wu et al. 2007). These studies also suggested
Arabian Peninsula (Mason 1984; Peters 1997). the occurrence of introgression of Asian domestic pigs into
Jianlin (2005a) have reviewed the development of cam- some European breeds during the 18th and 19th centuries.
elid microsatellite markers. Recently, Maté et al. (2005) Larson et al. (2007) demonstrated that domestic pigs of
reported an additional four microsatellite markers. Twenty- Near Eastern ancestry were introduced into Europe during
five markers are included in the current list of markers the Neolithic, and that the European wild boar was also
recommended by the ISAG/FAO working group for both the domesticated by this time. Once domesticated, European
New and Old World camelids (Hoffmann et al. 2004). So far, pigs rapidly replaced the introduced domestic pigs of Near
these markers have been used only for studies with a re- Eastern origin throughout Europe.
gional scope. Jianlin et al. (2004) suggested that the Y-chromosomal variation demonstrated the existence of
domestic Bactrian camels from China and Mongolia should two highly divergent and ancient lineages, with an esti-
be considered as distinct populations in conservation and mated divergence time of c. 0.33 Myr, i.e. in the order of the
breeding programmes. Nolte et al. (2005) found no evidence species age (O. Ramı́rez, personal communication). A recent
for loss of genetic diversity within, and a very low differ- study (Ramirez et al. 2009) based on microsatellite, mtDNA
entiation among 16 southern African dromedary popula- and Y-chromosomal data has confirmed the divergence of
tions. Mburu et al. (2003) identified two separate genetic East-Asian and European pigs. In both regions, wild and
entities present in Kenyan dromedaries, namely the Somali domestic populations were found to be related to each other.
dromedary and a group including the Gabbra, Rendille and All three marker types showed that Southwest Asian,
Turkana populations. Vijh et al. (2007) indicated that there African and American pigs were most closely related to
were two distinct genetic clusters in the Indian dromedaries, the European population, but East-Asian mtDNA and

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16 Groeneveld et al.

Y-chromosomal haplotypes occurred in East-African and have increased the extent of LD in Europe. The haplotypic
Nicaraguan populations. Anglosaxon, African local pigs diversity has also been studied in other material, focusing
and especially the international breeds (e.g. Large White, on the IGF2 gene (Ojeda et al. 2008).
Landrace and Pietrain) are of mixed European-Asian origin. The ongoing project PigBioDiv2 covers 50 Chinese breeds
The almost complete predominance of the HY1 Y-chromo- and mtDNA and Y-chromosomal regions in addition to the
somal haplotype in Europe, including in the international microsatellite data of the European breeds. Trait gene loci
breeds, and in Southwestern Asia, argues against male- and markers will be analysed to seek insight into the
mediated introgression and suggests that Chinese intro- functional differences between breeds. The first results on
gression in British breeds was mainly maternal. microsatellites using pooled DNA samples indicate that the
Fang et al. (2009) investigated genetic variation in the Chinese breeds show a higher degree of genetic variability
melanocortin receptor 1 (MC1R) gene among 15 wild and 68 than the European breeds both within and between breeds
domestic pigs from both Europe and Asia to address why (Megens et al. 2008).
coat colour is so much more variable in domestic animals Detailed studies have also been carried out for local breeds
than in their wild ancestors. They found that all mutations in several countries. The important local Iberian breed was
were silent in wild animals, suggesting purifying selection, analysed using microsatellite markers by Fabuel et al.
but nine of ten mutations found in domestic pigs resulted in (2004), who compared different methods, such as Weitz-
altered protein sequence, suggesting that early farmers man, cluster analysis or optimal contributions, to establish
intentionally selected for novel coat colour. conservation priorities. Moreover, Alves et al. (2003)
Across the world, nearly 400 breeds have been exploited, showed that, unlike other European breeds, the Iberian
the largest number of breeds being found in Asia and Eur- breed has not been introgressed with Asian mtDNA. Finally,
ope. In a collaborative EU project (PigBioDiv1), 58 European an allelic richness analysis indicated that the desirable
populations, including local breeds, national varieties of integration of allelic richness into the diversity theory cur-
international breeds, privately owned commercial popula- rently poses some unsolved difficulties (Rodrigáñez et al.
tions, and the Chinese Meishan breed as an outgroup were 2008).
genotyped for 50 microsatellites and 148 AFLP markers.
Data from 11 breeds included in the PiGMaP study (Laval
Horses
et al. 2000) were also included. The microsatellite data
showed that the individual breed contributions to between- A total of over 100 distinct equine mtDNA haplotypes have
breed diversity ranged from 0.04% to 3.94% of the total been described in multiple studies focusing on the domes-
European between breed-diversity, and that the local breeds tication of horses in general, or on the origin of specific
accounted for 56% of the total, followed by commercial lines breeds (Bowling et al. 2000; Vila et al. 2001; Jansen et al.
and international breeds (Ollivier et al. 2005). They also 2002; Kavar et al. 2002; reviewed in Kavar & Dovc 2008).
applied a cryopreservation potential criterion as proposed by Joint analyses showed that, in contrast to the double
Weitzman (1993), taking into account the risks of extinc- broomstick topology of mtDNA networks of the principal
tion. SanCristobal et al. (2006a), analysing the same data, livestock species (Troy et al. 2001; Bruford et al. 2003), the
showed a clear structure of the European pig breeds with a equine mtDNA network shows a typical star-like branching
FST value of 0.21. With the exception of five local breeds, structure (Jansen et al. 2002; Kavar & Dovc 2008). In a
the between-breed general structure exhibited a star-like dataset comprising extant horse breeds, as well as wild
tree with no visible phylogenetic relationship between the horses from 12 000 to 28 000 years ago, an unexpectedly
local and the main international breeds. Even the inclusion high genetic divergence between clades was found (Vila
of the Chinese Meishan breed as an outgroup did not allow et al. 2001). Analyses of DNA from horses of Chinese tombs
the tree of European breeds to be rooted. SanCristobal et al. from the 3rd century BC (Keyser-Tracqui et al. 2005) and
(2006b) proposed that AFLPs produce diversity patterns from the Bronze Age (Lei et al. 2009) showed that the high
similar to microsatellites and can be combined with micro- mtDNA diversity is of ancient origin. Clearly, the divergence
satellite data. However, Foulley et al. (2006) highlighted the of horse mtDNA must have predated domestication, which
problems arising in the analysis of these types of markers on the basis of archaeological evidence has been dated at
and suggested that AFLPs are more sensitive than micro- around 6000 YBP in a broad region of the Eurasian Steppe.
satellites to selection and/or other forces. This is consistent with the notion that capture and exploi-
Amaral et al. (2008) evaluated LD and haplotype block tation of wild mares took place independently in multiple
structure in 15–25 individuals from each one of 10 Euro- locations over a broad time span (Lister 2001; Vila et al.
pean and 10 Chinese breeds genotyped for 1536 SNPs in 2001; Hill et al. 2002; Kavar & Dovc 2008). Apparently,
three genomic regions. The LD extends up to 2 cM in the know-how required for domestication, rather than the
Europe and up to 0.05 cM in China. The authors suggest domestic animals themselves, spread from one region to the
two possible explanations: either European ancestral stock next, challenging the suggestion that the domestication
has a higher level of LD, or modern breeding programmes process was confined to a restricted area. However, the

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 Genetic diversity in farm animals 17

horse domestication scenario has recently been complicated dence for a Mongolian origin of Japanese breeds. Evidence
by the analysis of matrilines from Lusitano and Soraia for a relationship of Mongolian and Norwegian breeds on
populations, which suggests a role of the Iberian Peninsula the basis of 26 microsatellites was only incomplete
as a glacial refugium and a possible second centre of horse (Bjornstad et al. 2003), but is consistent with the morpho-
domestication (Lopes et al. 2005). Interestingly, analysis of logical appearance of the Nordic breeds.
fossil remains showed that domestication of horses from
5000 YBP onward was followed by the spread of mutations
Chickens
resulting in a large variety of coat colours (Ludwig et al.
2009). Among poultry species, chickens are the most important
AMOVA analysis of 72 populations from Europe, South- and provide an important source of human food. The red
western Asia, Eastern Asia and Africa revealed a non-ran- jungle fowl (Gallus gallus) is believed to be the progenitor of
dom distribution of diversity among populations and a clear, the domesticated chicken and has its widest distribution in
although weak, geographical partitioning of mtDNA varia- East Asia, from Pakistan through China, Eastern India,
tion (McGahern et al. 2006). In a few instances, mtDNA has Burma, most of Indo-China, and on the islands of Sumatra,
provided evidence for the origins of specific horse breeds. Java and Bali (Crawford 1990). As in other livestock species,
Luis et al. (2006) found Iberian haplotypes in New World sequence variation in mtDNA, in particular in the highly
breeds with a high frequency, which is in line with historic polymorphic control region, has been used to study
evidence for the origin of American horses, while Yang et al. domestication events and relationships in the chicken. First
(2002) identified Mongolian haplotypes in the Korean Cheju results with representatives of each of the four wild Gallus
breed. The association of haplogroup F with Eastern-Asia species, domestic chickens from Indonesia and two com-
was proposed as an argument for a Chinese domestication of mercial breeds, has suggested that domestic chickens des-
the haplogroup (Lei et al. 2009). cend from only one species, Gallus gallus, and that a single
Analysis of Y-chromosomal data supported a strong sex- domestication event took place in Thailand and its adjacent
bias in the domestication process. Lindgren et al. (2004) regions (Fumihito et al. 1996). Subsequent studies of sam-
screened 14.3 kb of non-coding Y chromosome sequence in ples from various regions in Europe and Asia suggested
52 male horses of 15 different breeds and did not identify a multiple origins of domestic chickens in South and South-
single segregating site. Even though their observations east Asia, which is consistent with archaeological data
cannot exclude the possibility that Y-chromosomal varia- (West & Zhou 1988; Liu et al. 2006; Oka et al. 2007).
tion was low before domestication took place, their results Moreover, whole mtDNA sequences and two nuclear
strongly suggest that only a few stallions have contributed markers revealed that, besides Gallus gallus, Gallus sonneratii
genetically to the domestic horse. and Gallus lafayettii might have also contributed to the ge-
Several studies have compared horse breeds or assessed netic make-up of contemporary domesticated chickens, al-
the genetic structure of single breeds on the basis of though to a lesser extent (Nishibori et al. 2005). Recently
microsatellites. Most of these targeted local breeds and used Eriksson et al. (2008) provided further evidence of a hybrid
their own marker panel, meaning that data from different origin of the domestic chickens. They studied sequence
studies cannot be compared directly. Thus, for many breeds, variation of the BCDO2 gene in domestic chickens and
data on genetic diversity are available, but insights into closely related wild species. BCDO2 encodes beta-carotene
breed relationships are still fragmentary. dioxygenase 2, which cleaves colourful carotenoids to col-
The so far unrealized potential of a standardized micro- ourless apocarotenoids and is an obvious candidate gene for
satellite panel for the elucidation of breed relationships is skin colour. Sequence comparison revealed that yellow skin,
illustrated by three well-supported clusters of two riding a common feature of many breeds of domestic chicken, does
breeds (Arabian, Hanoverian), two ÔprimitiveÕ breeds (Ex- not originate from the red jungle fowl (Gallus gallus), but is
moor and Sorraia) and six German cold-blooded breeds most likely from the grey jungle fowl (Gallus sonneratii), a
(Aberle et al. 2004). Similarly, Bigi et al. (2007) found, wild relative of domestic fowl found in India. A study of
using only 12 markers, significant clustering of the Thor- African domestic chickens revealed the presence of two
oughbred and Anglo-Arabian breeds and of Haflinger, Ital- maternal lineages among Zimbabwean, Sudanese and
ian heavy draught and Bodaglino. Based on 17 protein and Malawian chickens, one of Southeast Asian and the other of
12 microsatellite markers, Luis et al. (2007) reported eight presumably Indian origin (Muchadeyi et al. 2008). mtDNA
breed groups among 33 breeds, of which four groups were analyses also showed that modern Chilean breeds, pre-
well supported (Andalusian with Lusitano; Friesian with sumed to be of Polynesian origin (pre-Columbian), are
two pony breeds; Morgan, Standardbred, Rocky Mountain actually of Indo-European and Asian origin. Ancient
and American Saddlebred; Irish Draught, Quarter Horse, mtDNA haplotypes found in pre-Columbian archaeological
Hanoverian, Holsteiner and Thoroughbred). Microsatellites chicken remains on Easter Island support the theory of early
have also been used to assess possible origins of specific Polynesian/Pacific chicken transport. Either these haplo-
horse breeds. For instance, Kakoi et al. (2007) found evi- types never reached South America, or they were

 2010 The Authors, Journal compilation  2010 International Society for Animal Genetics, Animal Genetics, 41 (Suppl. 1), 6–31
18 Groeneveld et al.

subsequently displaced by new introductions (Gongora et al. 2001). Furthermore, small-scale studies analysing only a
2008). few local Italian or Japanese fancy breeds showed that these
Since domestication, chickens have been distributed breeds can be genetically identified and that they generally
throughout various countries, continents and cultures. As a display low genetic diversity (Tadano et al. 2007, 2008;
result of many years of adaptation and breeding, a wide Zanetti et al. 2007).
range of chicken breeds exist today. These encompass more For 28 of the 30 FAO-recommended microsatellite mark-
or less unselected indigenous chickens and ecotypes from ers, data for around 100 breeds are currently published.
various regions in the world, standardized fancy breeds Additional studies, including of West African, South African
selected for morphological traits and maintained for leisure and Vietnamese breeds, are underway (M. Tixier-Boichard
activities, and experimental and commercial lines. An and H. Jianlin, personal communication; S. Weigend,
increasing number of local chicken breeds are under threat unpublished data). Although merging microsatellite datasets
of extinction, and valuable genotypes and traits may be at generated in different laboratories is often problematic,
risk of being lost (Blackburn 2006). Berthouly et al. (2008) succeeded, after calibrating 14 of 22
Insight into the extent of diversity of chicken breeds markers, in combining genotypes from different laboratories.
worldwide has been gained using microsatellites in numer- SNPs now have also become a well-established genetic
ous studies (Wimmers et al. 2000; Berthouly et al. 2008; marker system. In the AVIANDIV project, one SNP per
Chen et al. 2008), including the European research project 50 bp was found on average in a subset of ten highly di-
AVIANDIV and follow-up studies (Rosenberg et al. 2001; verse chicken populations (10 individuals per population,
Hillel et al. 2003; Granevitze et al. 2007, 2009). Overall, Schmid et al. 2005). This frequency is higher than that
results suggest that Jungle Fowl populations and traditional found by comparing different domestic breeds (Wong et al.
unselected breeds are widely heterogeneous populations, 2004). The high frequency found in the AVIANDIV project
which include a large portion of the total genetic diversity. presumably reflects the wide genetic spectrum of chicken
Within commercial chickens, broiler lines were slightly more breeds collected. SNP arrays with over 2500 informative
polymorphic than layers. Among the layers, the white layers SNPs in commercial chicken lines and other resource pop-
were less polymorphic than the brown layers. In recent years, ulations indicated that individual commercial breeding lines
there has been concern about reduced genetic variability in have lost 50% or more of their genetic diversity. Only a
commercial white egg layers that have originated from a limited fraction of this loss can be recovered by combining
sole breed, the Single Comb White Leghorn. Although find- all stocks of commercial poultry (Muir et al. 2008). How-
ings of the AVIANDIV project support this concern to some ever, it appears that modern breeding was not the primary
extent, commercial lines still exhibit a considerable amount source of this loss of alleles, and that many alleles were lost
of variation at microsatellite loci. prior to the formation of the current industry.
Hillel et al. (2007) undertook a large-scale analysis of Andreescu et al. (2007) assessed the extent of LD in nine
2000 individuals from 65 populations representing different commercial broiler breeding populations using genotype
chicken types from various geographical regions. Individu- data for 959 and 398 SNPs on chromosomes 1 and 4
als were genotyped at 29 microsatellite loci. Model-based respectively. Results showed that in these lines LD did not
clustering (as implemented in Structure (Pritchard et al. extend much beyond approximately 0.5 cM, which is
2000)) indicated that the 65 populations split into groups shorter than previously reported for other livestock species.
corresponding to their geographical origin and cultivation However, it seems to be much larger in White Leghorn-
history, i.e. Asia, Europe and Africa (Hillel et al. 2007). based breeds. Within 1 cM, LD tended to be consistent
Using the same dataset, Granevitze et al. (2007) showed across related populations. Calculating the correlation of LD
that the degree of polymorphism varies between clusters. between neighbouring SNPs within and between popula-
The relatively low genetic diversity observed in the native tions closely matched the line relationships based on marker
European breeds, mainly standardized fancy breeds, was allele frequencies. Thus, there are indications that this
presumably resulting from positive assortative mating and approach is equivalent to estimating kinship coefficients,
small effective flock size. By contrast, native populations and it might also be of interest for other livestock species. As
from Africa and Asia had high genetic diversity and did not in other farm animal species, initiatives are underway to
show a typical population structure. Differentiation was develop genomic 60 K SNP arrays for chickens.
only observed between populations from distant areas and
countries (Muchadeyi et al. 2007; Mwacharo et al. 2007;
Molecular databases
Berthouly 2008; Chen et al. 2008). Rosenberg et al. (2001)
demonstrated that it was possible to assign individuals to Sequence data generated by individual laboratories or large-
their correct breeds with 90% efficiency based on only 12 scale sequencing projects are usually deposited in one of
microsatellite markers genotyped in 30 animals from 20 three major databases: GenBank (NCBI, National Center for
diverse chicken populations. By increasing the number of Biotechnology Information), EMBL-Bank (European Molec-
loci used to 24, accuracy was close to 97% (Rosenberg et al. ular Biology Laboratory-Bank) or DDBJ (DNA Databank of

 2010 The Authors, Journal compilation  2010 International Society for Animal Genetics, Animal Genetics, 41 (Suppl. 1), 6–31
 Genetic diversity in farm animals 19

Japan). These publicly accessible databases are synchro- crosatellites to extensive link lists. Even if several are no
nized on a daily basis, so that the data become available at longer updated, these databases remain valuable resources
all three sites (Benson et al. 2008; Cochrane et al. 2008; for the development of markers as well as for fundamental
Sugawara et al. 2008). A great amount of data from live- research on livestock animals.
stock species is included in these databases. However, most
of the records represent data on the respective genomes of
Discussion
the species and not single individuals, which would be
required for assessment of genetic diversity. Despite this, Genetic variation in traits of interest is the basis for future
the framework of the NCBI databases does allow for the breeding programmes. Variation is displayed by genetic
submission of individual, even redundant, sequences, differences between individuals, families and populations
including microsatellites and SNPs (both stored in dbSNP; within a given species. Pronounced erosion of these genetic
http://www.ncbi.nlm.nih.gov/projects/SNP/) (Wheeler et al. resources across all farm animal species within the last
2005). In general, the number of records for each species, century has been ascertained. In the last two decades, the
which are bound to change their order of magnitude soon, erosion of genetic resources is being counteracted by efforts
reflect the agricultural importance of the species and/or the directed at their conservation. This has resulted in consid-
current state of progress of the genome projects. Further- erable progress on two fronts. First, there is a growing
more, NCBI hosts organism-specific genome resource pages, amount of systematically collected information on livestock
which include links to resources found within and outside breeds and their environment. Second, in most species of
NCBI (e.g. http://www.ncbi.nlm.nih.gov/projects/genome/ livestock many breeds have been the subjects of molecular
guide/chicken/). analyses. This has resulted in a great number of publica-
A multitude of other smaller publicly accessible databas- tions ranging from descriptions of local populations to more
es, often with more specific purposes, are available besides systematic assessments of global diversity patterns. The
the previously mentioned databases. For individual livestock results of both phenotypic and molecular approaches are, or
records, three databases were identified: AVIANDIV for should be, accessible in databases with the ultimate objec-
chickens, CaDBase for cattle and PigDBase for pigs. tive of providing an integrative platform for scientific anal-
The AVIANDIV database (http://aviandiv.tzv.fal.de/) in- ysis and decision-making. However, the current state of the
cludes: (i) genotypes for 20 microsatellite loci from DNA databases leaves much to be desired. Furthermore, docu-
pools of 52 European breeds and commercial lines (Hillel mentation of phenotypic data and molecular genotyping,
et al. 2003); (ii) individual data from 600 individuals rep- both having their own merits, still have to converge on
resenting 20 breeds for 27 microsatellites (Rosenberg et al. consistent and plausible valuations of specific breeds for
2001); and (iii) SNPs from 13 random non-coding DNA conservation.
fragments typed in 100 individuals belonging to 10 breeds/ Our understanding of breed diversity has been deepened
populations. The last update of the database was in 1999 significantly by technological progress in molecular genet-
(AVIANDIV 1999). ics. Blood groups, enzyme polymorphisms, transplantation
PigDBase (http://www.projects.roslin.ac.uk/pigbiodiv/in- antigens and RFLPs have been succeeded by mtDNA and
dex.html) contains the data from the EU PigBioDiv project. Y-chromosomal haplotypes and autosomal microsatellites.
The data consist of 118 188 microsatellite and 349 348 For all domestic species, mtDNA data have allowed the
AFLP genotypes from 60 distinct populations and 50 mi- elucidation of the relationships with wild ancestor species,
crosatellite and 148 AFLP markers. Unfortunately, the and for most species it is also informative at the intercon-
database is password-protected (Russell et al. 2003). tinental level. In combination with archaeological data, it
CaDBase (http://www.projects.roslin.ac.uk/cdiv/ – access has been shown that the most important areas for domes-
to some areas of this system requires username/password tication events of the main livestock species and chickens
authorisation) contains data on 134 breeds and 30 are found in Asia and Europe, with the South American
microsatellite markers that are recommended by the FAO camelids representing an exception. There is evidence of
(http://lprdad.fao.org/cgi-bin/getblob.cgi?sid=-1,50006220) multiple domestication events for most species, often
(Williams 2002). However, as it does not contain data from involving more than one ancestor species or subspecies and
the most recent large projects (Li et al. 2007; Martin-Burriel repeated introgression events of closely related ancestor
et al. 2007; Lenstra 2008), data for all 30 markers are listed species. Sheep, goats, and taurine cattle (Bos taurus) are
for only few breeds. Furthermore, allele sizes within presumed to have been domesticated in Southwestern Asia.
CaDBase are not consistent across breeds. The Indus valley has been proposed to be the site of
Besides the three major sequence databases and those domestication of indicine cattle and the river type of water
containing individual livestock records, numerous data- buffalo, while the swamp type of water buffalo is thought to
bases on livestock genomics are available (Table 1). The have originated in the Yangtze valley. The domestication of
contents range from genome maps including annotations, pigs is considered to have happened across Eurasia and
SNPs, QTL data, whole genome shotgun libraries and mi- Eastern Asia in at least seven separate events involving both

 2010 The Authors, Journal compilation  2010 International Society for Animal Genetics, Animal Genetics, 41 (Suppl. 1), 6–31
 20
Table 1 Non-exhaustive list of publicly accessible livestock genome resources. Database or project name and the respective URL are given. For pigs, cattle, goats, sheep, chicken and any additional species
(other sp.), databases are scored according to presence (y) or absence (n) of data for the respective species. Non-available data are denoted by n/a.

Other
Database/project name URL Pigs Cattle Goats Sheep Chicken sp. Type of data included Last updated References
Groeneveld et al.

AVIANDIV http://aviandiv.tzv.fal.de/ n n n n y n Microsatellite genotypes, 6 September 1999 AVIANDIV (1999)

SNPs
CaDBase http://www.projects.roslin.ac.uk/cdiv/ n y n n n n Microsatellite genotypes n/a Williams (2002)
PigDBase http://www.projects.roslin.ac.uk/ y n n n n n Microsatellite and n/a Russell et al. (2003)
pigbiodiv/index.html AFLPgenotypes
PEDE: Pig Expression http://pede.dna.affrc.go.jp/ y n n n n n Full-length cDNA clones 21 October 2006 Uenishi et al. (2007)
Data Explorer and ESTs
AnimalQTLdb http://www.animalgenome.org/QTLdb/ y y n y y n Quantitative Trait Loci data Last release: 10 Hu et al. (2007)
30 December 2009
ARKdb http://www.thearkdb.org/arkdb/index.jsp y y n y y y Genome mapping data  2007–2009 Hu et al. (2001)
ChickVD: Chicken http://chicken.genomics.org.cn/index.jsp n n n n y n Sequence variation map, 16 December 2006 Wang et al. (2005)
Variation Database primarily SNPs
Bovine Genome Project http://www.hgsc.bcm.tmc.edu/ n y n n n y BAC and Whole  1998–2010 n/a
projects/bovine/ Genome Shotgun (WGS)
libraries
Cattle Genome Database http://www.cgd.csiro.au/ n y n n n n Comparative mapping, QTL 10 December 2002 n/a
LivestockGenomics http://www.livestockgenomics.csiro.au/ n y n y n n Genome Browsers (maps)  2001–2010 n/a
and SNPs
Pig Genomic Informatics http://pig.genomics.org.cn/ y n n n n n Gene annotations,  2006 Ruan et al. (2007)
System maps, SNPs
Bovine Genome Database http://genomes.arc.georgetown.edu/ n y n n n n Genome analysis and n/a n/a
drupal/bovine/ annotation, QTL
US Poultry Genome Project http://poultry.mph.msu.edu/ n n n n y y SNPs, BACs linked to genes, 4 November 2008 n/a
primers
COMRAD – comparative http://www.projects.roslin.ac.uk/ n y n n n n Whole genome radiation  2002 n/a
radiation hybrid mapping comrad/introduction.html hybrid map
Gallus Genome Gbrowse http://birdbase.net/cgi-bin/ n n n n y y Wide array of chicken 27 January 2007 Schmidt et al. (2008)
gbrowse/gallus08/ genome data
Geisha – gallus expression http://geisha.arizona.edu/geisha/ n n n n y n In situ hybridization  2008 Darnell et al. (2007)
in situ hybridization information
analysis
AgBase http://www.agbase.msstate.edu/ y y n y y y Genome, functional 13 January 2010 McCarthy et al.
annotations (2006, 2007)
BBSRC ChickEST Database http://www.chick.manchester.ac.uk/ n n n n y n ESTs Last addition Hubbard et al. (2005)
September 2004
Chicken full-length http://bioinfo.hku.hk/chicken/ n n n n y n cDNA Has been updated Wang et al. (2007)
cDNA Database in 2007

 2010 The Authors, Journal compilation  2010 International Society for Animal Genetics, Animal Genetics, 41 (Suppl. 1), 6–31
 Table 1 (Continued)

Other
Database/project name URL Pigs Cattle Goats Sheep Chicken sp. Type of data included Last updated References

e!Ensembl http://www.ensembl.org/index.html# n y n n y y Comprehensive genome Ensembl Release Flicek et al. (2008)

information system, 57 – March 2010
genome annotation
s! Public Sigenae Contig http://public-contigbrowser.sigenae.org: y y n y y y ESTs, based on Ensembl,  2010 n/a
browser 9090/index.html Release 40, August 2006
Sheep Genomics server http://www.sg.angis.org.au/ y n n y n n Gene maps n/a n/a
at the University of Sydney
EuMicroSatdb (Eukaryotic http://veenuash.info/web/ n y n n y y Microsatellites Last visible Aishwarya et al.
Microsatellite database) database.htm acitvity 2007 (2007)
UgMicroSatdb (Unigene http://www.veenuash.info/veenu/ y y n y y y Microsatellites from various n/a Aishwarya & Sharma
MicroSatellite database) index.asp# eukaryotic genomes, (2008)
unigenes
OXGRID – The Oxford Grid http://oxgrid.angis.org.au/ y y y y y y Gene maps (oxford grids)  2005 n/a
Project
International Sheep http://www.sheephapmap.org/ n n n y n n BAC library, SNPs  2002–2010 e.g. Oddy et al. (2007)
Genomics Consortium
A database of Avian http://birdbase.net/# n n n n y y Links  2010 n/a
genes and genomes
AvianNET – The avian http://www.chicken-genome.org/ n n n n y n Links  2003, 2004 n/a
information network
US Livestock Species http://www.animalgenome.org/ y y n y y y Genome resources, 21 March 2010 n/a
Genome Projects mostly links
BOVMAP http://locus.jouy.inra.fr/cgi-bin/ n y n n n n Genome resources, incl. n/a Gas et al. (1996)
bovmap/intro2.pl microsatellites, SNPs,
maps
Origin and diversity of http://www.rala.is/beta/ n n n y n n Microsatellite primers, n/a n/a
North European Default.htm allele lengths per marker
sheep breeds

 2010 The Authors, Journal compilation  2010 International Society for Animal Genetics, Animal Genetics, 41 (Suppl. 1), 6–31
Genetic diversity in farm animals
21
22 Groeneveld et al.

European and Asian subspecies of boar. The Yak is pre- The greatest value of breed description databases is that
sumed to be the result of a single domestication event in they present the large variation that exists among livestock
China/Tibet with at least three maternal lineages contrib- breeds from around the world. Hence, a rough idea of the
uting to the ancestral yak gene pool. Domestic chickens are number of breeds is available, often with estimates on
thought to be the result of multiple domestication events, population sizes. Nonetheless, for a large number of breeds
predominantly of Red jungle fowl (Gallus gallus) in South- contained in the most comprehensive and detailed database,
eastern Asia and possibly also involving Gallus sonneratii the FAO Global Databank for Animal Genetic Resources,
and maybe Gallus lafayettii. Horses were domesticated in a very little information other than the name and country of
broad area across the Eurasian steppe, and in this species origin is available. Here, it should be noted that the breed
the husbandry style has left considerable signatures. It is concept is less useful in characterizing livestock variability
presumed that mares were domesticated numerous times, in developing countries than it is in developed countries.
but that only a few stallions contributed to the genetic Performance figures, if available at all, rarely have a refer-
make-up of the domestic horse. The last finding illustrates ence point, e.g. the production system. Census data on
the use of Y-chromosomal haplotypes as a marker for population sizes are very often lacking and where available
mammalian patrilines. This is still limited by the identifi- tend not to be up to date and may be inaccurate. This,
cation of haplotypes, but probably has the same potential as together with a delay in reporting, does not allow for real-
in human population genetics. time monitoring of the status of species endangerment.
A consistent finding with all molecular markers is that Currently, the breed is the unit of conservation. However,
genetic variability declines with increasing distance from breeds are also social entities with a role in the national or
the domestication centres. This has been shown for pigs, regional identity, which leaves room for subjective percep-
sheep, goats, cattle and chickens. Within breeds, autosomal tions of their uniqueness. Breed uniqueness is also not
microsatellite markers allow parameters such as expected immediately obvious from molecular data. These show
heterozygosity and allelic richness to be calculated and may invariably that most of the variation is shared by the breeds,
reveal effects of genetic isolation, inbreeding, population most of which harbour a considerable part of the total
bottlenecks, introgression and subdivision. Relationships diversity of the species. In other words, most of the genetic
between breeds can often be represented schematically via diversity is present within a breed and not between breeds.
trees, networks, coordination plots or clustering diagrams. This is analogous to what was found by Rosenberg et al.
Most rewarding are then inferences regarding the history of (2002) for humans. Furthermore, the variation displayed by
livestock, such as evidence for more recent events like current microsatellite panels of 10–30 markers only partially
migrations, introgressions, expansions and/or selection. reflects the diversity of the animal genomes, and it remains
The content of the molecular project-specific databases unknown how the variation of these selectively neutral and
described in this article is rather outdated. Updating of both quickly evolving markers relates to other parts of the gen-
main and project-specific databases is often neglected. A ome. However, as illustrated by several examples cited above,
second problem caused by the coexistence of numerous pro- this does allow a reconstruction of the history of breeds.
ject-specific databases is that searches across different pro- In the near future, new technologies such as high
jects are not possible, as each database has its own throughput SNP typing or even whole-genome sequencing
architecture and thus different report formats and export are likely to revolutionize our insight into the diversity and
functions. Thus, it is very tedious to combine data retrieved uniqueness of breeds, with the ultimate objective of gaining
from different databases. This problem could be overcome a fuller understanding of the molecular basis of functional
either by storing all data within one database or by setting up diversity.
a database search engine that can execute searches across a
number of individual databases. This is only feasible if the
Acknowledgements
project-specific databases fulfil certain structural require-
ments that the scientific community would have to decide on The authors thank L. Ollivier, M. SanCristobal, L. Silió and
and adhere to when setting up such databases. This setup, M. Pérez-Enciso for their comments. The Authors state that
which returns search results from a number of individual there is no conflict of interest regarding the material dis-
databases, has been implemented successfully on a national cussed in the manuscript. Action GLOBALDIV AGRI GEN
level for plant genetic resources (Harrer et al. 2002). RES 067 receives financial support from the European
Molecular datasets have the additional problem that Commission, Directorate-General for Agriculture and Rural
only a minority of the research institutes use the FAO- Development, under Council Regulation (EC) No 870/2004.
standardized microsatellite markers (see http://www.
globaldiv.eu/docs/Microsatellite%20markers.pdf for sur-
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