ORIGINAL ARTICLE
Microsatellite diversity of the Nordic type of goats in relation to
breed conservation: how relevant is pure ancestry?
J.A. Lenstra1, J. Tigchelaar2, I. Biebach3, Econogene Consortiuma, J.H. Hallsson4, J. Kantanen5,6,
V.H. Nielsen7, F. Pompanon8, S. Naderi9, H.-R. Rezaei10, N. Sæther11, O. Ertugrul12, C. Grossen3,
G. Camenisch3, M. Vos-Loohuis1, M. van Straten2, E.A. de Poel2, J. Windig13 & K. Oldenbroek2,13
1 Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands
2 Stichting Zeldzame Huisdierrassen, Wageningen, The Netherlands
3 Institute of Evolutionary Biology and Environmental Studies, University of Z€urich, Z€urich, Switzerland
4 Faculty of Land and Animal Resources, Agricultural University of Iceland, Reykjavik, Iceland
5 Green Technology, Natural Resources Institute Finland, Jokioinen, Finland
6 Department of Environmental and Biological Sciences, University of Eastern Finland, Kuopio, Finland
7 Research Centre Foulum, Aarhus University, Tjele, Denmark
8 Universite Grenoble Alpes, Grenoble, France
9 Environmental Sciences Department, Natural Resources Faculty, University of Guilan, Guilan, Iran
10 Environmental Sciences Department, Gorgan University of Agriculture and Natural Resources, Gorgan, Iran
11 Norwegian Genetic Resource Centre,As, Norway
12 Veterinary Faculty, Ankara University, Ankara, Turkey
13 Animal Sciences Group and Centre for Genetic Resources-Wageningen UR, Lelystad, The Netherlands
Keywords
Conservation; diversity; goats; microsatellite.
Correspondence
J.A. Lenstra, Faculty of Veterinary Medicine,
Utrecht University, Yalelaan 104, 3584CM
Utrecht, The Netherlands.
Tel: +31 30 2534992;
Fax: +31 30 2535077;
E-mail: J.A.Lenstra@uu.nl
Received: 17 March 2016;
accepted: 24 May 2016
aThe members of “Econogene Consortium”
are listed in Appendix.
This is an open access article under the terms
of the Creative Commons Attribution-
NonCommercial-NoDerivs License, which
permits use and distribution in any medium,
provided the original work is properly cited,
the use is non-commercial and no
modifications or adaptations are made.
Summary
In the last decades, several endangered breeds of livestock species have
been re-established effectively. However, the successful revival of the
Dutch and Danish Landrace goats involved crossing with exotic breeds
and the ancestry of the current populations is therefore not clear. We
have generated genotypes for 27 FAO-recommended microsatellites of
these landraces and three phenotypically similar Nordic-type landraces
and compared these breeds with central European, Mediterranean and
south-west Asian goats. We found decreasing levels of genetic diversity
with increasing distance from the south-west Asian domestication site
with a south-east-to-north-west cline that is clearly steeper than the
Mediterranean east-to-west cline. In terms of genetic diversity, the Dutch
Landrace comes next to the isolated Icelandic breed, which has an extre-
mely low diversity. The Norwegian coastal goat and the Finnish and Ice-
landic landraces are clearly related. It appears that by a combination of
mixed origin and a population bottleneck, the Dutch and Danish Land-
races are separated from the other breeds. However, the current Dutch
and Danish populations with the multicoloured and long-horned appear-
ance effectively substitute for the original breed, illustrating that for con-
servation of cultural heritage, the phenotype of a breed is more relevant
than pure ancestry and the genetic diversity of the original breed. More in
general, we propose that for conservation, the retention of genetic diver-
sity of an original breed and of the visual phenotype by which the breed is
recognized and defined needs to be considered separately.
© 2016 The Authors.
Journal of Animal Breeding and Genetics Published by Blackwell Verlag GmbH • J. Anim. Breed. Genet. 134 (2017) 78–84
doi:10.1111/jbg.12226
J. Anim. Breed. Genet. ISSN 0931-2668
Introduction
In comparison with other farm animals in the devel-
oped world, goats are not of major economic impor-
tance, but nonetheless contribute considerably to the
diversity of livestock production. The Saanen and
Boer breeds are the major producers of goat milk and
meat, respectively, and the Angora and Kashmere
goats provide special types of wool (Mason 1984).
Many local goat breeds are suitable for marginal, often
mountainous areas, in developing countries for small
holders and in developed countries for hobby breed-
ing (Porter 1996; Dohner 2001). As horses and cats,
goats easily survive if escaped from the domestic habi-
tat and have established more feral populations than
any other livestock species (Mason 1984).
The Nordic type of goats is a primitive longhaired
and multicoloured type, which are kept as landraces
in Finland, Sweden, Norway, Denmark, Iceland, Bri-
tain, Ireland and the Netherlands (http://www.ansi.
okstate.edu/breeds/goats/index.html/goats). The Ice-
landic goats are believed to descend from Scandina-
vian animals imported more than 1000 years ago
(Baldursdottir et al. 2012). In Britain, authentic goats
mainly survived as feral populations (Mason 1984;
Porter 1996). The original Danish Landrace has in the
19th century been crossed with German Harz
and Swiss Saanen goat (http://naturerhverv.dk/land
brug/genetiske-ressourcer/husdyrgenetiske-ressourcer/
husdyrarter/faar-og-geder/#c9129).
In the beginning of the 20th century, Dutch Land-
race goats were influenced by Saanen and Toggen-
burg goats. Following a serious decline after the
World War II, the Dutch Landrace population was
revived and remained popular as backyard goat for
smallholders. However, after the mid-20th century,
the Dutch Landrace goats nearly disappeared by the
rationalization of animal husbandry, and in 1958,
only a few animals were left (Frankenhuis & Hazen-
broek 1984). A second revival started in the Blijdorp
Zoo in Rotterdam, possibly with only two animals,
and was continued with four males and four females
in the village of Leersum. These animals along with
six additional unregistered animals of unknown origin
became the ancestors of the current population of
approximately 2000 animals, which are kept by
hobby breeders and are used in nature management
systems.
Molecular markers now allow studying breed rela-
tionships and geographic patterns of diversity as indi-
cators of migrations, admixture and genetic
bottlenecks (Groeneveld et al. 2010). A study of
south-west Asian, Mediterranean and central
European goats using the FAO-recommended
microsatellites (Canon et al. 2006) revealed a clear
clustering of breeds from the same region and a
decrease in the genetic diversity with increasing dis-
tance from the domestication site in south-west Asia
to Central Europe. However, northern European
goats have so far not been investigated on the DNA
level.
In an attempt to characterize further the phylo-
geography of European goats and to trace the ancestry
of the Dutch and Danish Landraces, we have com-
pared microsatellite genotypes of these breeds with
those of other Nordic and European goat breeds
(Canon et al. 2006; Glowatzki-Mullis et al. 2008). We
propose that the complex history of the Danish and
Dutch Landraces, which confounds the regional pat-
tern of breed relationships, does not affect their status
of heritage breeds.
Materials and methods
Samples from 32 Dutch goats from different breeding
lines were collected with a Genotek nasal swab kit.
DNA was extracted by standard procedures from
blood samples of 35 Danish, 32 Finnish, 32 Norwegian
and 16 Icelandic goats from six farms and from tissue
samples of five Iranian Bezoars collected in the wild
(Table S1). Genotyping with the FAO-recommended
microsatellites (FAO, 2011) was performed as
described (Canon et al. 2006), but markers BM6444,
DRBP and SRCRSP7 were excluded from analysis
because of departure from HW equilibrium and
SRCRSP3 because of a low scoring success in our sam-
ples. Harmonization of allele lengths with previous
data (Canon et al. 2006; Glowatzki-Mullis et al. 2008)
was achieved by genotyping two samples from the
Econogene data set (Canon et al. 2006), which
allowed a combination with this data set and an over-
lapping data set panel of Swiss goat breeds as well as
the African Boer goats (Glowatzki-Mullis et al. 2008).
The Dutch Landrace goat was also genotyped for 37
microsatellite markers selected for genotyping ibex
goats (Capra ibex, Biebach & Keller 2009), 11 of which
were shared with the FAO panel (Table S1).
A separate data set of the Turkish Angora, Honamli,
Kil, Kilis and Norduz breeds (Agaoglu & Ertugrul
2012) shared with our data set the Angora breed and
13 of the 26 FAO microsatellites. Sharing the Angora
breed allowed a tentative harmonization of allele sizes
for the 13 common microsatellites (see Supporting
Information).
Data were analysed with the Microsatellite Tool Kit
(http://animalgenomics.ucd.i.e/sdepark/ms-toolkit/),
© 2016 The Authors. Journal of Animal Breeding and Genetics Published by Blackwell Verlag GmbH • J. Anim. Breed. Genet. 134 (2017) 78–84 79
J. A. Lenstra et al. Genetic diversity of Nordic goats
and allelic richness was calculated with the FSTAT pro-
gram using a sample size of 13. Genetic distances were
calculated with the MICROSAT program (Minch 1997).
Reynolds’ genetic distance was visualized via Neigh-
bourNet graphs using SPLITSTREE version 4.0 (Reynolds
et al. 1983; Huson 1998). Distances from the domesti-
cation site (Naderi et al. 2008) in kilometres were
calculated as
acosðsinðlat1:p=180Þsinðlat2:p=180Þ
þ cosðlat1:p=180Þcosðlat2:p=180Þcosðlon2:p=180
 lon1:p=180ÞÞ:ð6378:135Þ;
in which acos is the arccosine, lat1 and lon1 latitude
and longitude, respectively, of the breed in degrees
(www.econogene.eu), and lat2 (37.67°) and lon2
(43.05°) the coordinates of a central point in the esti-
mated domestication area in east Anatolia. The corre-
lation of genetic and geographic distances was
visualized by linear regression. Model-based cluster-
ing was carried out as described previously (Canon
et al. 2006) with 150 000 burnins and 350 000
simulations.
Results
We found a good correlation of the two most common
diversity parameter expected heterozygosity (HE) and
allelic richness (Table S1, r2 0.94). To survey the pat-
terns of genetic diversity, we plotted in Figure 1a HE
against the distance from the domestication site. A
decrease in diversity with increasing distance is most
evident in the northern European breeds. Clines were
observed from east to west and south-east to north-
west, respectively, with a clear difference between the
two (broken lines in Figure 1a). Icelandic goats have
an extremely low diversity (HE 0.279, complete
homozygosity in six of 26 markers). From the other
breeds, the Dutch Nordic goat is the most inbred breed
(HE 0.527, two homozygous markers).
Inbreeding coefficients within breeds (FIS) on the
basis of expected and observed heterozygosities are
for most breeds in the range of 0.04–0.12 (Figure 1b).
Exceptionally, high values are observed for the Ice-
landic goats (Baldursdottir et al. 2012) and for the
French Pyrenean breed. In contrast, low values are
observed for the Swiss Appenzell, Saanen, St. Gallen
Booted and Toggenburg goats.
For model-based clustering (Pritchard et al. 2000)
the northern European breeds were analyzed together
with the German Fawn and Thuringian Wald goats.
We also added the Swiss Saanen and Toggenburg,
which are reported to have influenced the Danish and
Dutch Landraces and the Thuringian Wald goat (Por-
ter 1996). Figure 2 shows a consistent clustering of
the Norwegian and Finnish goats, which at k = 3 and
4 form a separate cluster with the Icelandic breed,
excluding, however, the Dutch and Danish landraces.
The patterns reproduce the documented incrossing of
Toggenburg in the Thuringian Forest, but not the
introgression of Saanen or Toggenburg in the Danish
and Dutch breeds. However, these introgressions may
very well have been masked by later shifts in allele
frequencies as a consequence of the severe population
bottlenecks in both breeds.
0.5
0.6
0.7
0.8
0 1000 2000 3000 4000 5000
south-west Asia
south-west Europe
Central Europe
Northern Europe
east to west  (Mediterranean)
south-east to north-west 
0.05
0.15
0.25
south-east Europe
south-west Asia
south-east Europe
south-west Europe
Central Europe
Northern Europe
Pyrenean Icelandic
Distance from domestication site (km)
H E
F I
S
–0.05
(a)
(b)
Figure 1 (a) Expected heterozygosity (HE)
plotted against the distance from the domesti-
cation site. The trend lines were generated by
least-square analysis and show the observed
clines in heterozygosity from east to west and
south-east to north-west. The low heterozy-
gosity of the Icelandic goat (0.28) is outside
the range of the plot. (b) Inbreeding coefficient
(FIS), calculated as (HEHO)/HE.
© 2016 The Authors. Journal of Animal Breeding and Genetics Published by Blackwell Verlag GmbH • J. Anim. Breed. Genet. 134 (2017) 78–8480
Genetic diversity of Nordic goats J. A. Lenstra et al.
Visualization of the genetic distances (Figure S1,
Table S2) reproduces the clustering of south-west
Asian, Italian with south-east European, Iberian and
central European breeds (Canon et al. 2006) as well as
the clustering of Finnish, Norwegian and Icelandic
Nordic goats. Although the low quality of the bezoar
DNA samples may have led to allele dropout and have
shifted the estimated allele frequencies, its position in
the tree confirms the relatedness of the Turkish breeds
to the first domesticates. The separate position of Afri-
can Boer goats is partly due to low heterozygosity (HE
0.602), but also illustrates the strong geographic dif-
ferentiation of goats (Canon et al. 2006; Groeneveld
et al. 2010).
The Finnish, Norwegian and Icelandic Nordic
breeds again form a separate cluster with as closest
relative the northernmost continental breed repre-
sented in our data set, the Fawn German (BDE, Bunte
Deutsche Edelziege). Remarkably, the extremely low
diversity of the Icelandic goats did not obscure their
Scandinavian origin (Figure S1). On the other hand,
sharing of short branches suggests a spurious affinity
of the Danish Landrace with the Nordic cluster and of
the Dutch Landrace with the Swiss Saanen, respec-
tively (Figure S1).
As the complex phylogenetic networks as shown in
Figure S1 may obscure other phylogenetic relation-
ships and the relationships between the breed clusters
(Lenstra et al., 2012), we reduced the complexity of
the data set. Figure 3a shows a network of the regio-
nal clusters (Table S3) together with breeds that are
intermediate between the clusters (Hungarian Native,
French Pyrenean, French Rove, Fawn German) or
occupy extreme positions (Bezoar, African Boer). This
network clearly visualizes the genetic trends from
south-west Asia to northern and south-west Europe.
Replacing the Nordic cluster by the four separates
Nordic breeds (Figure 3b) again clusters the Finnish,
Norwegian and Iceland goats. However, in this
network, the Dutch and Danish breeds are clearly sep-
arate from the more northern Nordic breeds and are
linked to the network close to the central European
cluster.
This is confirmed by a network of the north Euro-
pean breeds and Swiss Saanen with the central Euro-
pean cluster indicating the root of the network
(Figure 3c). This network also suggests a shared genetic
history of Saanen and the Dutch Landrace goat, which
is in agreement with Figure S1 and is not observed if
Saanen is replaced by any other central European
breed. A clustering of the Dutch and Danish landraces
is more spurious, but is also observed in Figure 3b.
In general, European breeds have distinct pheno-
types and are, as evidenced by the long genetic
distances, genetically clearly differentiated, yet are
genetically clustered according to their region of ori-
gin (Canon et al. 2006; this study). Similar observa-
tions have been reported for Asian goats (Nomura
et al. 2012). In contrast, the four Turkish breeds repre-
sented in our data set combine phenotypic variation
with short genetic distances. We have explored this
further by a tentative meta-analysis of our 26-micro-
satellite data set with an independent data set of five
Turkish breeds (Agaoglu & Ertugrul 2012), which
shares the Ankara (=Angora) breed and 13 microsatel-
lites with our data set. In the resulting network
(Figure S2), the duplicate samplings of the Angora are
closely linked, which supports the validity of the
meta-analysis (Lenstra et al., 2012). The network fur-
ther indicates that all eight Turkish breeds with
diverse breeding purposes and appearances form a
tight geographic cluster and confirm the findings of
Bulut et al. (2016).
Inspection of allele frequencies of the Dutch goats
reveals in addition to the two homozygous markers
high-frequency alleles in nine marker that have low
allele frequencies in other breeds. As the last authen-
tic Dutch Landrace goats were kept in a zoo that also
possessed cross-fertile ibex animals, ibex introgression
may have occurred. However, comparison of allele
frequencies of Dutch goats and four ibex populations
for 37 markers (Table S4) did not show any sharing of
major alleles and for all 10 markers clear differences
in allele distributions, arguing against ibex introgres-
sion as explanation for the deviating allele frequencies
in Dutch Landrace goats.
2
3
4
5
7
9
k:
Figure 2 Model-based clustering with indicated number of clusters (k).
For each k value, the program was run four times and only patterns are
shown that were inferred at least three times. Only at k = 2, all four
runs generated the same pattern. The clustering of the Norwegian and
Finnish breeds and of the Thuringian Forest and Toggenburg was also
observed if the north European breeds were analysed together with
central European, Mediterranean and south-west Asian breeds shown in
Figure S1. According to the Evanno criterion (Evanno et al. 2005), k = 5
is the most likely number of clusters.
© 2016 The Authors. Journal of Animal Breeding and Genetics Published by Blackwell Verlag GmbH • J. Anim. Breed. Genet. 134 (2017) 78–84 81
J. A. Lenstra et al. Genetic diversity of Nordic goats
Discussion
Our analysis of northern European breeds illustrates
the strong geographic differentiation of the Eurasian
goat populations. This is supported by a study of east
Asian goats (Nomura et al., 2012) and our meta-ana-
lysis of Turkish breeds, but is less evident in mito-
chondrial DNA data sets (Luikart et al. 2001; Naderi
et al. 2008). We observed a decline of genetic diversity
(Figure 1a), which probably indicates the effect of
genetic drift by repeated founder effects during the
gradual Neolithic introduction of livestock animals,
starting in south-east Europe and finally reaching
northern and western Europe (Groeneveld et al.
2010). The cline is stronger for central and northern
European breeds than for Mediterranean breeds. This
has been observed previously in cattle (Cymbron et al.
2005) and possibly reflects that the Danubian migra-
tion route that populated central and northern Eur-
ope (Tresset & Vigne 2011) involved either more
numerous or more severe population bottlenecks
than the Mediterranean route.
The extremely low diversity of Icelandic goats (HE
0.279) is in agreement with (Baldursdottir et al. 2012)
and reflects their isolation from other goat popula-
tions since ca. 1100 years. The Dutch Landrace goat is
the second most inbred population with a HE of 0.527.
Strikingly, both populations and the Finnish and Dan-
ish Landrace goats combine a low genetic diversity
with a considerable variation in coat colour and col-
our pattern, indicating that a low genetic diversity in
an isolated population does not preclude the mainte-
nance within the population of different visual phe-
notypes. Most northern-central European breeds with
low HE have low FIS values as well, indicating an
absence of significant genetic subdivision within the
breeds with the highly fragmented Icelandic goat pop-
ulation (Baldursdottir et al. 2012) and the Pyrenean
goats as notable exceptions.
Visualization of genetic distances in a NeighborNet-
work extends the geographic clustering of European
goats (Canon et al. 2006) with a separate cluster of
Norwegian, Finnish and Icelandic goats (Figure 3a).
However, the Danish and Dutch landraces do not
Figure 3 NeighborNetwork of Reynolds’ dis-
tances (DR) between breeds or regional clus-
ters of breeds as defined in Table S3. Colours
indicate regional clusters of related breeds
(see Figure 1). Breeds that do not belong to a
cluster or are intermediate between two clus-
ters are indicated in black. (a) Clusters and
intermediate breeds; (b) without the Nordic
cluster but with the Nordic type of breeds; and
(c) the Nordic breeds, Fawn German (Buntes
Deutsche Edelgeiss) and Swiss Saanen relative
to the central European cluster. Essentially,
the same topology was obtained using Greek
Goat instead of the central European cluster to
indicate the phylogenetic root of the network.
© 2016 The Authors. Journal of Animal Breeding and Genetics Published by Blackwell Verlag GmbH • J. Anim. Breed. Genet. 134 (2017) 78–8482
Genetic diversity of Nordic goats J. A. Lenstra et al.
conform to the geographic pattern of breeds relation-
ships. A separate analysis links the Danish and Dutch
Landrace breeds to the network close to the central
European breeds with only spurious relationships
with each other (Figure 3b,c) or of the Dutch Land-
race with the Swiss Saanen (Figure 3c and Figure S1).
We propose that a combination of mixed origin and
severe population bottlenecks during the recovery of
both north-continental breeds has effectively erased
trace of their origin in the microsatellite data set.
Admixture of Swiss Saanen and German Harz goats
during the 19th century in the Danish population has
been documented (http://naturerhverv.dk/landbrug/
genetiske-ressourcer/husdyrgenetiske-ressourcer/husd
yrarter/faar-og-geder/#c9129), but took place well
before the decline of the population. The popular Saa-
nen and Toggenburg were crossed into the Dutch
Land-race in the beginning of the last century and fur-
ther admixture may have occurred during the recovery
of the breed; this might explain the sharing of a short
branch in the networks in Figure 1c and Figure S1.
However, both breeds are characterized by large
horns and diverse multicolour coats similar in appear-
ance to the original landrace populations and the
authentic Finnish and Icelandic breeds. The popula-
tion size of the Danish Landrace is stable but marginal
with only 400 animals. The 2000 Dutch Landrace
goats on the other hand effectively fulfil their role as a
traditional breed. This illustrates that conservation of
phenotypic and molecular diversity should be consid-
ered separately (Hall et al. 2012). The examples of the
Icelandic goats and several other livestock breeds (Hall
2004) also show that phenotypic and molecular varia-
tion is affected in different degrees by a low popula-
tion size.
More in general, maintaining an authentic and
variable phenotype does not guarantee the conserva-
tion of original wide genetic variation of the original
authentic landrace (Hall et al. 2012). This raises the
question whether for goat keepers and breeders pure
genetic ancestry should be a prerequisite for the suc-
cessful revival and maintenance of a breed. Instead,
crossing with genetically related breeds with a similar
appearance originating from a similar environment
avoids the depleting effects of genetic drift and
inbreeding. It may be argued that genetic purity is for
heritage breeds less essential than an authentic
appearance, even if expressed in another genetic con-
text than the original breed. However, other traits of
the original breed have to be conserved as well. In this
respect, adaptation to local conditions and suitability
for extensive management that are typical for
traditional livestock breeds are most important (Doh-
ner 2001; Hall 2004).
Acknowledgements
This study has been supported financially by the
Stichting Zeldzame Huisdierassen.
References
Agaoglu O.K., Ertugrul O. (2012) Assessment of genetic
diversity genetic relationship and bottleneck using
microsatellites in some native Turkish goat breeds. Small
Rumin. Res., 105, 53–60.
Baldursdottir B.K., Kristjansson T., Hallsson J.H. (2012)
Diversity of the Icelandic goat breed assessed using
population data. Acta Agric. Scand. A Anim. Sci., 62, 53–65.
Biebach I., Keller L.F. (2009) A strong genetic footprint of
the re-introduction history of Alpine ibex (Capra ibex
ibex). Mol. Ecol., 18, 5046–5058.
Bulut Z., Kurar E., Ozsensoy Y., Altunok V., Nizamlioglu
M. (2016) Genetic Diversity of eight domestic goat popu-
lations raised in Turkey. Biomed Res. Int., 2016, 283094.
Canon J., Garcia D., Garcia-Atance M.A., Obexer-Ruff G.,
Lenstra J.A., Ajmone-Marsan P., Dunner S., ECONO-
GENE Consortium. (2006) Geographical partitioning of
goat diversity in Europe and the Middle East. Anim.
Genet., 37, 327–334.
Cymbron T., Freeman A., Malheiro M.I., Vigne J.D., Brad-
ley D. (2005) Microsatellite diversity suggests different
histories for Mediterranean and Northern European cat-
tle populations. Proc. Biol. Sci., 272, 1837–1843.
Dohner J.V. (2001) Historic and Endangered Livestock and
Poultry Breeds. Yale University Press, New Haven.
Evanno G., Regnaut S., Goudet J. (2005) Detecting the num-
ber of clusters of individuals using the software STRUC-
TURE: a simulation study.Mol. Ecol., 14, 2611–2620.
FAO. (2011) Molecular Genetic Characterization of Ani-
mal Genetic Resources. FAO Animal Production and
Health Guidlines. No. 9. FAO, Rome.
Frankenhuis M.T., Hazenbroek E. (1984) De Veluwse geit -
heden en verleden. Zeldzaam Huisdier, 9, 6–16.
Glowatzki-Mullis M., Muntwyler J., B€aumle E., Gaillard
C. (2008) Genetic diversity measures of Swiss goat
breeds as decision-making support for conservation pol-
icy. Small Rumin. Res., 74, 202–211.
Groeneveld L.F., Lenstra J.A., Eding H., Toro M.A., Scherf
B., Pilling D., Negrini R., Finlay E.K., Jianlin H.,
Groeneveld E., Weigend S., The GLOBALDIV
Consortium. (2010) Genetic diversity in farm animals: a
review. Anim. Genet., 41, 6–31.
Hall S.J.G. (2004) Livestock Biodiversity. Genetic
Resources for the Farming of the Future. Blackwell Pub-
lishing, Oxford.
© 2016 The Authors. Journal of Animal Breeding and Genetics Published by Blackwell Verlag GmbH • J. Anim. Breed. Genet. 134 (2017) 78–84 83
J. A. Lenstra et al. Genetic diversity of Nordic goats
Hall S.J.G., Lenstra J.A., Deemin D.C., The European Cat-
tle Genetic Diversity Consortium (2012) Prioritization
based on neutral genetic diversity may fail to conserve
important characteristics in cattle breeds. J. Anim. Breed.
Genet., 128, 218–225.
Huson D.H. (1998) SplitsTree: analyzing and visualizing
evolutionary data. Bioinformatics, 14, 68–73.
Lenstra J.A., Groeneveld L.F., Eding H., Kantanen J.,
Williams J.L., Taberlet P., Nicolazzi E.L., S€olkner J.,
Simianer H., Ciani E., Garcia J.F., Bruford M.W.,
Ajmone-Marsan P.M., Weigend S. (2012) Molecular tools
and analytical approaches for the characterization of farm
animal diversity. Anim. Genet., 43, 483–502.
Luikart G., Gielly L., Excoffier L., Vigne J.D., Bouvet J.,
Taberlet P. (2001) Multiple maternal origins and weak
phylogeographic structure in domestic goats. Proc. Natl.
Acad. Sci. USA, 98, 5927–5932.
Mason I.L. (1984) Evolution of Domesticated Animals.
Longman, London and New York.
Minch E. (1997) MICROSAT, version 1.5b, Stanford
University Medical Center, Stanford.
Naderi S., Rezaei H.R., Pompanon F., Blum M.G., Negrini
R., Naghash H.R., Balkiz O., Mashkour M., Gaggiotti
O.E., Ajmone-Marsan P., Kence A., Vigne J.D., Taberlet
P. (2008) The goat domestication process inferred from
large-scale mitochondrial DNA analysis of wild and
domestic individuals. Proc. Natl. Acad. Sci. USA, 105,
17659–17664.
Nomura K., Ishii K., Dadi H., Takahashi Y., Minezawa M.,
Cho C.Y., Sutopo Faruque M.O., Nyamsamba D., Amano
T. (2012) Microsatellite DNA markers indicate three
genetic lineages in East Asian indigenous goat popula-
tions. Anim. Genet., 43, 760–767.
Porter V. (1996) Goats of the World. Farming Press, Ipswich.
Pritchard J.K., Stephens M., Donnelly P. (2000) Inference
of population structure using multilocus genotype data.
Genetics, 155, 945–959.
Reynolds J., Weir B.S., Cockerham C.C. (1983) Estimation
of the coancestry coefficient: basis for a short-term
genetic distance. Genetics, 105, 767–779.
Tresset A., Vigne J.D. (2011) Last hunter-gatherers and
first farmers of Europe. C. R. Biol., 334, 182–189.
Appendix
Members of the ECONOGENE Consortium are as
follows:
Mahamoud Abo-Shehada, Paolo Ajmone Marsan,
Jamil Al Tarrayrah, Antonella Angiolillo, Philip Baret,
Roswitha Baumung, Albano Beja-Pereira, Marco
Bertaglia, Salvatore Bordonaro, Horst Brandt, Mike
Bruford, Regis Caloz, Gabriele Canali, Javier Canon,
Irene Cappuccio, Antonello Carta, Mario Cicogna,
Paola Crepaldi, Stella Dalamitra, Petrit Dobi, Susana
Dunner, Giuseppe D’Urso, M. A. A. El Barody, Phillip
England, Georg Erhardt, Okan Ertugrul, Marie-Louise
Glowatzki, Eveline Ibeagha-Awemu, Ewa Strzelec,
Aziz Fadlaoui, Francesca Fornarelli, David Garcia,
Andreas Georgoudis, Stefano Giovenzana, Katja
Gutscher, Godfrey Hewitt, Anila Hoda, Anton Istvan,
Sam Jones, Stephane Joost, Gabriela Juma, Katerina
Karetsou, Georgios Kliambas, Evren Koban, Daniela
Krugmann, Olga Kutita, Fesus Lazlo, Johannes A.
Lenstra, Christina Ligda, Shirin Lipsky, Gordon Lui-
kart, Gesine L€uhken, Marta Marilli, Donata Marletta,
Elisabetta Milanesi, Riccardo Negrini, Isa€ac J. Nijman,
Roman Niznikowski, Gabriela Obexer-Ruff, Christos
Papachristoforou, Lorraine Pariset, Marco Pellecchia
Peter, Christina, Trinidad Perez, Emilio Pietrola, Fabio
Pilla, Dominik Popielarczyk, Maria-Eva Prinzenberg,
Jutta Roosen, Riccardo Scarpa, Tiziana Sechi, Pierre
Taberlet, Martin Taylor, Inci Togan, Michel Trommet-
ter, Alessio Valentini, Lisette M. Van Cann, Augustin
Vlaic, Louise Wiskin and Stephanie Zundel. For affili-
ations, see www.econogene.eu.
Supporting Information
Additional Supporting Information may be found in
the online version of this article:
Table S1 Geographic origin and diversity statistics
of goat breeds. HE, expected heterozygosity; HO,
observed heterozygosity, FIS, inbreeding coefficient,
n.r, not recorded.
Table S2 Reynolds’ genetic distances between
breeds. For breed abbreviations, see Table S1.
Table S3 Combination of breeds in geographical
clusters for NeighborNet analysis.
Table S4 Microsatellite allele frequencies of four
ibex populations (Biebach & Keller 2009) and of the
Dutch Landrace goat.
Figure S1 NeighborNetwork of Reynolds’ distances
(DR) between goat populations.
Figure S2 NeighborNetwork of DR distances show-
ing a meta-analysis of our breed panel and a data set
of five Turkish breeds indicated by asterisks and shar-
ing 13 microsatellites with our panel. The duplicate
samplings of the Angora breed are tightly linked,
which supports the validity of the meta-analysis and
indicates a close relationship of all sampled Turkish
breeds.
© 2016 The Authors. Journal of Animal Breeding and Genetics Published by Blackwell Verlag GmbH • J. Anim. Breed. Genet. 134 (2017) 78–8484
Genetic diversity of Nordic goats J. A. Lenstra et al.