Assessing inbreeding and loss of genetic variation in canids, domestic Canis familiaris lupus

Assessing inbreeding and loss of
genetic variation in canids, domestic
dog (Canis familiaris) and wolf (Canis
lupus), using pedigree data
Mija Jansson
DEPARTMENT OF ZOOLOGY
DIVISION OF POPULATION GENETICS
STOCKHOLM UNIVERSITY
2014
Cover illustration: Mija Jansson
©Mija Jansson, Stockholm 2014
ISBN 978-91-7447-858-7
Printed in Sweden by US-AB, Stockholm 2014
Distributor: Department of Zoology, Stockholm University
Om saker och ting rullar på
för enkelt är du bergis mitt i
en utförsbacke.
Claes Wiberg
Abstract
Genetic variation is necessary to maintain the ability of wild and domestic populations to genetically adapt to changed selective pressures.
When relationships among individuals are known, conservation genetic management can be based on statistical pedigree analysis. Such
approaches have traditionally focused on wild animal conservation
breeding in captivity. In this thesis, I apply pedigree-based techniques
to domestic and wild animal populations, focusing on two canids – the
domestic dog and the wild wolf.
Main objectives include to 1) develop a means for making any pedigree fit the input requirements of the software Population Management x (PMx) and to use this program to 2) investigate rate of inbreeding and loss of genetic variation in dog breeds, including possible correlations between recent inbreeding and health problems, 3)
estimate effects on inbreeding of the 2010 hunt of the endangered
Swedish wolf population, and to 4) evaluate the potential to genetically support this wolf population through cross-fostering releases of zoo
bred pups from a conservation breeding program.
Results include successfully developing the converter program mPed
(Paper I) and applying both mPed and PMx to dog and wolf pedigrees. I found extensive loss of genetic variation and moderate rates of
recent inbreeding in 26 dog breeds, but no major difference in these
parameters between breeds classified as “healthy” vs. “unhealthy“
(Paper II). I found average inbreeding coefficients to more than double (from F=0.03 to 0.07) and founder genetic variation to decrease by
c. 30 percent over the past few decades in traditional Swedish dog
breeds identified as being of conservation concern (Paper IV). Hunting will make it less likely to reach genetically based Favourable Conservation Status criteria for the Swedish wild wolf population (Paper
III), but release of zoo bred wolves through cross-fostering may potentially almost double founder genetic variation of this population
(Paper V).
This thesis is based on the following papers, which in the text will be
referred to by their corresponding Roman numerals.
I:
Jansson, M., Ståhl, I., Laikre, L. (2013) mPed: a computer
program for converting a text file into a pedigree file used
by the PMx-software for conservation genetic analysis.
Conservation Genetics Resources, 5:651-653.
II:
Jansson, M., Laikre, L. (2013) Recent breeding history of
dog breeds in Sweden: modest rates of inbreeding, extensive
loss of genetic diversity, and lack of correlation between inbreeding and health. Journal of Animal Breeding and Genetics, Article first published online: 2 DEC 2013;
DOI: 10.1111/jbg.12060
III:
Laikre, L., Jansson, M., Allendorf, F. W., Jakobsson, S.,
Ryman, N. (2013) Hunting threatens achieving Favourable
Conservation Status for an isolated, highly inbred wolf population. Conservation Biology, 27: 248-253.
IV:
Jansson, M., Laikre, L. Monitoring rate of inbreeding and
loss of genetic variation in traditional Swedish dog breeds of
conservation concern using pedigree data. (Manuscript)
V:
Jansson, M., Amundin, M., Laikre, L. Supportive release
from a zoo population by cross-fostering can significantly
increase genetic variation in the highly inbred wild Swedish
wolf population. (Manuscript)
Paper III is reprinted with kind permission of the original publisher,
Conservation Biology, which owns the copyrights.
Assessing Inbreeding and Loss of Genetic Variation in Canids,
Domestic Dog (Canis familiaris) and Wolf (Canis lupus), Using
Pedigree Data
Mija Jansson
Division of Population Genetics, Department of Zoology, Stockholm University, SE-106 91, Stockholm, Sweden
INTRODUCTION ..................................................................................................................................... 11
Conserving Genetic Diversity ................................................................................................................. 11
The Founders of a Population ................................................................................................................. 11
Assessing Inbreeding Levels ................................................................................................................... 12
NATIONAL AND INTERNATIONAL CONSERVATION POLICY ................................................ 12
OBJECTIVES ........................................................................................................................................... 14
STUDY SPECIES ..................................................................................................................................... 15
The Domestic Dog .................................................................................................................................. 15
The Wolf ................................................................................................................................................. 16
INBREEDING DEPRESSION ................................................................................................................ 18
Inbreeding Depression in the Domestic Dog .......................................................................................... 18
Inbreeding Depression in the Wild Wolf ................................................................................................ 19
Inbreeding Depression in the Zoo Wolf .................................................................................................. 19
MATERIALS AND METHODS ............................................................................................................. 20
Paper I: The mPed Converter Program .................................................................................................. 20
Paper II: Recent Inbreeding and Health in Dogs .................................................................................... 20
Paper III: Genetic Effects of Wolf Hunting ........................................................................................... 25
Paper IV: Swedish Native Dog Breeds................................................................................................... 25
Paper V: Supportive Release from a Zoo Population ............................................................................. 25
RESULTS .................................................................................................................................................. 26
mPed (Paper I) ........................................................................................................................................ 26
Inbreeding and Health in Dogs (Paper II) .............................................................................................. 27
Genetic Effects of Hunting the Wild Swedish Wolf Population (Paper III) .......................................... 28
Inbreeding and Genetic Variation in Dog Breeds of Conservation Concern (Paper IV) ........................ 29
Supportive Release from a Zoo Population (Paper V)............................................................................ 30
DISCUSSION AND CONCLUSIONS .................................................................................................... 30
ACKNOWLEDGEMENTS...................................................................................................................... 33
9
REFERENCES .......................................................................................................................................... 35
APPENDIX 1 – CONSERVATION GENETIC CONCEPTS IN PEDIGREE ANALYZIS .............. 40
APPENDIX 2 – INBREEDING DISTRIBUTION, SCHILLER HOUND........................................... 43
APPENDIX 3 – INBREEDING DISTRIBUTION, BULLDOG ........................................................... 45
APPENDIX 4 – MEAN KINSHIP DISTRIBUTION, SCHILLER HOUND ...................................... 47
APPENDIX 5 – MEAN KINSHIP DISTRIBUTION, BULLDOG ....................................................... 49
APPENDIX 6 – AUTOSOMAL RECESSIVE DISEASE IN DOMESTIC DOGS ............................. 51
APPENDIX 7 – CHAMPIONSHIPS ....................................................................................................... 60
10
INTRODUCTION
Conserving Genetic Diversity
Many old, domestic breeds, which are not used in large scale commercial production, typically
have a small population size, and many are considered threatened (Lannek 2007). Domesticated
animals are under strong selective breeding that result in a loss of genetic variation (Johansson
and Rendel, 1968), and during recent years conservation genetic focus has increased in domestic
animal populations (Teinberg et al. 1995, Stephens and Splan 2013, Joly et al. 2012, Leroy et al.
2011). This attention includes both scientific efforts and international and national policy work,
including the Global Plan of Action for Animal Genetic Resources adopted in Interlaken,
Switzerland (FAO, 2007).
Traditionally, pedigree analysis for conservation management has focused on zoo populations of
threatened wild animals (Frankhamn et al 2004); available software has been developed in that
context (Ballou et al. 1995). The necessity of conserving genetic variation in wild animals has
been recognized and studied for quite some time (e.g. Chesser et al. 1982). As conservation
genetic management extends to include domestic populations, and as pedigree data becomes
increasingly available also for wild populations, there is an increasing need for methods,
including software, developed for zoo populations (Koch et al 2008, Naish and Hard 2008) to be
applied to populations outside the zoo community.
In statistical pedigree analysis, exact genotypic probabilities are often too complex to compute
even for modern day personal computers. Computer simulations thus become a valuable tool
(Ballou et al. 1995). For example, the Gene dropping (MacCluer et al. 1986) computer
simulation application is frequently used to analyze loss of genetic variation over time in
populations bred for conservation purposes in zoos. Gene dropping simulates how alleles from
individual founders are spread to descendants in the pedigree, and may be used to address a
series of questions relating to allele diversity retention and genotypic similarity among various
groups of individuals in the pedigree (Lacy 1989; Geyer et al. 1989). Examples of the use of
gene dropping include (MacCluer et al. 1986); estimating inbreeding coefficients and the amount
of existing genetic variation in the population, as well as predicting the risk of future loss of
genetic variation (for conservation genetic concepts in pedigree analysis, see further in Appendix
1).
The Founders of a Population
The population founders limit the genetic potential of a population: the amount of genetic
variation in a population cannot exceed that contributed by the founding individuals.
In dog breeds, because of the closed gene pools, founder effects are responsible for several breed
related diseases (Ubbink et al. 1998). Today’s modern breeds have closed gene pools, and 99 %
of 414 dogs from 85 breeds are correctly assigned to their breed in a cluster analysis, meaning
11
that the relationships within a breed are not really questionable. This results in a reduced
population size and an overall increase in genetic drift among domestic dogs (Wayne &
Ostrander 2007). The increase in genetic drift results in a loss of genetic diversity within breeds
and greater divergence among them. In some breeds, genetic variation has been further reduced
by catastrophic events such as World War II (Wayne & Ostrander 2007), which reduced the
number of pure bred dogs during that time. The variation (or lack of variation) in dog traits also
seems to be driven by artificial selection (Vilà et al. 1999). It is possible that the intense
inbreeding during the founding of the breeds made the deleterious recessive alleles widely
spread already within the breeds (Vilà et al. 1999).
For many wild species, it is natural to identify the subgroups within a geographical region, but
this is less natural for purebred dog populations, mainly due to the effective use of popular sires
(Calboli et al. 2008). The wild wolves of Scandinavia, like many other threatened wolfpopulations in the world, suffer from geographic isolation and fragmentation (Liberg and Sand
2009) which leads to no or minimal immigration and that the population could never extend its
original potential.
Assessing Inbreeding Levels
Indications of inbreeding depression has been shown among both domestic dogs and the wild
wolf-population of Scandinavia (e.g. Olafsdottir and Kristjansson 2008; Liberg et al. 2005;
Räikkönen et al. 2006). Many pedigree-dogs have high coefficients of inbreeding (Calboli et al.
2008), and the wild wolves of Scandinavia are, on average, more related than siblings (Paper
III).
Given a situation with no immigration (and a finite population size), inbreeding levels increase
over time. Pedigree analysis is useful to estimate loss of genetic variation due to inbreeding
increases (Calboli et al. 2008). Even though homozygosity in smaller numbers of loci and
inbreeding coefficients or in extreme inbreeding situations (such as selfing) are sometimes
reported to be significantly associated, heterozygosity measured by molecular markers and
inbreeding coefficient are generally uncorrelated (Bolloux et al. 2004).
NATIONAL AND INTERNATIONAL CONSERVATION POLICY
Both wild and domestic animals are explicitly mentioned in the United Nations Convention on
Biological Diversity (CBD; www.cbd.int) and the National Swedish Environmental Objectives.
Other policies handle either wild (The Habitats Directive, 92/43/EEC, available at:
http://ec.europa.eu/environment/nature/legislation/habitatsdirective/index_en.htm) or domestic
populations (Global Plan of Action for Animal Genetic Resources, available at:
www.fao.org/docrep/010/a1404e/a1404e00.htm).
12
The CBD aims at conserving biological diversity, sustaining the use of the components of
biological diversity and fair and equitable sharing of the benefits arising from the utilization of
genetic resources. The importance of conserving genetic variability of domestic populations of
animals and plants is becoming increasingly recognized. The CBD, as well as the National
Swedish Environmental Objectives (www.miljomal.nu), explicitly state that domesticated
animals, and the genetic resources they represent, are part of the biological diversity that should
be conserved, monitored, and sustainably used. Domesticated animals are mentioned as an
indicator for assessing biologic diversity trends (http://www.bipindicators.net/), and Target 13 of
the new Strategic Plan for 2011-2020 explicitly focuses on genetic variation of domestic
populations (www.cbd.int/sp)
The Habitats Directive (92/43/EEC) is the central biodiversity legislation within the European
Union, which forces all member countries to promote a Favourable Conservation Status (FCS) of
certain listed habitats and species, including the wolf (except for a Spanish and a Greek
population). FCS of a species is defined in Article 1i of the Habitats Directive as:
“conservation status of a species means the sum of the influences acting on the species
concerned that may affect the long-term distribution and abundance of its populations within the
territory referred to in Article 2;
The conservation status will be taken as ‘favourable’ when:



population dynamics data on the species concerned indicate that it is maintaining itself
on a long-term basis as a viable component of its natural habitats, and
the natural range of the species is neither being reduced nor is likely to be reduced for
the foreseeable future, and
there is, and will probably continue to be, a sufficiently large habitat to maintain its
populations on a long-term basis”
The Interlaken Declaration on Animal Genetic Resources for food and agriculture has been
signed by 109 countries, including Sweden. The declaration recognizes that there are significant
gaps and weaknesses in national and international capacities to inventory, monitor, characterize,
sustainably use, develop and conserve domestic animal genetic resources, and this needs to be
addressed urgently. It also calls for mobilization of substantial financial resources and long-term
support for national and international animal genetic resources programs.
Wolf conservation is a controversial issue in Sweden, heavily and constantly debated. In this
debate, unfortunately, scientific results are often used to legitimize different, and often
conflicting, positions (Möller-Hansen et al. 2011).
13
OBJECTIVES
The aim of my work is to generate knowledge that will contribute to a sound conservation
genetic management of the domestic dog and the wild wolf, for both species pedigrees exists.
For this thesis, I used pedigree data to address questions relating to rates of inbreeding and loss
of genetic variation (measured in terms of founder alleles; Lacy 1989). The major objectives
were:


To develop a converter that can transform a studbook from a text file (.txt) to an input file
for the pedigree analysis software PMx (.ped; Paper I) which can be analyzed in the free
software Population Management x (Papers II, III, IV, V).
To examine levels and rates of inbreeding and degree of retention of genetic variation in
dog and wolf pedigrees with the specific objective of addressing the following questions:
 Is there a difference in inbreeding levels and retention of genetic variability between
healthy versus unhealthy dog breeds that may imply that recent genetic management
affects their health status? (Paper II.)
 Were levels of inbreeding, kinship and retention of founder genetic variation in the
Scandinavian wild wolf population affected by the hunt in 2010?
(Paper III.)
 What are the rates of inbreeding and loss of genetic variation measured in terms of
founder alleles in 12 dog breeds originating in Sweden, including the 10 breeds
identified as of conservation concern? (Paper IV.)
 What is the potential of a zoo population of wolves, bred for conservation purposes,
to provide genetic support for the genetically weak wild Scandinavian wolf
population? (Paper V.)
14
STUDY SPECIES
The model organisms used in this thesis are the domestic dog (Canis familiaris) and the wolf
(Canis lupus; Figure 1). I provide a brief description of these species relating to this thesis.
Figure 1. Study species of this thesis, wolf left (Canis lupus; photo by Lovisa Häggström) and
domestic dog right (Canis familiaris) as exemplified by a Norwegian elkhound, grey (photo by
Sannse and obtained from en.wikipedia.org).
The Domestic Dog
Although domesticated animal breeds account for only a small number of species, they have had
profound effects on the evolution of human societies and on the course of human history (Ruane
2000). The dog is considered the first domestic animal. Its wild ancestor, the wolf, was probably
domesticated by mobile hunters/gatherers rather than by settled farmers (Savolainen 2007). The
domestication of the dog occurred around 14,000-15,000 years ago (Sundqvist et al. 2006,
Savolainen et al. 2002). Up until 200 years ago, dogs were primarily selected for breeding based
on practical use for hunters and herders, but for a long time dogs have also been used for other
practical purposes such as pulling sledges, guarding property, and as lapdogs to provide warmth
(Beilharz 2007).
In the last centuries, morphology has become the primary focus of selection. Sundqvist et al.
(2006) suggest that most modern dog breeds have a recent origin, probably less than 200 years
old. They also show that there was an unequal contribution of sexes in the origin of modern dog
breeds with fewer males than females contributing genetically.
15
According to phylogenetic studies, dog breeds are organized into a distinct evolutionary
hierarchy with the following primary groups (Wayne and Ostrander 2007; Vilà and Leonard
2007, Table 1, materials and methods, below):




“Herding”
“Mastiff” (including e.g. some terriers)
“Modern European” (from the 1800th)
“Mountain” (including e.g. German shepherd and some spaniels)
There are associations of dog haplotypes with wolf lineages which indicate admixture between
wolves and dogs which could have been an important source of genetic variation for domestic
dogs (Vilà et al. 2003). Some North Scandinavian/Finnish dog breeds were recently proven to
have a different origin than the rest of domestic dog breeds. These breeds are the results of wolf
and dog crossings a few hundred to a few thousand years ago, rather than from one single
domestic event (Klütsch et al. 2009). The breeds are Finnish spitz, Norwegian elkhound (grey),
Norwegian elkhound (black), and Finnish lapphund.
With respect to domestic animal populations, the Swedish Board of Agriculture has identified a
number of traditional Swedish breeds of particular conservation concern, including ten dog
breeds (Lannek 2007). In Paper V, we describe the conservation genetic situation of the dog
breeds that are Sweden’s conservation responsibility.
The Wolf
Recent studies have shown that large carnivores have even greater effects on eco-system than
previously assumed and the grey wolf has been shown to affect not just the fauna but the flora as
well (Ripple et al. 2014) – the wolf is an important species. The wolf (Canis lupus L.) is a native
species of Sweden since the last ice age, but it is currently classified as Endangered (Swedish
Species Information Centre; www.artdata.slu.se). It was hunted to extinction during the first part
of the 20th century. In the mid-1960s the species became protected when only occasional
individuals were observed, but unfortunately this did not prevent their extinction in the first part
of the 20th century. In the winter of 1982-83, a breeding pair was established in the border region
between the Province of Värmland and Norwegian Hedmark and provided the foundation for the
return of the species to the Swedish fauna (Liberg and Sand 2009). These two individuals,
together with a male wolf which immigrated from Finland/Russia around 1990, constitute the
primary genetic basis for the current population more than 300 wolves inhabiting the central part
of the Scandinavian Peninsula. For more than 18 years, none of at least ten wolves that
immigrated via Finland to Northern Scandinavia were able to reach the population in MidScandinavia and contribute genes to the population (Liberg and Sand 2009). New genes were
added in 2008 when two unrelated immigrating male wolves reproduced with females from the
Scandinavian population (Åkesson and Bensch 2010).
16
Figure 2. The location of the
breeding sites for the first five
founders of the Swedish wolf
population. Nyskoga refers to a
mating couple from Nyskoga, all
other founders were males.
Every immigrant is important to the isolated Scandinavian wolf population. Since 2008, only
seven more wolves, apart from the original founders, have migrated into Scandinavia (Ann
Dahlerus, Svenska rovdjursföreningen and Mikael Åkesson, Grimsö Wildlife Research Station,
personal communication, January 2014.). Five of them have had contact with the Scandinavian
wolf population. One of these wolves, a female that was first observed in the northern part of
Sweden in the Province of Norrbotten and later in the Province of Jämtland in 2010
(“Kilbergstiken” later “Junselevargen”), caused damage to reindeer and was subsequently moved
south – three times – only to travel north again. Her first partner was illegally shot following
their first relocation. In 2012, the female settled near Junsele with a new male, but he was shoot
by authorities after killing reindeer. Authorities stopped the hunt on the female after public
complaints and due to EU regulations. The female has currently bonded with a male from
Siljansringen. In 2013, a couple from Finland immigrated and were moved from northern
Sweden to Tiveden where they settled down and had at least three, probably five, pups. Thus,
there are currently seven and one potential founder of the existing Swedish wolf population. This
is a low number from a conservation genetics perspective, because the amount of genetic
variation in a population cannot exceed that contributed by the founding individuals.
The precarious situation of the Swedish wolves has been pointed out for decades (e.g. Laikre
1999, Liberg et al 2005, Hagenblad et al 2009). Rapid population growth and gene flow from
neighboring populations are critical for achieving long-term population viability. Nevertheless,
population levels have been kept low and in 2009, the Swedish Parliament “temporarily” decided
17
that the population should be kept below 210 individuals (Swedish Government 2008/09:210). In
order to achieve this, 28 wolves were culled in 2010 and 19 in 2011. In addition, close to 30
animals were shot in these two years for other reasons (e.g., causing damage to livestock), 16
were killed in traffic and two drowned because of sedation after being tagged with radio
transmitters. In 2014, the Swedish Government decided on a new licensed killing of 30 wolves in
the provinces of Dalarna, Värmland and Örebro even though it is against both Swedish and EU
legalization and after appeals to the administrative court, the Government had to call off the
hunt, at least temporarily.
For the past decades, the issue of viable carnivorous population has been discussed in Sweden. A
population's viability is affected by both external factors, such as climate, food sources and
diseases, and, for populations less than thousands of animals, the population size in itself is
considered a risk as inbreeding leads to less evolutionary potential and inbreeding depression
(Ebenhard and Höggren, 1999).
INBREEDING DEPRESSION
Conservation is particularly complicated in small populations (Franklin1980) because they
inevitably suffer from inbreeding and loss of genetic variation, which may cause inbreeding
depression and loss of evolutionary potential (i.e. the ability to adapt to changes in the
environment; Gyllensten and Ryman 1985). Virtually all the genetic effects which arise in small
populations result from the random sampling of alleles from parents to offspring. This process is
known as genetic drift. In a small population, gene frequencies change rapidly from one
generation to another because of this random process. A small population size may have genetic
effects in both a long-time and short- time ´perspective. Inbreeding depression may occur over a
short period. More long-term, sampling effects causing fluctuations in gene frequencies have
important consequences for the future evolution of the species (Crow and Kimura 1970).
Long-term species survival is dependent on retaining enough genetic diversity both within and
between populations to accommodate new selection pressure brought about by environmental
change (Schonewald-Cox et al. 1983). But there are examples of wild populations with a longterm small and effective population size with small genetic variations that are viable (Rodríguez
et al. 2011).
Inbreeding Depression in the Domestic Dog
In the domestic dog, several breed-related diseases have been attributed to founder’s effect
(Ubbink et al. 1998). Such diseases constitute a huge problem in many dog populations and are
probably threatening their survival (Ubbink et al. 1998). For example, a population of Dutch
Labrador retrievers (with elbow dysplasia) showed estimates of relatedness to seven related
ancestors when modeling the most likely pattern in passage of genetic risk for the disease over
generations (Ubbink et al. 1998). In investigations of cone degeneration (achromatopsia; Yeh et
18
al. 2013) in Siberian husky and Alaskan sled dogs and miniature Australian shepherd, all
affected alleles were shown to be identical by descent, strongly suggesting a founder effect.
Since the miniature Australian shepherd is not known to be genetically related to the Alaskan
Malamute, other breeds may potentially carry the same allele and be affected by cone
degeneration (achromatopsia).
English keeshounds have problems with canine epilepsy. By calculating inbreeding and
identifying common ancestors (under the hypothesis that both parents of an epileptic pup were
themselves carriers; Hall & Wallace 1996), it could be assumed that the predisposition to
epilepsy in keeshounds is determined by a single autosomal recessive gene. In the Icelandic
sheepdog, hip dysplasia was also found to be significantly related to inbreeding depression
(Ólafsdóttir & Kristjánsson 2008).
P G C Bedford, at the Royal Veterinary College in UK, states in an editorial comment in
Animal Welfare 1999 that:
“Within the world of the pedigree dog, competition is extreme – and breeding policy
based on dedication to breed type has resulted in the appearance of some 300 inherited
diseases among canine species worldwide.”
In appendix 6, I have compiled 145 diseases in the domestic dog with autosomal recessive
inheritance.
Inbreeding Depression in the Wild Wolf
The genetic problems of the wild wolf population of Scandinavia include inbreeding depression
(Liberg et al. 2005; Räikkönen et al. 2006). The number of surviving pups per litter during their
first winter after birth are strongly correlated with inbreeding coefficients of pups (R2=0.39,
p=0.001; Liberg et al. 2005). Several congenital malformations of the backbone have been
shown (Räikkönen et al. 2006). Immigration of wolves from eastern populations is essential in
order to counteract the possible manifestation of high frequencies of deleterious traits
(Räikkönen et al. 2006).
Inbreeding Depression in the Zoo Wolf
Previous studies on captive wolves have shown negative effects of inbreeding (Laikre and
Ryman 1991, Laikre et al. 1993). These effects are expressed as a reduction of juvenile weight,
reproduction, longevity and a hereditary form of blindness. Presently, there are no documented
negative effects of inbreeding in the captive population of wolfs (personal communication
January 2014, Mats Amundin, official studbook keeper within the framework of the Swedish
Association of Zoos and Aquaria).
19
MATERIALS AND METHODS
Paper I: The mPed Converter Program
In Paper I, I present the mPed program which we developed to convert studbook data into a
format that can be used in the Population Management x software (PMx; Ballou et al. 2011;
Lacy et al. 2011). PMx is a free software for analysis and conservation management of pedigreed
zoo populations. It provides tools for optimal genetic management of populations for which
preserving genetic diversity is a primary goal. The software can handle large data set outputs of
several parameters relating to inbreeding and loss of genetic variation. PMx is most easily used
as an accessory program to the SPARKS software for studbook management, but it can also be
used as a stand-alone software for population management of the demographic and genetic data
The data must first be prepared in a specific format (.ped, the PMx input file). It is quite timeconsuming, to the point where it is impossible, to create .ped files from else than SPARKS’s
studbooks, with many manual steps.
Paper II: Recent Inbreeding and Health in Dogs
Paper II focuses on the investigation of potential correlations between recent inbreeding and
health in populations of dog breeds recorded in Sweden and those we obtain from the Swedish
Kennel Club. In total, 332,784 individuals from 26 pedigrees (breeds) of domestic dog were
analyzed (Table 2).
I selected populations for analysis by first identifying ‘‘healthy’’ and ‘‘unhealthy’’ breeds based
on information from insurance companies. Statistics reflecting the extent of veterinary care per
dog breed were obtained from Sweden’s four most prominent pet insurance companies for pets
(Agria; http://www.agria.se, Folksam; http://www.folksam.se, If; http://www.if.se, and Sveland;
http://www.sveland.se). The companies Agria, Folksam and Sveland use six price categories (six
being the highest costs for veterinary care per dog, and one the lowest). The “If” insurance
company uses eight price categories (where eight represents the highest costs for veterinary care
per dog, and one the lowest). I ranked dog breeds based on the classifications from the four
companies, respectively, and defined “unhealthy” breeds as those classified as most expensive
with respect to veterinary care by at least three of the four companies. The opposite was done to
identify “healthy” breeds (breeds classified in the category of lowest veterinary care expenses by
at least three of the four companies). I identified 15 “unhealthy” and 11 “healthy” breeds. These
breeds are presented in Table 1, together with the classification of each breed with respect to
type of dog made by the international kennel club FCI (www.fci.be), Parker et al. (2004), and
Wayne and Ostrander (2007), respectively. The number of individuals per pedigree is shown in
Table 2.
20
Table 1. Unhealthy/healthy breeds were chosen from data from insurance companies. The type
of dog is based on the nomenclature from the international kennel club (FCI). The final
classification was based on analysis in the publications of Parker et al. (P. et al. 2004) and
Wayne and Ostrander (W. and O. 2007). We have used the categories of W. and O., namely:
Ancient breeds (A), Herding (H), Mastiff (M), Modern European (E), Mountain (X). In Paper II,
only a certain type of bull terrier - the miniature bull terrier - was studied.
Class
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Healthy
Healthy
Healthy
Healthy
Healthy
Healthy
Healthy
Healthy
Healthy
Healthy
Healthy
Breed
bull terrier
bulldog
bullmastiff
dogo Argentino
German boxer
great Dane
mastiff
Neapolitan mastiff
Rottweiler
shar pei
French bulldog
Bernese mountain dog
dobermann
deer hound
Irish wolfhound
coton de Tuléar
Hamilton hound
Schiller hound
Småland hound
Finnish lapphund
Finnish spitz
Norrbottenspitz
Norwegian buhund
Norwegian elkhound, black
Norwegian elkhound, grey
Siberian husky
Type of breed
(FCI Breeds
nomenclature)
Bulltype terrier
Molossioid breed
Molossioid breed
Molossioid breed
Molossioid breed
Molossioid breed
Molossioid breed
Molossioid breed
Molossioid breed
Molossioid breed
Small Molossian type
Mountain Dog
Pinscher
Sighthound
Sighthound
Companion and Toy
dog
Scenthound
Scenthound
Scenthound
Spitz type
Spitz type
Spitz type
Spitz type
Spitz type
Spitz type
Spitz type
21
Classification
P. et al.
M
M
M
M
E
M
M
A
M
M
E
H
W. and O.
M
M
M
M
H
M
X
A
M
X
E
H
E
A
E
A
Bulltype terriers are terriers that originally were used for fighting (Bull terriers and Staffordshire terriers).
Molossers are solidly built, generally quite large dog breeds mostly used for guarding people or livestock.
Mountain dogs are molossoid breeds but more of a farm dog.
Pinschers (and schnauzers) are continental dogs of the type that in Great Britain are called terriers but
unlike the terriers the pinschers (and schnauzers) were farm dogs.
Sighthounds hunt primarily by speed and sight.
Companion and Toy dogs are small in body size and are primarily used as companions.
Scenthounds hunt primarily by scent.
Table 2. The number of individuals in the pedigree for each of the 26 dog breeds included in
Paper II. The type of breed is based on Federation Cynologique Internationale (FCI) Breeds
nomenclature.
Status
Healthy
Healthy
Healthy
Healthy
Healthy
Healthy
Healthy
Healthy
Healthy
Healthy
Healthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Unhealthy
Full name
coton de Tuléar
Hamilton hound
Schiller hound
Småland hound
Finnish lapphund
Finnish spitz
Norrbottenspitz
Norwegian buhund
Norwegian elkhound, black
Norwegian elkhound, grey
Siberian husky
Bull terrier
Bulldog
Bullmastiff
dogo Argentino
German boxer
great Dane
mastiff
Neapolitan mastiff
Rottweiler
shar pei
French bulldog
Bernese mountain dog
Dobermann pinscher
deer hound
Irish wolfhound
No. in ped.
3563
46571
13660
7118
6465
15449
8176
4123
994
51552
15620
4870
5830
3749
1295
30972
15177
1678
1207
36054
2475
8933
20088
18108
1555
7502
22
The health problems occurring in the breeds classified as unhealthy have been noted by the
Swedish Kennel Club (SKC). Attention to these health issues caused by exterior exaggerations
has been noted for instance in the publication “Special Breed Specific Instructions (BSI) regarding exaggerations in pedigree dogs” for both the individual dog and the development of
the breed as a whole. BSI is handed out to every judge at Swedish dog shows. The aim is to
identify areas of risk and to prevent possible future problems. 10 of the 15 unhealthy breeds in
this study are noted in the BSI, i.e.: Bull Terrier (and Miniature Bull Terrier), Bulldog,
Bullmastiff, German Boxer, Great Dane, Mastiff, Neapolitan Mastiff, Shar Pei, French Bulldog,
and Irish Wolfhound. The origins of the dog breed exteriors are explained by their original tasks,
even though the interpretations of the breed standards do not always reflect their original task.
The molossoid and bulltype breeds are typically heavy and solid. When these physical
characteristics are exaggerated, the exterior becomes unhealthy. The pincher and sighthounds
included in the study are very large in body size for their group of breeds.
Typical molossoid breed diseases are shown in Table 3. Though molossoid breeds show
common problems (they all have skin problems), it is unknown whether this caused by a
common genetic background.
To address the issue of possible temporal trends in average inbreeding and retention of founder
genetic diversity, we analyzed levels of inbreeding and loss of founder genetic variation at three
points in time including dogs alive at 31th of December, 1980, 1995, and 2010, respectively. The
pedigrees of December 31, 2010, represent the full pedigree of each breed (Table 2). The number
of individuals per full pedigree varied from 994 (Norwegian elkhound, black; Table 1) to 47 892
(Norwegian elkhound, grey).
See further Appendix 2-5.
23
Table 3. Typical health problems of some of the breeds classified as unhealthy. Data were obtained from Breeds Specific Strategies
available from the Swedish Kennel Club (http://www.skk.se/hundraser/ [in Swedish]). Breed type classification is based on Parker et
al. 2004 (P et al) and Wayne and Ostrander 2007 (W & O); Mastiff (M) and Mountain (X).
Breed
P et al
W&O
Health problems
immunological diseases (mainly skin diseases), patellaluxation, heart and kidney
problems
bull terrier
M
M
bulldog
M
M
weak contractions, HD1, a large number of skin diseases, eye problems, problems
with circulation and breathing, epilepsy
bullmastiff
M
M
cancer (lymphoma), skin diseases, eye problems, ligament injuries, HD, ED2, aortic
stenosis
German boxer
M
M
HD, osteoarthritis, PNP (kidney disease), heart problems, skin problems, epilepsy,
Cryptorchidism, spondylosis, weak contractions
mastiff
M
M
ear and eye problems, obstetric complications, HD, ED, cruciate ligament injuries,
gastric torsion/bloat stomach, skin problems
Rottweiler
M
X
HD, ED, epilepsi, thyroid diseases
French bulldog
M
M
respiratory problems, eye problems, ear infections/problems, allergies (including
skin), patella dislocationtumors of the mouth/throat sarcoma lymphon, back pain,
epilepsy, othematom, problems in the lower urinary tract
Bernese
mountain
dog
M
X
HD, ED, PNP (kidney disease), umbilical hernia, tumors,
pyometra, cruciate ligament injuries
1
Hip dysplasia
2
Elbow dysplasia
24
Paper III: Genetic Effects of Wolf Hunting
Paper III aimed to investigate if levels of inbreeding, kinship and retention of founder genetic
variation in the Scandinavian wild wolf population were affected by the hunt performed in 2010
and to assess whether the Swedish wolf hunts in 2010 and 2011 were in line with national and
international policy agreements (including agreements within the European Union [EU] of which
Sweden is a part).The study is based on a studbook of the Swedish wild wolf population that has
been generated by the Skandulv Research Project (http://skandulv.nina.no). The Swedish wolf
population has been monitored closely since the establishment in the 1980s. Tracking data in
combination with molecular genetic analysis of collected blood, hair, and other biological
material including tissue from dead animals has resulted in an almost complete pedigree of the
population that is maintained by the Skandulv Project (Liberg et al. 2005). We analyzed the
genetic effects of the 2010 wolf hunt using the pedigree data from the Skandul Project as of
November 2010 obtained from the Skandulv Project. We used the Population Management 2000
software (http://www.vortex9.org/pm2000.html) to compute inbreeding coefficients, mean
kinship, to analyze founder contribution and loss of founder genetic variation. Paper III also
relates wolf hunting and the genetic situation of the Swedish wolf population to existing
international and national conservation policies, particularly the EU Habitats Directive
(http://ec.europa.eu/environment/nature/legislation/habitatsdirective/index_en.htm), the UN
Convention on Biological Diversity (www.cbd.int), and the Swedish national environmental
goals (Swedish Government Bill 2004/05:150, Environmental Quality Objectives - A Shared
Responsibility, adopted by the Swedish Parliament in November 2005).
Paper IV: Swedish Native Dog Breeds
In Paper IV, we described the rates of inbreeding and loss of genetic variation, measured in
terms of founder alleles in 12 dog breeds originating in Sweden, including the 10 breeds
identified as being of conservation concern. The pedigrees of nine of the 12 breeds date back to
the 1960s or before. Four of the breeds were recognized as pedigree breeds relatively late by the
Swedish Kennel Club – the Danish Swedish Farmdog (1987; Table 1), the Gotland hound
(1990), the Swedish white elkhound (1993), and the Hällefors hound (2000). The pedigrees of
these breeds date back to the 1970s for Hällefors hound and to the 1980s for Danish Swedish
farmdog, Gotland hound, and Swedish white elkhound.
To monitor possible temporal trends, we analyzed levels of inbreeding and loss of founder
genetic variation (see below) at five points in time including dogs alive on December 31 in the
years of 1980, 1990, 2000, 2006, 2012, respectively. To determine the number of live dogs at the
three points in time, we had to make assumptions about the longevity of dogs and we only
considered dogs with a Swedish registration number as being alive.
Paper V: Supportive Release from a Zoo Population
This paper describes the potential of a zoo population, bred for conservation purposes, to provide
genetic support for the genetically weak wild Scandinavian wolf population. The pedigree of the
wild Scandinavian wolf population is maintained by the Skandulv Project. We obtained studbook
data as of January 2012, and this pedigree included a total of 740 individuals, 376 of which were
25
classified as being alive. This classification was based on the assumption that identified
individuals that have not yet been documented as dead are alive unless they are unreasonably old
and/or have not been seen for many years.
The pedigree of the captive population is maintained by Mats Amundin, a co-author who
maintains the official studbook keeper within the framework of the Swedish Association of Zoos
and Aquaria. We used pedigree records per January 2012 comprising a 132 total of 1229
individuals out of which 145 were alive at that time.
We used the Population Management x software to obtain the quantities assessed, and mPed to
convert the pedigree of the wild wolf population into PMx input format (see Paper 1 above).
Input files to PMx for the captive population pedigree were generated through PopLink 2.3
(Faust et al. 2012). PopLink is a computer program designed for management and analysis of
studbook databases. (Zoo studbooks include information on each individual in a population,
including pedigrees, and dates of birth, death and transfers between institutions. The studbook
traces the entire history of each individual in a population; these collective histories describe the
population's genetic and demographic identity.) PopLink can help maintain, analyse and export
data for a captive population which are relevant to their genetic and demographic management.
PopLink imports a studbook from SPARKS, the current software used to manage studbook
datasets in Zoos. (Faust et al. 2012.)
RESULTS
In this section, the results are presented by paper.
mPed (Paper I)
To simplify the creation of new ped-files from databases which were not originally constructed
for PMx, we developed a converter called mPed (make ped file) in the C programming language.
The converter we developed (Paper I), proved to be useful in transforming studbook data into a
pedigree file (a .ped file) which can be used by Population Manager x. We had several problems
with some dog pedigrees obtained, including too extensive data for PMx (Table 2), which
typically have an upper limit of about 20,000 individuals, but also depending on the complexity
of the pedigree. mPed was constructed to reduce the file by deleting dead individuals which have
no descendants in the living population. Also, data on date of birth are sometimes missing in the
SKC studbooks, and mPed can help estimate birthdates in such cases. Similarly, the SKC
databases do not include dates of death, but mPed can provide estimated dates. There are also
other ways in which mPed can modify pedigrees, and in addition to providing input files for
PMx, mPed can produce input data to the Vortex Population Viability Analyses Software
simulation program (www.vortex9.org). mPed was successfully used to provide pedigree files
used for Papers II and III.
26
Inbreeding and Health in Dogs (Paper II)
We found extensive loss of genetic variation and moderate rates of inbreeding in all the 26
breeds examined, but no strong indication of a difference in these parameters between healthy
and unhealthy breeds (Table 4). Thus, we conclude that recent breeding history with respect to
inbreeding levels and maintenance of founder alleles does not appear to be a main cause of poor
health in some dog breeds.
Table 4. Summary of results from Paper II regarding healthy and unhealthy breeds at the three
different points of time. Mean values, for all breeds, of founder, founder genome equivalents
(fge), mean kinship (MK) and inbreeding (F).
Health status
Healthy
Healthy
Healthy
Unhealthy
Unhealthy
Unhealthy
Year
1980
1995
2010
1980
1995
2010
Founders
180
137
300
147
256
624
fgeLacy1995
12.6
9.9
12.7
11.8
12.0
22.4
MK
0.05
0.06
0.05
0.07
0.05
0.03
F
0.04
0.05
0.04
0.04
0.04
0.02
Appendices 2-3 show an example of distribution of F for a healthy and an unhealthy breed and
Appendices 4-5 show MK for the same breeds. MK typically varies less than F when the mean
kinship is the theoretical F for the next generation. Figure 3 includes a figure for inbreeding level
and one for genetic variation for all breeds during the years, grouped in “unhealthy” and
“healthy” breeds. The inbreeding Figure (3a) illustrates the lack of a linear trend in inbreeding.
27
Figure 3. Left (a) - Mean inbreeding for breeds, classified as healthy (light) and unhealthy
(dark). The classification of “healthy” or “unhealthy” was based on statistics on extent of
veterinary care obtained from Sweden’s four largest insurance companies for pets. Right (b) The Loss of Genetic Variation measured as Founder Genome Equivalents (fge) per Founder for
each breed, grouped as unhealthy breeds (dark) and healthy breeds (light).
Genetic Effects of Hunting the Wild Swedish Wolf Population (Paper III)
Prior to the 2010 hunt, the wild Swedish wolf population consisted of 209 individuals. Fourteen
of these wolves were protected from hunting because they represented the territories of the two
males that immigrated into Sweden in 2007/2008. This implies that 195 animals were subjected
to hunting.
The mean inbreeding coefficients among the 195 animals was F=0.29. Among the 28 wolves
which were killed, the average inbreeding was F=0.26. This was significantly less than what
would be expected if the 28 animals killed had been selected at random. Average F was at 0.27
after the 2010 hunt. If pedigree data had been used to identify the most inbred individuals,
average F could have been reduced to 0.25. However, reducing the average level of inbreeding
28
should not be the only objective of genetic management in a case like this; it is equally important
to maintain as much as possible of the remaining allelic diversity from the five founders of the
population. Maximizing the retention of their alleles includes reducing further loss of genetic
variation and striving to spread the genes of the two most recent immigrant males to make their
genetic contribution similar to that of the three original founders. During the 2010 hunt,
offspring from the two immigrant males were protected. Thus, the genetic contribution from
these founders was not reduced, but the proportion of lost variation measured as founder allele
survival as calculated from the pedigree increased from 18% to 20% for the two original
founders and from 4% to 5% for the male which immigrated in 1990.
Inbreeding and Genetic Variation in Dog Breeds of Conservation Concern (Paper IV)
Inbreeding is relatively extensive in these breeds with the average F across all breeds exceeding
that of first cousin mating in both 2006 and 2012, and for 8 of the 12 breeds the average F of the
living population exceeds 0.0625 at one or more points over time. Similarly, the ranges of F
within breeds show conspicuously high inbreeding coefficients for at least individual dogs within
all breeds.
There is no correlation between average F and population size and there is no correlation
between F and the number of founders at any of the points in time, indicating that, contrary to
what would be expected; number of founders or population size does not explain inbreeding
levels.
MK is used in conservation breeding to choose breeding animals; by prioritizing low MK,
individual inbreeding and loss of founder genetic variation is minimized. Average and range of
MKs among the Swedish dog breeds show that such prioritization has typically not been carried
out for these breeds. In many cases, average MK at one point in time is lower than average F for
the next time point. For instance, average F for the Swedish lapphund is consistently larger than
the average MK for the prior time point. In contrast, for the Swedish white elkhound, the
Norrbotten spitz, the Danish Swedish farmdog, and the Gotland hound, the average F is below
the MK of the preceding time step, indicating that dogs chosen for breeding have had lower MK
than the average among living dogs. Comparing ranges of MK to ranges of F, however, indicates
that for none of these dogs, breeding animals are consistently chosen to primarily reduce
inbreeding and retain genetic variation.
Genetic variation is measured in relation to population founders as the proportion of founder
alleles that remain among living animals at separate points in time, and the results show that the
loss of such variation is extensive. Similar results are observed when retention of founder alleles
is quantified as founder genome equivalents. The result indicate that current gene pools of
separate Swedish traditional dog breeds represents variation of less than 20 unrelated founders,
and in many cases less than 10 unrelated founders.
29
Supportive Release from a Zoo Population (Paper V)
We combined the pedigrees of the captive and wild populations to investigate the potential for
genetic support from the zoo to the wild. The joint population has 15 founders and 21 of their
alleles remain, fgeLacy1995= 3.2 and fgeLacy1989=4.8. Thus, founder genetic variation of the wild
wolf population can be almost doubled using genetic support from the zoo. We computed target
values for genetic contribution of separate founders taking their retention of genetic variation
into account, and found that for maximum founder allele retention, the zoo founders should
contribute just below 50 percent to a joint population.
We investigated how much of the genetic variation of the zoo population would remain in
five or ten hypothetical offspring from each of eight established captive breeding pairs existing
at the time of our data collection. For separate PMx runs, we assumed that only hypothetical
offspring (5 or 10) from a particular pair was alive. The amount of remaining founder genetic
variation is consistent and not much affected by the number of offspring (5 or 10). The
remaining number of founder alleles is around 3.5, representing 30 percent of current levels of
variation . Further, if all eight pairs produced either 3 or 5 offspring, resulting in 24 or 40
hypothetical pups and assuming only these pups remain alive, the number of retained founder
alleles is 9.9 or 10.3, fgeLacy1995 is 3.0 or 3.1, and fgeLacy1989 is 4.6 or 4.7, respectively. Thus, both
3 and 5 pups per pair retain a large proportion of the remaining genetic variation of the zoo
population.
Founder allele retention can be computed for a large number of hypothetical combinations of
reproducing pairs. Our limited analysis indicates that a relatively large proportion of the founder
allelic gene pool of the captive population can be maintained by a limited part of the population.
DISCUSSION AND CONCLUSIONS
Even though pedigree information can be used to monitor and control inbreeding in a population,
molecular data can also be used. A study shows that the heterogeneity found when estimating the
alleles identical by descent between pairs of dogs ranged from 0 to 0.60 within the same breed
(Pertoldi, 2013). The 0.6 value is much higher than common inbreeding levels (and this is
probably due to early inbreeding in the origin of breeds). Despite this, pedigree analysis is more
cost-effective when investigating recent inbreeding in large dog populations.
In this section, I will briefly go through the conclusions for the different papers followed by
some discussion.
Developing a converter that can transform a studbook from a text file (.txt), to a input file for the
PMx pedigree analysis software (.ped; Paper I): Me and my colleagues were able to develop the
mPed converter program which allows for a broad range of pedigrees outside the zoo community
30
to be easily analysed using already available software specializing in conservation genetic
management. This includes domestic populations such as rare breeds subjected to conservation
breeding programs in Sweden (e.g. Wennerström 2009) and wild populations for which
pedigrees are becoming available for an increasing number of populations (e.g. Naish and Hard
2008).
We then used mPed to address conservation genetic issues using domestic dog (Paper II and IV)
pedigrees and the pedigree of the wild Swedish wolf population (Paper III and V), the estimated
inbreeding, mean kinship and loss of founder-genetic variation in these populations.
Is there a difference with respect to inbreeding levels and retention of genetic variability in
healthy versus unhealthy dog breeds that could imply that recent genetic management affects
health status? (Paper II.) We found no difference regarding inbreeding levels or retention of
genetic variation in dog breeds which are classified as unhealthy versus those classified as
healthy. Thus, inbreeding and loss of variation over the last few decades do not seem to be
associated with the health problems in many dog breeds. It is possible that the initial inbreeding
and founder effects associated with the creation of separate dog breeds are the major causes of
these health issues. The fact that the same type of defects occur in closely related breeds supports
this idea.
The temporal tendency of reduced inbreeding levels and an increasing number of founders
indicate that these Swedish dog populations are not closed, but dogs from other pedigrees of the
same breeds in other countries are added to the majority of these populations. Firstly, inbreeding
and mean kinship coefficients may be underestimated in cases where imported dogs have
ancestors in the Swedish population, but further back than three generations (which is what is
registered). Imported dogs may be regarded as unrelated to the Swedish population while, in
fact, they are not.
Secondly, founder statistics could be affected; if an imported dog does not have Swedish
ancestors in its pedigree three generations back, up to eight new founders will be added to the
Swedish population of the breed. The exact number depends on potential relationships among
the dogs of the three generations back pedigree of the imported dog. If one dog occurs in several
places in this pedigree, the number of added founders will be less than eight.
The need for international collaboration on dog studbook data is being increasingly recognized
(Wilson and Wade 2012, Fikse et al 2013). Pooling of pedigree and phenotype data from
different countries may improve the accuracy of derived indicators of both genetic diversity and
genetic merit of traits of interest (Fikse et al 2013). There is many interesting questions that
could be answered with sush an international database, one I would like to investigate is if there
is any difference regarding dogs that are bred for work or show (mesuered by championships,
see Appendix 7. Even when the studbooks are linked together in an international database, it
would be interesting to estimate founder relationships (Haig et al. 1994) as most dog breeds are
supposed to be created from only a few breeding animals.
What are the rates of inbreeding and loss of genetic variation measured in terms of founder
alleles in 12 dog breeds originating in Sweden, including the 10 breeds identified as being of
conservation concern? (Paper IV.) I found average inbreeding coefficients to more than double
(from F=0.03 to 0.07). Retention of founder alleles is quantified as founder genome equivalents.
The range of fgeL89 and fgeL95 among live dogs in 2012 is 5.0-18.2 and 3.3-11.5, respectively.
31
The averages over all breeds are fgeL89=13.0 and fgeL95=7.1, respectively, indicating that current
gene pools of separate Swedish traditional dog breeds represents variation of less than 20
unrelated founders, and in many cases less than 10 unrelated founders.
Were levels of inbreeding, kinship and retention of founder genetic variation in the Scandinavian
wild wolf population affected by the hunt in 2010? (Paper III.) With respect to the wolf pedigree,
the 2010 hunt resulted in 28 animals being killed, and they were on average less inbred than
expected from a random sample among the 195 wolves subjected to the hunt. On average two
percent of the remaining genetic variation from the original Nyskoga founders (G1-83, D85-01;
Figure 2) were lost during the hunt and one percent of the remaining variation from the Gillhov
male founder (G1-91; Figure 2). We conclude that the official hunts decided by the Swedish
Government have not contributed to the genetic health of the population. Furthermore, the hunt
was not carried out in a manner that agrees with adaptive management because available
pedigree information was not used in the best possible way. For example, a common
conservation genetic recommendation when genetically managing populations with a known
pedigree is to identify and remove individuals with the highest mean kinship (Lacy 1995).
Relating the genetic situation of the Swedish wild wolf population and the hunt to international
and national conservation policies, we conclude that hunting to reduce wolf numbers in Sweden
is currently not in line with national and EU policy agreements and will make it less likely that
genetically based FCS criteria are achieved for this species. To reach FCS for the wolf in
Sweden, we suggest that the following criteria need to be met: i) a well-connected, large,
subdivided wolf population across Scandinavia, Finland and the Russian Karelia-Kola region
must be reestablished, ii) a genetically effective population size (Ne) with a minimum range of
Ne=500-1000, iii) Sweden should harbour a part of this total population that substantially
contributes to the total Ne, and which is large enough not to be classified as threatened
genetically or according to IUCN Red List criteria, and, iv) average inbreeding levels in the
Swedish population of <0.1.
What is the potential of a zoo population of wolves, bred for conservation purposes, to provide
genetic support to the weak wild Scandinavian wolf population? (Paper V.) We conclude that the
zoo wolf population held in northern European zoos can contribute genetically to the wild
Swedish wolf population. Genetic variation measured as founder alleles can be almost doubled.
Relatively few zoo wolves are needed to capture the remaining genetic variation of that
population – 3-5 offspring from each of the eight established breeding pairs would retain 90
percent of the remaining founder alleles, and over 95 percent of the remaining genetic variation
measured as founder genome equivalents (Lacy 1989, 1995). Theoretically, 24-40 wolf pups
could therefore retain the genetic variation of the captive population. In practice, however, the
number of wolves needed to transfer and establish this variation into the wild will depend on the
survival and reproduction of the released wolves and their descendants. The genetic relationship
between the zoo and the wild populations and current levels of close relationships precludes a
reduction of inbreeding below the management target of 0.1 (Hansen et al 2011). Thus, release
of genes from zoos cannot fully resolve the genetic problems of the wild population.
32
ACKNOWLEDGEMENTS
Först och främst – tack till min handledare Linda Laikre för din enorma insats för att få till den
här avhandlingen, för att du gav mig chansen, för den här tiden och för allt jag har lärt mig av
och tack vare dig och, inte minst, tack för alla skratt.
Stort tack också till min biträdande handledare Nisse Ryman för din konstruktiva kritik, för allt
du kommer på när du ber om att få vara ifred och för att du är så inspirerande.
Tack till Hasse Temrin och Bengt Karlsson, i min uppföljningsgrupp samt Birgitta Tullberg som
bistod när jag, eller om det var avhandlingen, eller både och kanske, krisade lite. Tack också till
Hasse för gott samarbete och roliga lärorika stunden på och kring kursen ”Hundens evolution,
genetik och beteende, orienteringskurs, 7.5 hp” och för hundsnack i största allmänhet.
Tack till mina medförfattare: Fred Allendorf (University of Montana); big thanks, Sven
Jakobsson (Tovetorps forskningsstation), Mats Amundin (Kolmårdens djurpark) and Ingvar
Ståhl. Ingvar, avdelningens IT-konsult och programmerare, har bidragit mycket till denna
avhandling.
Stort tack också till Thomas Wink, Svenska kennelklubbens IT-avdelning, för data och support.
Tack till alla, nuvarnade och tidigare kollegor på avdelningen för populationsgenetik:
Karin Tahvanainen att Fjant är lugn på labbet med dig men inte någon annanstans på kontoret
talar sitt tydliga språk.
Lovisa Wennerström – jag har sagt det förut, men, på riktigt, jag hade blivit galnare utan dig. Du
är och har varit ovärderlig.
Lena Larsson, Anna Palmé och Johan Charlier: tack för att ni ”skolade in mig” som doktorand
och för att jag fått återkomma med frågor även sedan ni slutat på avdelningen. Givetvis också
tack för social samvaro, i fält i Jämtland såväl som på Stockholms krogar.
Tidigare examensstuderande på avdelningen har också bidragit till den här avhandlingen. Tack
för hjälpen och trevligt sällskap Peter Guban, Rebecka Salamon och Anastasia Andersson som
numera är doktorand på avdelningen.
Thanks to the new group in the division of population genetics – the butterfly people led by
Chris Wheat. Alyssa Woronik, Naomi Keehnen, Peter Pruisscher, Ramprasad Neethiraj and
Jason Hill, thanks for a breath of fresh air (and good beers).
Thank you to all, present and former, colleagues at the Department of Zoology. I have had a
great time. (And thanks to Facebook for keeping me in touch with so many of you.)
Tack, James Dickson, för tio år med en intelligent över-akademisk snubbe med skruvad humor.
Tack, Peppe Tapper, som hjälpte mig med taktiken inför floristiken, trots att jag ringde mitt
under en fotbollslandskamp (utan floristik ingen examen och ingen doktorandtjänst).
Tack, Petra Nilsson Lindström, som tidigt tyckte att det var ”självklart” att jag skulle doktorera
och som har varit ett stöd genom hela processen.
Tack, Anders Nyholm, för ego-livscoaching när jag behövde det som bäst.
33
Tack, styrelsekollegor i Solna agilityklubb och Ms Xlntdog Veronica Bache för att att ni hjälpt
mig få till bra agilityträning – det roligaste jag vet och absolut nödvändigt för att jag ska fungera.
Tack också till Mrs Klickerklok Fanny Gott för att du så ofta är tillgänglig för att reda ut diverse
agilityteoretiska frågetecken (utan dessa utredningar hade jag haft väldigt svårt att fokusera på
någon avhandling).
Tack, Mari Edman, för alla gånger du hjälpt mig få ordning på orden och allt annat.
Tack, Helene Wallskär för att du funnits för mig och för att du är en sådan smart och kul prick.
Tack, Sussie Strandberg och Annica Vestman – riktiga vänner är sådana som vet hur illa det är
men finns kvar ändå, eller kanske just därför.
Tack, farmor för att du lärde mig om skogen och hur man ska få svampar att anfalla en och
sådant. Och tack för att du är så stolt över mig.
Tack, morfar för att du vågat vägra Jante och grattis till hedersdoktorstiteln i medicin. Jag vill
bara påpeka att jag skrivit en avhandling för att få min titel.
Tack, mamma och pappa för att ni såg till att jag pluggade. Det blev ju riktigt kul, till slut.
Till alla mina syskon: Micke, Magnus, Marcus och Moa - innan någon av er påstår att att
doktorera inte är ett arbete nästa gång så vill jag se era avhandlingar. Puss! Tack också för de
visdomsord vi kommit fram till här i livet:
Låt inte andras solsken tränga igenom dina mörka moln.
When nothing goes right – go to sleep!
I vanliga fall skulle jag tycka att det var rätt så töntigt att tacka sina hundar men i det här fallet
känns det berättigat. För det finns naturligtvis ingen som påverkat mitt hundintresse så starkt
som just mina hundar och det var genom att lära känna hunden som art som mitt allmänna
djurintresse väcktes.
I hundhimlen: Cosy (flat), Smulan (cavalier), Sasha (cavalier) och Jojje (BC).
Mina nuvarande hundar har i allra högsta grad bidragit positivt till mitt välbefinnande och
därmed till mitt arbete som doktorand:
Råttan (kelpie, född 2001) har bland annat varit en riktig hjälte i fält och hon stökar till livet på
ett härligt vis i största allmänhet.
Rasken (Råttans son, född 2006) är ett riktigt agilitygeni vilket givit mig obeskrivlig glädje.
Fjant (BC, född 2013) har kanske mest ”bidragit” till denna avhandling som dokumentförstörare
och elektroniksaboterare men han är väldigt söt.
TACK!
34
REFERENCES
Ballou, J.D., Gilpin, M., Foose, T.J. (eds). (1995). Population Management for Survival and
Recovery. Analytical methods and strategies in small population conservation. Columbia Press.
Ballou, J.D., Lacy, R.C., Pollak, J.P. (2011). PMx: Software for Demographic and Genetic
Analysis and Management of Pedigreed Populations (Version 1.0). Chicago Zoological
Society, Brookfield, Illinois. http://www.vortex9.org/PMx.html.
Balloux, F., Amos, W., Coulson, T. (2004). Does heterozygosity estimate inbreeding in real
populations? Molecular Ecology 13: 3021–3031.
Beilharz, R. (2007). Evolutionary Aspects on Breeding of Working Dogs. Pages 166-181 in P.
Jensen, editor. The Behavioral Biology of Dogs. Cabi Publishing, Oxfordshire.
Calboli, F.C.F., Sampson, J., Fretwell, N., Balding, D. J. (2008). Population Structure and
Inbreeding from Pedigree Analysis of Purebred Dogs. Genetics 179: 593-601.
Chesser, R. K., C. Reuterwall, and N. Ryman. (1982). Genetic differentiation of scandinavian
moose alces-alces populations over short geographical distances. Oikos 39:125-130.
Crow, J. F., and Kimura, M. (1970). An introduction to population genetics theory. Times
Printers Sdn, Singapore.
Ebenhard, T. and Höggren, M. (red; 1999) Livskraftiga rovdjursstammar. CBM:s
Rovdjursseminarium 12 oktober 1998. CBM:s Skriftserie 1, Centrum för Biologisk Mångfald,
Uppsala.
FAO (2007). Report of the International Technical Conference on Animal Genetic Resources for
Food and Agriculture. Interlaken, Switzerland, 3 – 7 September 2007. FAO – Food and
Agriculture Organization of the United Nations, Rome, Italy.
Faust, L.J., Bergstrom, Y.M., Thompson, S.D., Bier, L., (2012). PopLink Version 2.3 Lincoln
Park Zoo, Chicago, IL.
Fikse, W.F., Malm, S., Lewis, T.W. (2013). Opportunities for international collaboration in dog
breeding from the sharing of pedigree and health data. The Veterinary Journal 197:873-875.
Frankham, R., Ballou, J.D., Briscoe, D.A. (2004). A Primer of Conservation Genetics.
University Press, Cambridge.
Franklin, I. R. (1980). Evolutionary change in small populations. Pages 135-135-150 in M.E.
Soule and B.A. Wilcox, editors. Conservation biology - an evolutionary-ecological
perspective. Sinauer Associates, Sunderland, Massachusetts.
Geyer, C.J., Thompson, E.A., Ryder, O.A. (1989). Gene survival in the Asian wild horse (Equusprezwalskii). 2. Gene survival in the whole population, in subgroups, and through history. Zoo
Biology 8:313-329.
35
Gyllensten, U., and N. Ryman. (1985). Bevarande av genetiska resurser – En kunskapsöversikt
med förslag till åtgärds- och forskningsprogram. 3004. Statens naturvårdsverk, Solna, Sweden.
Möller-Hansen, M., Wesley Andersen, L., Aspi, J., Fredrickson, R. (2011). ”Minst 3 000 djur
behövs för att vargen ska överleva”. Dagens Nyheter 2011-02-08
[http://www.dn.se/debatt/minst-3-000-djur-behovs-for-att-vargen-ska-overleva/]
Haig, S.M., Ballou, J.D., Casna, N.J. (1994) Identification of kin structure among Guam rail
founders: a comparison of pedigrees and DNA profiles. Molecular Ecology 3: 109-119.
Hagenblad, J., Olsson, M., Parker, H.G., Ostrander, E.A., Ellegren, H. (2009). Blackwell
Publishing Ltd Population genomics of the inbred Scandinavian wolf. Molecular Ecology
18:1341–1351.
Hall, S. J. G., and M. E. Wallace. 1996. Canine epilepsy: A genetic counselling programme for
keeshonds. The Veterinary record 138:358-360.
Hansen, M. M., L. W. Andersen, J. Aspi, and R. Fredrickson. 2011. Evaluation of the
conservation genetic basis of management of grey wolves in Sweden. Swedish large carnivore
inquiry. Publisher: Statens Offentliga Utredningar (The Swedish Government’s Official
Investigations), SOU 2011:37. Available at: http://www.artdata.slu.se/filer/Evaluation-of-theconservation-genetic-basis-of-management-of-grey-wolves-in-Sweden.pdf (accessed January
2014).
Johansson, I., Rendle, J. (1968). Genetics and Animal Breeding. Oliver and Boyd, London, UK.
Joly, T., Neto, V. & Salvetti, P. (2012). Cryopreservation of genetic diversity in rabbit
species (Oryctolagus cuniculus). In Current Frontiers in Cryopreservation: 179-186. Katkov,
I.I. (Ed.). InTech, Open Access Publisher (www.intech.com).
Klütsch, C., Seppälä, E.H., Fall, T., Uhlén, M., Hedhammar, Å., Lohi, H., Savolainen, P. (2009).
Regional occurrence, high frequency but low diversity of mitochondrial DNA haplogroup d1
suggests a recent dog-wolf hybridization in Scandinavia. University Press, Cambridge. Animal
Genetics 42: 100-103.
Koch, M., Hadfield, J.D., Sefc, K. M. Sturmbauer, C. (2008). Pedigree reconstruction in wild
cichlid fish populations. Molecular Ecology 17:4500–4511.
Lacy, R.C. (1989). Analysis of founder representation in pedigrees: Founder equivalents and
founder genome equivalents. Zoo Biology 8:111-124.
Lacy, R. (1995). Clarification of genetic terms and their use in the management of captive
populations. Zoo Biology 14:565-578.
Lacy R.C., Ballou J.D., Pollak J.P. (2011). PMx: software package for demographic and
geneticanalysis and management of pedigreed populations. Methods in Ecology and Evolution
3:433–437.
Laikre, L. (1999). Conservation genetics of Nordic carnivores: lessons from zoos. Hereditas
130:203-216.
36
Laikre, L., and N. Ryman. (1991). Inbreeding depression in a captive wolf (Canis lupus)
population. Conservation Biology 5:33–40.
Laikre, L., N. Ryman, and E. A. Thompson. (1993). Hereditary blindness in a captive wolf
(Canis lupus) population: frequency reduction of a deleterious allele in relation to gene
conservation. Conservation Biology 7:592–601.
Lannek, J. (2007). Delmål för husdjursgenetiska resurser åren 2010 till 2020. Underlagsrapport
inför den fördjupade utvärderingen av miljökvalitetsmålarbetet 2009. Jordbruksverket, Avel- och
djurhållningsenheten 2007-04-17. [online]
<http://www.sjv.se/download/18.b1bed21121e26684180006145/rapport+070511> Jönköping,
Sverige, Juni 2008 [2008-06-16].
Leroy G. (2011). Genetic diversity, inbreeding and breeding practices in dogs: Results
from pedigree analyses. Vet. J., 189, 177–182.
Liberg, O., Andrén, H. Pedersen, C.-H., Sand, H., Sejberg, D., Wabakken, P., Åkesson, M.,
Bensch, S. (2005). Severe inbreeding depression in a wild wolf Canis lupus population.
Biology Letters 1:17-20.
Liberg, O., Sand, H. (2009). Measures to strengthen the genetic situation of the Swedish wolf
population. Immigration history, demographics, policy options and international experience of
the transport of wolves. Report to the Swedish Environmental Protection Agency, included in
Appendix 1 of the Swedish Environmental Protection Agency´s report to the Swedish
Government no: Dnr 429-8585-08 Nv. Swedish Environmental Protection Agency, Stockholm,
Sweden (in Swedish).
MacCluer, J.W., VandeBerg, J.L., Read, B., Ryder, O.A. (1986). Pedigree analysis by computersimulation. Zoo Biology 5:147-160.
Naish, K.A., Hard, J.J. (2008). Bridging the gap between the genotype and the phenotype:
linking genetic variation, selection and adaptation in fishes. Fish and fisheries 9:396-422.
Olafsdottir, G.A., Kristjansson, T. (2008). Correlated pedigree and molecular estimates of
inbreeding and their ability to detect inbreeding depression in the Icelandic sheepdog, a recently
bottlenecked population of domestic dogs. Conservation Genetics 9(6).
Parker, H.G., Kim, L.V., Sutter, N.B., Carlson, S., Lorentzen, T.D., Malek, T.B., Johnson,
G.S., DeFrance, H.B., Ostrander, E.A., Kruglyak, L. (2004). Genetic Structure of the Purebred
Domestic Dog. Science 304:1160-1164.
Pertoldi, C. Kristensen, T.N., Loeschcke, V., Berg, P., Praebel, A., Stronen, A.V.,
Proschowsky, H.F., Fredholm, M. (2013). Characterization of the genetic profile of five
Danish dog breeds. Journal of Animal Science 91:5122-5127.
Ripple, R.W., Estes, J.A., Beschta, R.L., Wilmers, C.C., Ritchie, E.G., Hebblewhite, M., Berger,
J., Elmhagen, B., Letnic, M., Nelson, M.P., Schmitz, O.J., Smith, D.W., Wallach, A.D., Wirsing,
A.J. (2014) Status and Ecological Effects of the World’s Largest Carnivores. Science 343:151162.
37
Ruane, J. (2000). A framework for prioritizing domestic animal breeds for conservation purposes
at the national level: a Norwegian case study. Conservation Biology 14:1385-1393.
Rodríguez, R., Ramírez, O., Valdiosera, C.E., García, N., Alda, F., Madurell-Malaperia, J.,
Marmi, J., Doadrio, I., Willerslev, E., Götherström, A., Arsuaga, J.L., Thomas, M.G., LaluezaFox, C., Dahlén, L. (2011). 50,000 years of genetic uniformity in the critically endangered
Iberian lynx. Molecular Ecology. (18):3785-3795.
Räikkönen, J., Bignert, A., Mortensen, P., Fernholm, B. (2006). Congenital defects in a highly
inbred wild wolf population (Canis lupus). Mammalian Biology 71: 65-73.
Savolainen, P. (2007). Domestication of Dogs. Pages 21-37 in P. Jensen, editor. The Behavioural
Biology of Dogs. 1st edition. Cromwell Press, UK.
Savolainen, P., Y. Zhang, J. Luo, J. Lundeberg, and T. Leitner. (2002). Genetic evidence
for an East Asian origin of domestic dogs. Science 298:1610-1613.
Schonewald-Cox, C. M., S. M. Chambers, B. MacBryde, and L. Thomas. (1983). Genetics and
conservation. The Benjamin/Cummings publishing company, Melno Park, California.
Stephens, T.D. & Splan, R.K. (2013). Population history and genetic variability of the
American Shire horse. Animal Genetic Resources, 52: 31–38.
Sundqvist, A., Björnerfeldt, S., Leonard, J.A., Hailer, F., Hedhammar, Å. Ellegren, H., Vila,
C. (2006). Unequal contribution of sexes in the origin of dog breeds. Genetics 172:1121-1128.
Swedish Government. (2009). Regeringens proposition 2008/09:210. En ny
rovdjursförvaltning. (Swedish Government bill 2008/09:2010. A new large carnivore
management plan (In Swedish). 72 pp.
Teinberg, R., Kalamees, K. & Kallaste, A. (1995). Native cattle and horse breeds in Estonia.
Animal Genetic Resources 16: 65-70.
Ubbink, G. J., van de Broek, H.A.W., Hazewinkel, H.A.W.K., Rothuizen, J. (1998). Risk
estimates for dichotomous genetic disease traits based on a cohort study of relatedness in
purebred dog populations. The Veterinary Record 142(13).
Vilà, C., Leonard, J.A. (2007). Origin of Dog Breed Diversity. Pages 38-58 in P. Jensen, editor.
The Behavioural Biology of Dogs. 1st edition. Cromwell Press, UK.
Vilá, C., Maldonado, J.E., Wayne, R.K. (1999). Phylogenetic relationships, evolution, and
genetic diversity of the domestic dog. The American Genetic Association 90:71-77.
Vilà, C., Walker, C., Sundqvist, A.-K., Flagstad, O., Andersone, Z., Casulli, A., Kojola, I.,
Valdmann, H., Halverson, J. Ellegren, H. (2003). Combined use of maternal, paternal and biparental genetic markers for the identification of wolf-dog hybrids. Heredity 90:17-24.
Wayne, R.K., Ostrander, E.A. (2007). Lessons learned from the dog genome. Trends in genetics,
23:557 – 567.
38
Wilson, B.J., Wade, C.M. (2012). Empowering international canine inherited disorder
management. Mammalian Genome (2012) 23:195–202
Wennerström, L. (2009). Bevarandegenetisk status hos gotlandskanin – en svensk lantras.
Examensarbete, Avdelningen för populationsgenetik, Zoologiska Institutionen, Stockholms
universitet.
Yeh, C.Y., Goldstein, O., Kukekova, A.V., Holley, D., Knollinger, A.M., Huson, H.J., PearceKelling, S.E., Acland, G.M., Komáromy, A.M. (2013). Genomic deletion of CNGB3 is identical
by descent in multiple canine breeds and causes achromatopsia. BMC Genet 14:27-38.
Åkesson, M., Bensch, S. (2010). Undersökning rörande flytt och jakt på varg; delredovisning
från Leverantör 4 på uppdrag av Naturvårdsverket (dnr 235-3697-10). (Investigation concerning
migration and hunting of wolves; interim report from Supplier 4 for the Environmental
Protection Agency ref no 235-3697-10.), Swedish Environmental Protection Agency, Stockholm,
Sweden (in Swedish).
Some text in this thesis is reused from my doktoranduppsats and licentiate thesis:
Jansson, M. (2009). Conservation genetic management of domestic animals with particular focus
on the dog (Canis familiaris). Doktoranduppsats, 2009:3, Populationsgenetik, Zoologiska
instititutionen, Stockholms universitet.
Jansson, M. (2012). Assessing inbreeding and loss of genetic variation in Canids, domestic dog
(Canis familiaris) and wolf (Canis lupus), using pedigree data. Licentiatavhandling 2012:3,
Populationsgenetik, Zoologiska instititutionen, Stockholms universitet.
39
APPENDIX 1 – CONSERVATION GENETIC CONCEPTS IN PEDIGREE ANALYZIS
Below is a brief description of some common concepts and functions applied in conservation
genetic pedigree analyses that were used in this thesis.
Founder
A founder is an individual at “the top” of the pedigree that is expected to be unrelated to all other
founders and to all other individuals in the pedigree except for its descendants.
As applied in the PMx software only individuals that have living descendants in the population
are considered to be founders.
Mean kinship (MK)
The MK is the mean kinship coefficient between one individual and all living animals, including
the individual itself, in the population. An individual that has an unknown (UNK) parent is
considered haploid and has kinship one (1) with itself. As a consequence an individual that has
several UNK in its studbook might have MK higher than one.
Founder genome equivalents (fge, Lacy 1989)
The fge is the number of founders that the living population of today corresponds to.
fge = 1 / ∑(pi2/ri)
pi = the proportion of the genes in the living population given by a founder (representation)
ri = (retention) proportion of founder i:s alleles represented in descendants in the living
population
Examples, exploring the fge when two founders mate and have one offspring:
p=0.5
r= 0.5
fge = 1/(0.25/0.5)+(0.25/0.5) = 1
Founder genome equivalents (fge, Lacy 1995)
In the 1989 paper Lacy states that fge is “that number of equally contributing founders with no
random loss of founder alleles that would be expected to produce the same genetic diversity as in
the population under study”. fge is depending on the source population though. It is the number
of founders drawn from a source population containing the same amount of genetic variation as
the population we study.
While gene diversity (GD; expected heterozygosity), based on MK (GD = 1 – mean MK), is a
more precise way to calculate the quantity of loss of genetic variation Lacy (1995) changed the
formula to (subscripts denote generation):
fge = 0.5 / (1-(GDt / GD0 ))
40
Inbreeding coefficient
The probability that two alleles in a certain locus are ”identical by descent” (equivalent with the
kinship between the individuals parents).
Fi = Σ 0.5n-1 (1+FA)
Fi = inbreeding coefficient for the individual i
FA = inbreeding coefficient for an common ancestor for the individuals parents
n = the number of gene transmissions from parents to offspring
Over generations
Over generations is the mean number of generations from founders to living individuals.
Example: A set of parents with two offspring, all four still alive, gives a mean generation of 0.5
between founders and living descendants with the setting “include founders”. If using the default
setting (not to include founders) gives mean generation, 1.
Illustration:
Including founders: A and B are founders and are in thus 0
generations from founders. C and D are 1 generation from
founders. (0+0+1+1)/4=0.5
Default setting in PMx (not including founders):
C and D gives (1+1)/2=1
One more example (founders included): If A and C in the
pedigree have one offspring the offspring will be 1.5
((1+2)/2) generations from founders. The mean number of
generation will then be (0+0+1+1+1.5)/5=0.7.
Unknown parents in relation to percent known.
Percent known = (known share of mothers pedigree + known share of fathers pedigree) /2
Example: please turn page over
41
ID
1
2
3
4
5
6
7
8
9
10
DAM
WILD
WILD
1
1
3
3
6
6
8
8
SIRE
WILD
WILD
2
UNK
4
5
4
7
5
9
Mean:
% KNOWN
100
100
100
50
75
87.5
68.75
78.125
76.5625
77.34375
81.328125
(100 + 50)/2
(100 + 75)/2
(50 + 87.5)/2
(87.5 + 68.75)/2
(78.125+75)/2
(78.125 + 76.5625)/2
If every animal in a pedigree has known ancestors (starts with “WILD”) the Founder
contribution will sum up as a hundred percent. If many animals have unknown ancestry
(“UNK”) the inbreeding will be relatively low.
42
APPENDIX 2 – INBREEDING DISTRIBUTION, SCHILLER HOUND
Example of the distribution of inbreeding coefficients (F) for a dog breed at three points in time
(1980, 1995, and 2010). Here, the Shiller hound, classified as "healthy" based on insurance data.
F
3000
Number of Individuals
1980
N: 4768
MEAN: 0.044
SD: 0.034
VAR: 0.001
2500
2000
1500
1000
500
0
Inbreeding Coefficient
F
3000
Number of Individuals
1995
N: 4345
MEAN: 0.060
SD: 0.026
VAR: 0.001
2500
2000
1500
1000
500
0
Inbreeding Coefficient
43
2010
F
Number of Individuals
N: 1777
MEAN: 0.069
SD: 0.022
VAR: 0.001
1800
1600
1400
1200
1000
800
600
400
200
0
Inbreeding Coefficient
44
APPENDIX 3 – INBREEDING DISTRIBUTION, BULLDOG
Example of the distribution of inbreeding coefficients (F) for a dog breed at three points in time
(1980, 1995, and 2010). Here, the bulldog, classified as "unhealthy" based on insurance data.
F
Number of Individuals
1980
N: 235
MEAN: 0.020
SD: 0.041
VAR: 0.002
160
140
120
100
80
60
40
20
0
Inbreeding Coefficient
F
600
Number of Individuals
1995
N: 1053
MEAN: 0.056
SD: 0.056
VAR: 0.003
500
400
300
200
100
0
Inbreeding Coefficient
45
F
Number of Individuals
2010
N: 1484
MEAN: 0.021
SD: 0.036
VAR: 0.001
900
800
700
600
500
400
300
200
100
0
Inbreeding Coefficient
46
APPENDIX 4 – MEAN KINSHIP DISTRIBUTION, SCHILLER HOUND
Example of the distribution of mean kinship (MK) for a dog breed at three points in time (1980,
1995, and 2010). Here, the Shiller hound, classified as "healthy" based on insurance data.
1980
MK
3000
Number of Individuals
N: 4768
MEAN: 0.047
SD: 0.013
VAR: 0.0001
2500
2000
1500
1000
500
0
Mean Kinship
MK
Number of Individuals
1995
N: 4345
MEAN: 0.066
SD: 0.010
VAR: 0.0001
4500
4000
3500
3000
2500
2000
1500
1000
500
0
Mean Kinship
47
MK
2000
Number of Individuals
2010
N: 1777
MEAN: 0.079
SD: 0.007
VAR: 5.087E-05
1500
1000
500
0
Mean Kinship
48
APPENDIX 5 – MEAN KINSHIP DISTRIBUTION, BULLDOG
Example of the distribution of mean kinship (MK) for a dog breed at three points in time (1980,
1995, and 2010). Here, the bulldog, classified as "unhealthy" based on insurance data.
MK
Number of Individuals
1980
N: 235
MEAN: 0.043
SD: 0.013
VAR: 0.0002
180
160
140
120
100
80
60
40
20
0
Mean Kinship
1995
N: 1053
MEAN: 0.056
SD: 0.020
VAR: 0.0004
49
MK
Number of Individuals
2010
N: 1484
MEAN: 0.015
SD: 0.008
VAR: 6.507E-05
1600
1400
1200
1000
800
600
400
200
0
Mean Kinship
50
APPENDIX 6 – AUTOSOMAL RECESSIVE DISEASE IN DOMESTIC DOGS
Searching for autosomal recessive disease on Online Mendelian Inheritance in Animals, OMIA. Faculty of Veterinary Science, University
of Sydney, {January 9 2014}. World Wide Web URL: http://omia.angis.org.au/
Gene symbol
Disease name
Breeds in literature
ABCB1
Multidrug resistance 1
Australian shepherd, border collie, collie, German shepherd, longhaired whippet,
McNab shepherd, mixed-breed, old English sheepdog, Shetland sheepdog, silken
windhound, white Swiss shepherd
ADAM9
Crd3 - PRA
Glen of Imaal terrier
ADAMTS10
Glaucoma, primary open angle
beagle, shiba inu, shih tzu
ADAMTS17
Lens luxation
widespread among breeds and mixed-breeds
ADAMTSL2
Musladin-Lueke syndrome
beagle
AGL
Glycogen storage disease IIIa
(Pompe disease)
curly-coated retriever
AMHR2
Persistent Mullerian Duct
Syndrome
basset hound, miniature schnauzer
AMN
Intestinal cobalamin
malabsorption
Australian shepherd, giant schnauzer, Hungarian komondor
AP3B1
Gray Collie Syndrome
collie
ARSB
Mucopolysaccharidosis VI
miniature pinscher, miniature poodle
ARSG
Neuronal ceroid
lipofuscinosis, 4A
American Staffordshire terrier
ATF2
Neonatal encephalopathy with
seizures
standard poodle
ATP13A2
Neuronal ceroid
lipofuscinosis, 12
Tibetan terrier
BCAN
Episodic falling
cavalier King Charles spaniel
51
BEST1
Multifocal retinopathy 1
American bulldog, Australian shepherd, bullmastiff, dogue de Bordeaux, English
bulldog, English mastiff, great Pyrenees, Italian cane corso, perro de Presa Canario
BEST1
Multifocal retinopathy 2
coton de Tuléar
BEST1
Multifocal retinopathy 3
Lapponian herder
BIN1
Myopathy
great Dane
C17H2orf71
Rod-cone dysplasia 4
Gordon setter, Irish setter
C3
C3 deficiency
Brittany spaniel
CCDC39
Primary ciliary dyskinesia
old English sheepdogs, Staffordshire bull terrier, Newfoundland dogs, English
springer spaniel, bichon frisé, chow chow, Dalmatian, old English sheep dog
CCDC66
Generalized PRA
schapendoes
CHAT
Myasthenic syndrome,
congenital
old Danish pointer
CLCN1
Myotonia
Australian cattle dog, chow chow, great Dane, miniature schnauzer, Staffordshire bull
terrier
CLN5
Neuronal ceroid
lipofuscinosis, 5
border collie
CLN6
Neuronal ceroid
lipofuscinosis, 6
Australian shepherd
CLN8
Neuronal ceroid
lipofuscinosis, 8
English setter
CNGB1
PRA
Papillon
CNGB3
cone degeneration
Alaskan malamute, Alaskan sled dog, miniature Australian shepherd, Siberian husky,
German shorthair pointer
COL11A2
Skeletal dysplasia 2
Labrador retriever
COL4A4
Nephropathy
English cocker spaniel, English springer spaniel, Pembroke Welsh corgi
52
COL7A1
Epidermolysis bullosa,
dystrophic
golden retriever
COL9A2
Oculoskeletal dysplasia, 2
Samoyed
COL9A3
Oculoskeletal dysplasia, 1
Labrador retriever
COMMD1
Wilson disease
Bedlington terrier
CTSD
Neuronal ceroid
lipofuscinosis, 10
American bulldog
CUBN
Intestinal cobalamin
malabsorption
beagle, border collie
DNM1
Exercise-induced collapse
Boykin spaniel, Chesapeake bay retriever, curly-coated retriever, Labrador retriever
ENAM
Enamel hypoplasia
greyhound, standard poodle
F7
Factor VII deficiency
beagle
FAM83H
Dry eye curly coat syndrome
cavalier King Charles spaniel
FERMT3
Canine leukocyte adhesion
deficiency, type III
Irish red and white Setter, Irish setter
FNIP2
Hypomyelination of the
central nervous system
chow chow, Weimaraner
FUCA1
Fucosidosis (neurological
degeneration)
English springer spaniel
G6PC
Glycogen storage disease Ia
(Pompe disease)
Maltese terrier
GALC
Krabbe disease
cairn terrier, west highland white terrier
GLB1
proportional dwarfism
Alaskan husky, beagle, English springer spaniel, Portugese water dog, shiba
GRM1
Bandera's neonatal ataxia
(Ataxia, cerebellar)
coton de Tuléar
GUSB
Mucopolysaccharidosis VII
Brazilian terrier, German shepherd
53
HCRTR2
Narcolepsy
Afghan hound, Airedale terrier, beagle, Welsh corgi, dachshund, Doberman pinscher,
giant schnauzer, Irish setter, Labrador retriever, Alaskan malamute, miniature poodle,
Rottweiler, saint Bernard dog, springer spaniel, standard poodle, wirehaired griffon
HEXA
Gangliosidosis, GM2, type I
Japanese chin dog
HEXB
Gangliosidosis, GM2, type II
golden retriever, toy poodle
IDUA
Mucopolysaccharidosis I
Plott hound
IQCB1
Crd2 - PRA
American pit bull terrier
ITGA10
Chondrodysplasia,
disproportionate short-limbed
Karelian bear dog, Norwegian elkhound
ITGB2
Canine leukocyte adhesion
deficiency, type I
Irish setter and mixed-/crossbreed
KLKB1
Prekallikrein deficiency
shar pei
KRT10
Epidermolytic hyperkeratosis
Norfolk terrier
L2HGDH
L-2-hydroxyglutaric aciduria
Staffordshire bull terrier, west highland terrier, Yorkshire terrier
LAMA3
Epidermolysis bullosa,
junctionalis
German pointer
LGI2
remitting focal epilepsy
lagotto Romagnolo
LHX3
Dwarfism, pituitary
German shepherd
LOC607355
Oxalosis I
coton de Tuléar, Tibetan spaniel
MFN2
Neuroaxonal dystrophy
giant schnauzer
MLPH
Alopecia (hair loss)
German pinsher, Dobermann pinscher, Rhodesian ridgeback, whippet, Australian
shepherd, briard, bolonka swetna, Frensch bulldog, great dane, Chihuahua, beagle,
large Münsterlander, Newfoundland, Hovawart, miniatyre pinscher, border collie,
Slovakian rough hair pointer, American Staffordshire terrier, Italian greyhound, Jack
Russel terrier
NAGLU
Mucopolysaccharidosis IIIb
schipperke dog
54
NDRG1
Polyneuropathy
Alaskan malamute, border collie, Dalmatian, golden retriever, greyhound, miniature
schnauzer
NHEJ1
Collie eye anomaly
Australian shepherd, border collie, Boykin spaniel, Lancashire heeler, longhaired
whippet, Nova Scotia duck tolling retriever, rough collie, shetland sheepdog, Silken
windhound, smooth collie
NHLRC1
Myoclonus epilepsy of Lafora
miniature wirehaired dachshund, basset hound
NKX2-8
Spinal dysraphism
Weimaraner
NPHP4
Crd - PRA
standard wire-haired dachshund
P2RY12
Bleeding disorder
greater Swiss mountain dog
PDC
Photoreceptor dysplasia
miniature schnauzer
PDE6A
Rod-cone dysplasia 3
Cardigan Welsh corgi
PDE6B
Crd1 - PRA
American staffordshire terrier
PDE6B
Rod-cone dysplasia 1
Irish setter
PDE6B
Rod-cone dysplasia 1a
sloughi
PDK4
Dilated cardiomyopathy
German boxer, Doberman pinscher, Irish wolfhound
PDP1
Exercise intolerance
clumber spaniel, Sussex spaniel
PFKM
Glycogen storage disease VII
(Pompe disease)
American cocker spaniel, English cocker spaniel, Wachtelhund, whippet
PHC
Cataract
Australian shepherd, Boston terrier, Staffordshire bull terrier
PKLR
Pyruvate kinase deficiency
basenji, beagle, cairn terrier, west highland white terrier
PKP1
Ectodermal dysplasia/skin
fragility syndrome
Chesapeake bay retriever
PNPLA1
Ichthyosis
Golden retriever
PPT1
Neuronal ceroid
lipofuscinosis, 1
dachshund
55
PRCD
PRCD
American cocker spaniel, Australian cattle dog, Australian shepherd, Australian
stumpy tail cattle dog, Chesapeake bay retriever, Chinese crested dog, English cocker
spaniel, Entlebucher mountain dog, Finnish lapphund, golden retriever, Karelian bear
dog, Kuvasz, Labrador retriever, Lapponian herder, miniature poodle, Norwegian
elkhound, Nova Scotia duck tolling retriever, Portugese water dog, Spanish water dog,
Swedish lapphund, toy poodle, Yorkshire terrier
PRKDC
Combined immunodeficiency
disease
Jack Russell terriers
PTPLA
Myopathy, centronuclear
Labrador retriever
RD3
Rod-cone dysplasia 2
collie
RPE65
congenital stationary night
blindness
briard
RPGRIP1
Crd4 - PRA
miniature long-haired dachsund
SAG
PRA
basenji
SCA
Spinocerebellar ataxia
Parson Russell terrier
SEL1L
Ataxia, cerebellar
Finnish hound
SERPINH1
Osteogenesis imperfecta
dachshund
SGSH
Mucopolysaccharidosis IIIa
wire-haired dachshund
SLC13A1
Osteochondrodysplasia
miniature poodle
SLC2A9
Urolithiasis
dalmatians, cavalier King Charles spaniels, American stafforshire terrier, Australian
shepherd, German shepherd, giant schnauzer, Parson russel terrier, Labrador retriever,
large Münsterlander, Pomeranian, South African boerboel, Weimaraner, English
bulldog, black Russian terrier
SLC3A1
Cystinuria, type I - A
Labrador retriever, Landseer, Newfoundland dog
SLC4A3
PRA 1
golden retriever
SLC6A5
Hyperekplexia (Startle
disease)
Irish wolfhound, Labrador retriever
56
SOD1
Degenerative myelopathy
American Eskimo dog, Bernese mountain dog, German boxer, Cardigan Welsh corgi,
Chesapeake bay retriever, German shepherd, Golden retriever, Kerry blue terrier,
miniature poodle, Pembroke Welsh corgi, pug, Rhodesian ridgeback, Siberian husky,
soft coated wheaten terrier, standard poodle, wirehaired fox terrier
SPTBN2
neonatal cerebellar cortical
degeneration (NCCD)
beagle, kelpie
STK38L
Early retinal degeneration
Norwegian Elkhound
SUV39H2
Nasal parakeratosis
Labrador retriever
TGM1
Ichthyosis
Jack Russel terrier
TPO
Hypothyroidism
rat terrier, Spanish water dog, Tenterfield terrier, toy fox terrier
TPP1
Neuronal ceroid
lipofuscinosis, 2
dachshund
VDR
Vitamin D-deficiency rickets,
type II
Pomeranian
VPS13B
Trapped Neutrophil Syndrome
border collie
-
zinc deficiency
bullterrier
-
Ataxia, cerebellar
Malinois
-
Black hair follicle dysplasia
large Münsterlander , New Zealand huntaway dog, Gordon setter, mixed-breed dog,
bearded collie, border collie, saluki, Jack Russel terrier, mongrel dog
-
Brachydactyly (two-toed)
-
-
Cerebellar cortical atrophy
papillon, Portuguese podenco, Labarador retriever
-
Chondrodysplasia,
disproportionate short-limbed
Labrador retriever
-
Cleft lip and palate
Pyrenees shepherd, German boxer
-
Coloboma
Australian shepherd
57
-
Craniomandibular osteopathy
West highland white terrier, pit bull terrier, Akita, bullmastiff, Pyrenean mountain
dog, Shetland sheepdog, Labrador retriever
-
Cricopharyngeal dysfunction
Golden retrievers
-
Deficiency of cytosolic
arylamine N-acetylation
-
-
Dwarfism, hypochondroplastic
Irish setter
-
Encephalomyelopathy and
polyneuropathy
Alaskan husky
-
Epilepsy
Belgian shepherd, collie, Finnish spitz
-
Exfoliative cutaneous lupus
erythematosus
German shorthair pointer, mixed breed
-
Gangliosidosis, GM2, generic
German shorthair pointer, English setter, mixed-breed, Golden retriever
-
Gangliosidosis, GM2A
Japanese spaniel
-
Gaucher disease, type I
Sydney silky dog
-
Glomerulonephropathy
French mastiff (Bordeaux) dogs, Bullmastiff, beagle, Bernese mountain dog
-
Glossopharyngeal defect
(lethal)
-
-
Gluten-sensitive enteropathy
Irish setter
-
Goniodysplasia, mesodermal
Siberian husky, bouvier des Flandres
-
Kartagener syndrome
Staffordshire bull terrier, dachshund, Newfoundland dog, English cocker spaniel,
English springer spaniel, bichon frisé, chow chow
-
Leukoencephalomyelopathy
Rottweiler
-
Multiple system degeneration
Chinese crested, Kerry blue terrier
-
Nephritis, autosomal recessive
English cocker spaniel
-
Neurological syndrome
(lethal)
Gordon setter
58
-
Neuronal ceroid lipofuscinosis
Rottweiler, Kerry blue terrier, Jack Russell terrier, papillion, English setter, border
collie, Golden retriever, Australian cattle dog, saluki, Chihuahua, Tibetian terrier,
dachshund, miniature schnauzer, Australian shepherd, Polish owczarek nizinny
(PON), American bulldog, border collie, Labrador retriever, cocker spaniel
-
Canine Scott syndrome
German shepherd
-
Retinal dysplasia
miniature schnauzer
-
Rod dysplasia
Norwegian elkhound
-
Subaortic stenosis
Newfoundland, dogue de Bordeaux
-
Canine tricuspid valve
malformation
dogue de Bordeaux, Labrador retriever
-
Xanthinuria, generic
cavalier king Charles spaniel, dachshund
-
XX testicular DSD (Disorder
of Sexual Development)
cocker spaniel, mixed-breed Pit bull, mongrel dog, French bulldog, Bernese mountain
dog, pug, Podenco, beagle, Jack Russell terrier, basset hound, Norwegian elkhounds,
German shorthair pointer
59
APPENDIX 7 – CHAMPIONSHIPS
Four types of “Championships” exists in SKC’s records: Show Championships, Working
Championships, Combined Championships (several titels adds up to one) and Internationell
prüfungsordnung titles.
In IPO, the highest title is the ... III:
Number
795
88
420
510
797
Abbreviation
SCHHIII SG
BHPIII
VPGIII
IPOIII
SCHHIII
Full text
SKYDDSHUND III SEHR GUT
BRUKSHUNDPROV III
DETSAMMA SOM SKYDDSHUND III
INTERNATIONELL PRüFUNGSORDNUNG III
SKYDDSHUND III
Show Championships:
Number
482
491
773
794
889
980
983
7
53
54
63
148
164
165
184
185
194
202
223
265
270
281
291
297
Abbreviation
UY CH
BH CH
LU JCH
KBH V-06&NO V-05-08
UCH
FISPCH
BK CH
NO U(DV)CH
SL CH
NORD U(DV)CH
ZW CH
IE SHCH
CU CH
SK CH
LV CH
LT CH
CR CH
GR CH
DK U(S)CH
CL CH
GI CH
UA CH
CO CH
PANAMCH
Full text
URUGUAY CHAMPION
BOSNIEN-HERZEGOVINE CHAMPION
LUXEMBURGSK JUNIORCHAMPION
UTSTÄLLNINGSCHAMPION ANV EJ!
FINSK SPÅRCHAMPION
NORSK UTSTÄLLNINGS(DREVPROV&VILTSPÅR)CHAMPION
SLOVENSK CHAMPION
NORDISK UTSTÄLLNINGS(DREVPROV&VILTSPÅR)CHAMPION
ZIMBABWISK CHAMPION
IRLÄNDSK SHOW CHAMPION
CUBANSK CHAMPION
SLOVAKISK CHAMPION
LETTISK CHAMPION
LITAUISK CHAMPION
COSTA RICA CHAMPION
GREKISK CHAMPION
DANSK CHAMPION /SPÅR/
CHILENSK CHAMPION
GIBRALTISK CHAMPION
UKRAINSK CHAMPION
COLOMBIA CHAMPION
PANAMERIKANSK CHAMPION
60
329
360
372
388
389
400
405
421
437
455
456
457
460
464
493
501
556
559
560
564
586
610
632
676
691
694
709
741
745
790
791
800
801
802
803
804
BY CH
SE U(S)CH
GE CH
MA CH
MD CH
SE U(U)CH
BG CH
CZ CH
PH CH
MY CH
DK CH(U)
MT CH
TH CH
CY CH
HK CH
CHIB
IS CH
KZ CH
UZ CH
GT CH
AZ CH
HR CH
NO U(GV)CH
MK CH
ME CH
RS CH
EE CH
PR CH
SM CH
C.I.B
C.I.E
SE UCH
SE U(D)CH
SE U(G)CH
SE U(KV)CH
SE U(V)CH
806
807
808
SE U(GKV)CH
SE U(GV)CH
SE U(GK)CH
809
SE U(DGV)CH
VITRYSK CHAMPION
SVENSK UTSTÄLLNINGS(SKOGSPROV)CHAMPION
GEORGISK CHAMPION
MAROCKANSK CHAMPION
MOLDAVISK CHAMPION
SVENSK UTSTÄLLNINGSCHAMPION UTAN JAKTPROVSMERIT
BULGARISK CHAMPION
TJEKISK CHAMPION
FILIPPINSK CHAMPION
MALAYSISK CHAMPION
DANSKT UTSTÄLLNINGSCHAMPIONAT UTAN JAKTMERIT
MALTESISK CHAMPION
THAILÄNDSK CHAMPION
CYPRIOTISK CHAMPION
HONG KONG CHAMPION
INTERNATIONELL UTSTÄLLNINGSCHAMPION
ISLÄNDSK CHAMPION
KAZAKSTANSK CHAMPION
UZBEKISK CHAMPION
GUATEMALANSK CHAMPION
AZERBAIJAN UTSTÄLLNINGS CHAMPION
KROATISK CHAMPION
NORSK UTSTÄLLNINGS(GRYT-&VILTSPÅRPROV)CHAMPION
MAKEDONIEN CHAMPION
MONTENEGRISK CHAMPION
SERBISK CHAMPION
ESTNISK CHAMPION
PUERTO RICO CHAMPION
SAN MARINO CHAMPION
INTERNATIONAL BEAUTY CHAMPION
INTERNATIONAL SHOW CHAMPION
SVENSK UTSTÄLLNINGSCHAMPION
SVENSK UTSTÄLLNINGS(DREVPROV)CHAMPION
SVENSK UTSTÄLLNINGS(GRYTPROV)CHAMPION
SVENSK UTSTÄLLNINGS(KARAKTÄR&VILTSPÅR)CHAMPION
SVENSK UTSTÄLLNINGS(VILTSPÅR)CHAMPION
SVENSK
UTSTÄLLNINGS(KARAKTÄR&VILTSPÅR&GRYTPROV)CHAMPION
SVENSK UTSTÄLLNINGS(GRYTPROV&VILTSPÅR)CHAMPION
SVENSK UTSTÄLLNINGS(KARAKTÄR&GRYTPROV)CHAMPION
SVENSK UTSTÄLLNINGS(GRYT&DREVPROV&VILTSPÅR)
CHAMPION
61
810
SE U(DG)CH
811
812
813
821
822
823
824
825
829
830
831
832
836
863
874
875
880
881
885
892
893
911
917
920
921
922
923
925
926
935
940
941
SE U(DGKV)CH
SE U(RÄV)CH
SE U(DV)CH
FI U(V)CH
FI U(KV)CH
FI U(G)CH
FI U(D)CH
FI U(SP)CH
DK U(G)CH
DK UCH
NO UCH
FI UCH
CH
RU CH
BR CH
VDH CH
NORD UCH
INT UCH
PT CH
NZ CH
YU CH
SG CH
CH CH
NO U(V)CH
NO U(G)CH
NO U(KV)CH
NO U(D)CH
NO U(DG)CH
DDR CH
RO CH
INT U(G)CH
INT U(D)CH
942
INT U(KV)CH
943
944
945
948
950
INT U(GKV)CH
INT U(V)CH
INT U(DG)CH
ES CH
NORD U(G)CH
SVENSK UTSTÄLLNINGS(DREV&GRYTPROV)CHAMPION
SVENSK
UTSTÄLLNINGS(KARAKTÄR&VILTSPÅR&DREV&GRYTPROV)
CHAMPION
SVENSK UTSTÄLLNINGS(RÄV)CHAMPION
SVENSK UTSTÄLLNINGS(VILTSPÅR&DREVPROV)CHAMPION
FINSK UTSTÄLLNINGS(VILTSPÅR)CHAMPION
FINSK UTSTÄLLNINGS(KARAKTÄR&VILTSPÅR)CHAMPION
FINSK UTSTÄLLNINGS(GRYTPROV)CHAMPION
FINSK UTSTÄLLNINGS(DREVPROV)CHAMPION
FINSK UTSTÄLLNINGS(SPÅRHUND)CHAMPION
DANSK UTSTÄLLNINGS(GRYTPROV)CHAMPION
DANSK CHAMPION
NORSK UTSTÄLLNINGSCHAMPION
FINSK CHAMPION
CHAMPION
RYSK CHAMPION
BRASILIANSK CHAMPION
VDH CHAMPION
NORDISK UTSTÄLLNINGSCHAMPION
INTERNATIONELL UTSTÄLLNINGSCHAMPION
PORTUGISISK CHAMPION
NYA ZEELÄNDSK CHAMPION
JUGOSLAVISK CHAMPION
SINGAPORE CHAMPION
SCHWEIZISK CHAMPION
NORSK UTSTÄLLNINGS(VILTSPÅR)CHAMPION
NORSK UTSTÄLLNINGS(GRYTPROV)CHAMPION
NORSK UTSTÄLLNINGS(KARAKTÄR&VILTSPÅR)CHAMPION
NORSK UTSTÄLLNING(DREVPROV)CHAMPION
NORSK UTSTÄLLNINGS(DREV&GRYTPROV)CHAMPION
ÖSTTYSK CHAMPION
RUMÄNSK CHAMPION
INTERNATIONELL UTSTÄLLNINGS(GRYTPROV)CHAMPION
INTERNATIONELL UTSTÄLLNINGS(DREVPROV)CHAMPION
INTERNATIONELL
UTSTÄLLNINGS(KARAKTÄR&VILTSPÅR)CHAMPION
INTERNATIONELL
UTSTÄLLNINGS(KARAKTÄR&GRYTPROV&VILTSPÅR)CHAMPION
INTERNATIONELL UTSTÄLLNINGS(VILTSPÅR)CHAMPION
INTERNATIONELL UTSTÄLLNINGS(DREV&GRYTPROV)CHAMPION
SPANSK CHAMPION
NORDISK UTSTÄLLNINGS(GRYTPROV)CHAMPION
62
951
952
953
NORD U(D)CH
NORD U(KV)CH
NORD U(V)CH
954
955
958
959
960
961
962
963
964
965
966
967
969
970
971
972
973
975
976
977
988
989
992
993
994
995
996
997
999
1101
1103
1240
1241
NORD U(GKV)CH
NORD U(DG)CH
AR CH
PE CH
IE CH
PL CH
BM CH
LU CH
BE CH
MC CH
AU CH
GB SHCH
MX CH
FR CH
JP GCH
CSSP CH
IT CH
BR CH
IL CH
HU CH
AT CH
ZA CH
GB CH
US CH
CA CH
DE CH
NL CH
JP CH
EA CH
IS SH CH
C.E.C
TR CH
DK CH(+J)
NORDISK UTSTÄLLNINGS(DREVPROV)CHAMPION
NORDISK UTSTÄLLNINGS(KARAKTÄR&VILTSPÅR)CHAMPION
NORDISK UTSTÄLLNINGS(VILTSPÅR)CHAMPION
NORDISK UTSTÄLLNINGS(KARAKTÄR&
GRYTPROV&VILTSPÅR)CHAMPION
NORDISK UTSTÄLLNINGS(DREV&GRYTPROV)CHAMPION
ARGENTINSK CHAMPION
PERUANSK CHAMPION
IRLÄNDSK CHAMPION
POLSK CHAMPION
BERMUDA CHAMPION
LUXEMBURGSK CHAMPION
BELGISK CHAMPION
MONEGASKISK CHAMPION
AUSTRALISK CHAMPION
GREAT BRITAIN SHOW CHAMPION
MEXIKANSK CHAMPION
FRANSK CHAMPION
JAPANSK GRAND CHAMPION
TJECKISK CHAMPION
ITALIENSK CHAMPION
BRASILIANSK CHAMPION
ISRAELISK CHAMPION
UNGERSK CHAMPION
ÖSTERRIKISK CHAMPION
SYDAFRIKANSK CHAMPION
GREAT BRITAIN CHAMPION
AMERIKANSK CHAMPION
KANADENSISK CHAMPION
TYSK CHAMPION
NEDERLÄNDSK CHAMPION
JAPANSK CHAMPION
ÖSTAFRIKANSK CHAMPION
ISLÄNDSK UTSTÄLLNINGSCHAMPION
CENTENARY SHOWS CHAMPION
TURKISK CHAMPION
DANSK CHAMPION MED JAKTPROVSMERIT
Working Championships:
Number
290
759
Abbreviation
SE J(B)CH
NJ(+K)CH
Full text
SVENSK JAKTPROVS(BANDHUND)CHAMPION (SÄK)
GÄLLER STÅENDE FÅGELHUNDAR
63
4
56
57
59
66
67
70
100
138
146
161
162
167
169
183
196
208
224
226
231
263
264
298
324
326
336
340
341
350
363
366
369
371
373
376
379
380
385
386
387
404
BE JCH
SE (VALL-F)CH
SE (VALL-N)CH
SE RPCH
DE J(DG)CH
SE SPCH
SE SÖCH
FI SPCH
SE SPBCH
DE LCCH
SE VCH
FI AGCH
DK SCH
NL JCH
NORD VCH
DK VCH
DK L(ELIT)CH
NORD AGCH
FI J(RÄV)CH
AT JCH
DK J(D)CH
EE VCH
FI LCCH
SE LCCH
DK BRCH
EE LCH
IT LCH
INT AGCH
SE J(LE)CH
SE (AP)CH
US LCCH
INT LCCH
DK SPCH
SE AG(HOPP)CH
NO J(SCH)CH
FI AG(HOPP)CH
SE J(LÖ)CH
SE J(GS)CH
SE J(GF)CH
NORD J(GS)CH
NO LCCH
411
SE B(IPO/BHP)CH
BELGISK JAKTPROVSCHAMPION
SVENSK VALLHUNDS(FÅR)CHAMPION
SVENSK VALLHUNDS(NÖT)CHAMPION
SVENSKT RAPPORTPROVSCHAMPIONAT
TYSK JAKTPROVS(DREV&GRYT)CHAMPION
SVENSKT SPÅRPROVSCHAMPIONAT
SVENSKT SÖKPROVSCHAMPIONAT
FINSK SPÅRCHAMPION
SVENSK SPÅRPROVSCHAMPION BLODHUND
TYSK LURE COURSING CHAMPION
SVENSK VILTSPÅRPROVSCHAMPION
FINSK AGILITYCHAMPION
DANSK SPÅRCHAMPION
NEDERLÄNDSK JAKTPROVSCHAMPION
NORDISK VILTSPÅRPROVSCHAMPION
DANSK VILTSPÅRCHAMPION
DANSK ELITLYDNADSCHAMPION
NORDISK AGILITYCHAMPION
FINSK JAKTPROVS(RÄV)CHAMPION
ÖSTERRIKISK JAKTCHAMPION
DANSK JAKTPROVS(DREV)CHAMPION
ESTNISK SPÅRCHAMPION
FINSK LURE COURSING CHAMPION
SVENSK LURE COURSING CHAMPION
DANSK BRUGSCHAMPION
ESTNISKT LYDNADSCHAMPIONAT
ITALIENSK LYDNADSCHAMPION
INTERNATIONELL AGILITY CHAMPION
SVENSK JAKTPROVS(LEDHUND)CHAMPION
SVENSK ARBETSPROVSCHAMPION
AMERIKANSK LURE COURSING CHAMPION
INTERNATIONELL LURE COURSING CHAMPION
DANSK SPRINGCHAMPION
SVENSK AGILITYCHAMPION (HOPP)
NORSK JAKTPROVSCHAMPION SCHWEISSHUNDPRÖVE (VILTSPÅR)
FINSK AGILITYCHAMPION (HOPP)
SVENSK JAKTPROVS(LÖSHUND)CHAMPION
SVENSK JAKTPROVSCHAMPION /GRYT, SPRÄNGARE/
SVENSK JAKTPROVSCHAMPION /GRYT, FÖRLIGGARE/
NORDISK JAKTPROVSCHAMPION GRYT, SPRÄNGARE
NORSK LURE COURSING CHAMPION
SVENSK BRUKSPROVSCHAMPION (INT PRÜFINGSORDNUNG &
BRUKSHUNDPROV)
64
422
434
SE J(S)CH
IT AGCH
447
448
450
466
478
495
518
565
570
595
596
597
598
608
620
631
633
636
637
639
640
643
660
661
697
699
705
707
710
729
742
746
776
783
792
838
840
841
843
845
SE J(GFGS)CH
NORD J(LÖ)CH
SE J(J)CH
NO (VP)CH
DK J(G)CH
AU FTCH
EE LCCH
LT JCH
SE J(A)CH
DK AGCH
DK BCH(G)
DK BCH(D)
DK BCH(S)
DE JCH
HR JCH
IT JCH
FI VCH
NO J(B)CH
NO J(L)CH
INT LCH
SE (VP)CH
NO TCH
NORD LCCH
DK U(D)CH
LV JCH
CA FTCH
SE (POLAR)CH
HU JCH
NO AGCH
NO AG(HOPP)CH
SE AGCH
NO VCH
NZ FTCH
NO L(ELIT)CH
C.I.T
DK LCH
INT J(G)CH
INT J(D)CH
FR JCH
SE L(ELIT)CH
SVENSK JAKTPROVSCHAMPION /SKOG/
ITALIENSK AGILITYCHAMPION
SVENSK JAKTPROVSCHAMPION /GRYT; SPRÄNGARE &
FÖRLIGGARE/
NORDISK JAKT(LÖSHUND)CHAMPION
SVENSK JAKTPROVSCHAMPION UTAN UTSTÄLLNINGSMERIT
NORSK VATTENPROVSCHAMPION
DANSK JAKTPROVS(GRYT)CHAMPION
AUSTRALISK FIELD TRIAL CHAMPION
ESTNISK LURE CUORSING CHAMPION
LITAUISK JAKT CHAMPION
SVENSKT JAKTPROVSCHAMPIONAT A-PROV
DANSK AGILITYCHAMPION
DANSK BRUKSPROVSCHAMPION (GRYTPROV)
DANSK BRUKSPROVSCHAMPION (DREVPROV)
DANSK BRUKSPROVSCHAMPION (SPÅRPROV)
TYSK JAKTPROVSCHAMPION
KROATISK JAKTCHAMPION
ITALIENSK JAKTPROVSCHAMPION
FINSK VILTSPÅRPROVSCHAMPION
NORSK JAKTPROVS(BANDHUND)CHAMPION
NORSK JAKTPROVS(LÖSHUND)CHAMPION
INTERNATIONELL LYDNADSCHAMPION
SVENSK VATTENPROVSCHAMPION
NORSK TREKKEHUNDSCHAMPION
NORDISK LURE COURSING CHAMPION
DANSK UTSTÄLLNINGS(DREVPROV)CHAMPION
LETTISK JAKTCHAMPION
KANADENSISK FIELD TRIAL CHAMPION
SVENSK (POLARHUNDS) CHAMPION
UNGERSK JAKTPROVSCHAMPION
NORSK AGILITYCHAMPION
NORSK AGILITY HOPP CHAMPION
SVENSK AGILITYCHAMPION
NORSK VILTSPÅRCHAMPION
NYA ZEELÄNDSK FIELD TRIAL CHAMPION
NORSK LYDNADS(ELIT)CHAMPION
INTERNATIONAL WORKING CHAMPION
DANSK LYDNADSCHAMPION
INTERNATIONELL JAKTPROVS(GRYT)CHAMPION
INTERNATIONELL JAKTPROVS(DREV)CHAMPION
FRANSK JAKTPROVSCHAMPION
SVENSK LYDNADS(ELIT)CHAMPION
65
850
851
852
859
860
861
862
864
865
866
867
868
869
870
877
879
888
890
894
895
896
898
899
900
901
902
903
904
905
906
907
908
909
910
919
927
928
930
931
932
933
968
NORD J(G)CH
NORD J(D)CH
NORD J(V)CH
NO J(V)CH
NO JCH
NO J(G)CH
NO J(D)CH
RU JCH
FI JCH
FI J(D)CH
FI J(G)CH
FI J(V)CH
DK U(V)CH
DK JCH
SE J(V)CH
IT LCCH
BCH
SE LCH
EE JCH
SE J(DG)CH
SE J(DGV)CH
SE J(RÄV)CH
SE J(DV)CH
SE JCH
SE J(D)CH
SE J(G)CH
NORD JCH
INT JCH
SE BCH
SE J(KV)CH
SE (DRAG)CH
SE (VALLH)CH
NO LCH
NORD LCH
DK LCCH
US FTCH
IE FTCH
DK BCH
NO BCH
FI BCH
FR BCH
GB FTCH
NORDISK JAKTPROVS(GRYT)CHAMPION
NORDISK JAKTPROVS(DREV)CHAMPION
NORDISK JAKTPROVS(VILTSPÅR)CHAMPION
NORSK JAKTPROVS(VILTSPÅR)CHAMPION
NORSK JAKTPROVSCHAMPION
NORSK JAKTPROVS(GRYT)CHAMPION
NORSK JAKTPROVS(DREV)CHAMPION
RYSK JAKTPROVSCHAMPION
FINSK JAKTPROVSCHAMPION
FINSK JAKTPROVS(DREV)CHAMPION
FINSK JAKTPROVS(GRYT)CHAMPION
FINSK JAKTPROVS(VILTSPÅR)CHAMPION
DANSK UTSTÄLLNINGS(VILTSPÅR)CHAMPION
DANSK JAKTPROVSCHAMPION
SVENSK JAKTPROVS(VILTSPÅR)CHAMPION
ITALIENSK LURE COURSING CHAMPION
BRUKSPROVSCHAMPION
SVENSK LYDNADSCHAMPION
ESTNISK JAKT CHAMPION
SVENSK JAKTPROVS(DREV&GRYT)CHAMPION
SVENSK JAKTPROVS(GRYT&DREV&VILTSPÅR)CHAMPION
SVENSK JAKTPROVS(RÄV)CHAMPION
SVENSK JAKTPROVS(DREV&VILTSPÅR)CHAMPION
SVENSK JAKTPROVSCHAMPION
SVENSK JAKTPROVS(DREV)CHAMPION
SVENSK JAKTPROVS(GRYT)CHAMPION
NORDISK JAKTPROVSCHAMPION
INTERNATIONELL JAKTPROVSCHAMPION
SVENSK BRUKSPROVSCHAMPION
SVENSK JAKTPROVS(KARAKTÄR&VILTSPÅR)CHAMPION
SVENSK (DRAGPROVS)CHAMPION
SVENSK (VALLHUNDS)CHAMPION
NORSK LYDNADSCHAMPION
NORDISK LYDNADSCHAMPION
DANSK LURE LOURSING CHAMPION
AMERIKANSK FIELD TRIAL CHAMPION
IRLÄNDSK FIELD TRIAL CHAMPION
DANSK BRUKSPROVSCHAMPION
NORSK BRUKSPROVSCHAMPION
FINSK BRUKSPROVSCHAMPION
FRANSK BRUKSPROVSCHAMPION
GREAT BRITAIN FIELD TRIAL CHAMPION
66
990
991
998
1000
1102
1104
1105
1106
1107
1108
1109
1110
1116
1117
1216
1239
NORD BCH
INT BCH
FI LCH
SE FREECH
FI VPCH
C.I.C
SE J(VLÖ)CH
SE J(T)CH
SE J(FÅ)CH
SE PTRHCH
SE IPO-FH CH
SE RDHCH
SE B(IPO)CH
DK RLCH
FI J(A)CH
C.I.AG
NORDISK BRUKSPROVSCHAMPION
INTERNATIONELL BRUKSPROVSCHAMPION
FINSK LYDNADSCHAMPION
SVENSKT FREESTYLECHAMPIONAT
FINSK VATTENPROVSCHAMPION
INTERNATIONAL RACES CHAMPION
SVENSK JAKTPROVS(VILDSVIN-LÖSHUND)CHAMPION
SVENSK JAKTPROVSCHAMPION TOLLING
SVENSK JAKTPROVSCHAMPION(SKÄLLANDE FÅGELHUNDAR)
SVENSK PATRULLHUNDSCHAMPION
SVENSK IPO-FH CHAMPION
SVENSK RÄDDNINGSHUNDSCHAMPION
SVENSKT BRUKSPROVSCHAMPIONAT IPO
DANSK RALLYLYDNADSCHAMPION
FINSK JAKTPROVSCHAMPIONAT A-PROV
INTERNATIONELL AGILITY CHAMPION
Combined Championships:
Number
Abbreviation
17
19
23
25
INT&NORD&FI U(V)CH
INT&NORD&LU U(D)CH
FI&NL&LU CH
AT&BE&NL&VDH CH
INT&NORD&FI&NL&LU
CH
INT&NORD&LU CH
FI&NO U(G)CH
INT&NORD&LU&NL&PT
CH
FI U&J(G)CH
DK U&J(G)CH
INT&NORD&DK UCH
BE&FR&NL CH
EE&LV CH
NO U&VCH
DE&LU&NL&VDH CH
INT&NORD&NO UCH
FI&EE CH
INT&VDH CH
IPOIII&SCHHIII
FR&MC CH
26
28
30
38
40
41
43
46
48
50
80
81
84
89
91
92
Full text
INTERNATIONELL&NORDISK&FINSK UTSTÄLLNINGS
(VILTSPÅR)CHAMPION
INTERNATIONELL & NORDISK & LUXEMBURGSK CHAMPION
FINSK & NEDERLÄNDSK & LUXEMBURGSK CHAMPION
NEDERLÄNDSK & BELGISK & ÖSTERRIKISK & VDH CHAMPION
INTERNATIONELL & NORDISK & FINSK &
NEDERLÄNDSK & LUXEMBURGSK CHAMPION
INTERNATIONELL & NORDISK & LUXEMBURGSK CHAMPION
NORSK & FINSK UTSTÄLLNINGS(GRYTPROV)CHAMPION
INT & NORDISK & PORTUGISISK & LUXEMBURGSK
& NEDERLÄNDSK CHAMPION
FINSK UTSTÄLLNINGS & JAKTPROVS(GRYT)CHAMPION
DANSK UTSTÄLLNINGS & JAKTPROVS(GRYT)CHAMPION
INTERNATIONELL & NORDISK & DANSK CHAMPION
NEDERLÄNDSK & BELGISK & FRANSK CHAMPION
ESTNISK & LETTISK CHAMPION
NORSK UTSTÄLLNINGS & VILTSPÅRPROVSCHAMPION
NEDERLÄNDSK & LUXEMBURGSK & VDH & TYSK CHAMPION
INTERNATIONELL & NORDISK & NORSK CHAMPION
FINSK & ESTNISK CHAMPION
INTERNATIONELL & VDH CHAMPION
INTERNATIONELL PRüFUNGSORDNUNG III & SKYDDSHUND III
FRANSK & MONEGASKISK CHAMPION
67
93
DK&PL UCH
95
121
122
125
129
131
132
133
134
INT&NORD&FI&LU UCH
INT&DK&FI&EE&LU&NL
CH
INT&DE&PT CH
SE&NO JCH
INT&NORD&FI UCH
NORD&DK UCH
INT&SE&DK UCH
BE&FR CH
INT&DE&NL&VDH CH
INT&IT CH
CH&MC CH
BE&CH&FR&IT&LU&MC
CH
DK&DE UCH
AT&FR&NL CH
AT&NL CH
DK&BE&NL CH
AU&FI&PT UCH
DK&DE&LU&NL CH
PE&US CH
147
149
156
171
173
177
180
181
182
186
187
188
189
193
201
207
212
213
SE J&V CH
NORD&FI UCH
FI&EE&NL UCH
MX&PL CH
AT&CH CH
AU&NZ CH
IT&YU CH
SL&HR CH
SE&DK&US& UCH
DK&VDH CH
NORD&NO UCH
SE&DK&FI UCH
AU&SI CH
BE&LU CH
SE J(D,GS)CH
CH&US CH
SE&DK&ES&NL UCH
SE J(G)CH&FI JCH
216
NORD LCH&SE BCH
96
98
102
104
106
107
111
112
116
120
POLSK & DANSK CHAMPION
INTERNATIONELL & NORDISK & LUXEMBURGSK &
FINSK CHAMPION
INTERNATIONELL&FINSK&DANSK&LUXEMBURGSK&
NEDERLÄNDSK&ESTNISK CHAMPION
INTERNATIONELL & TYSK & PORTUGISISK CHAMPION
SVENSK & NORSK JAKTPROVSCHAMPION
INTERNATIONELL & NORDISK & FINSK CHAMPION
NORDISK & DANSK CHAMPION
INTERNATIONELL & DANSK & SVENSK CHAMPION
BELGISK & FRANSK CHAMPION
INTERNATIONELL & NEDERLÄNDSK & TYSK & VDH CHAMPION
INTERNATIONELL & ITALIENSK CHAMPION
MONEGASKISK & SCHWEIZISK CHAMPION
BELGISK&FRANSK&ITALIENSK&LUXEMBURGSK
&SCHWEIZISK&MONEGASKISK CHAMPION
TYSK & DANSK CHAMPION
NEDERLÄNDSK & FRANSK & ÖSTERRIKISK CHAMPION
ÖSTERRIKISK & NEDERLÄNDSK CHAMPION
NEDERLÄNDSK & BELGISK & DANSK CHAMPION
AUSTRALISK & PORTUGISISK & FINSK CHAMPION
NEDERLÄNDSK & LUXEMBURGSK & TYSK & DANSK CHAMPION
PERUANSK & AMERIKANSK CHAMPION
SVENSK VILTSPÅRCHAMPION & SVENSK
JAKTPROVSCHAMPION
NORDISK & FINSK CHAMPION
ESTNISK & NEDERLÄNDSK & FINSK CHAMPION
MEXIKANSK & POLSK CHAMPION
ÖSTERRIKISK & SCHWEIZISK CHAMPION
AUSTRALISK & NYA ZEELÄNDSK CHAMPION
JUGOSLAVISK & ITALIENSK CHAMPION
SLOVENSK & KROATISK CHAMPION
AMERIKANSK & DANSK & SVENSK CHAMPION
DANSK & VDH CHAMPION
NORDISK & NORSK CHAMPION
SVENSK & FINSK & DANSK UTSTÄLLNINGSCHAMPION
AUSTRALISK & SLOVENSK CHAMPION
BELGISK & LUXEMBURGSK CHAMPION
SVENSK JAKTPROVSCHAMPION /DREV,GRYT,SPRÄNGARE/
SCHWEIZISK & AMERIKANSK CHAMPION
DANSK & NEDERLÄNDSK & SPANSK & SVENSK CHAMPION
FINSK & SVENSK JAKPROVS(GRYT)TCHAMPION
NORDISK LYDNADSCHAMPION & SVENSK
BRUKSPROVSCHAMPION
68
219
229
236
DK&FI UCH
LT&LV CH
NORD&US CH
237
246
SE&DK&FI&NO U(DV)CH
INT&NORD&BENELUX
247
249
257
258
259
AT&CH&FR&IT&MC&VDH
CH
DE&ES&FR&IL&VDH CH
FR&PL CH
SE L&BCH
NORD&NO&LU CH
280
ES&GI&IT CH&EUW-99
288
296
307
308
319
320
331
338
344
347
351
355
382
ZA CH&ZA FTCH
PL CH & LU CH
LU&NL CH
INT&LU CH
INT&SE&NO UCH
LP&SE LCH
SE&NO VCH
FI&NO UCH
VHIII
INT&NORD LCH
NORD U(GV)CH
DK&NO UCH
FI J(V&G)CH
397
413
415
417
425
430
431
433
458
462
475
479
500
506
SE U(DKV)CH
SJ&V CH
SE&FI&NO AGCH
DE&PL CH
DK U(GV)CH
LPELIT&SE LCH
LPI LPII LPIII&SE LCH
SE J(G/F&D)CH
BGCH PTCH
BY&RU CH
LVCH LTCH
KORAD SE&NO UCH
US&CA CH
NO B(IPO/BHP)CH
DANSK & FINSK CHAMPION
LITAUISK & LETTISK CHAMPION
NORDISK & AMERIKANSK CHAMPION
SVENSK & FINSK & DANSK & NORSK
UTSTÄLLNINGS(DREVPROV&VILTSPÅR)CHAMPION
INTERNATIONELL & NORDISK & BENELUX CHAMPION
FRANSK&MONEGASKISK&SCHWEIZ&VDH&ÖSTERRIKISK&
ITALIENSK CHAMPION
SPANSK & FRANSK & ISRAELISK & TYSK & VDH CHAMPION
POLSK & FRANSK CHAMPION
SVENSK LYDNADS & BRUKSPROVSCHAMPION
NORDISK & NORSK & LUXEMBURGSK CHAMPION
ITALIENSK & SPANSK & GIBRALTISK CHAMPION &
EUROPAVINNARE -99
SYDAFRIKANSK CHAMPION & SYDAFRIKANSK
JAKTPROVSCHAMPION
POLSK & LUXEMB CHAMP
LUXEMBURGSK & NEDERLÄNDSK CHAMPION
INTERNATIONELL & LUXEMBURGSK CHAMPION
INTERNATIONELL & SVENSK & NORSK CHAMPION
LYDNADSPROV I & SVENSK LYDNADSCHAMPION
SVENSK & NORSK VILTSPÅRPROVSCHAMPION
FINSK & NORSK CHAMPION
HOLLÄNDSKT BRUKSHUNDPROV III ELLER SKYDDSHUND III
INTERNATIONELL & NORDISK LYDNADSCHAMPION
NORDISK UTSTÄLLNINGS(GRYTPROV&VILTSPÅR)CHAMPION
DANSK & NORSK CHAMPION
FINSK JAKTPROVS(VILTSPÅR&GRYT)CHAMPION
SVENSK
UTSTÄLLNINGS(DREVPROV&KARAKTÄR&VILTSPÅR)CHAMPION
SVENSK JAKTPROVS- & VILTSPÅRPROVSCHAMPION
SVENSK & NORSK & FINSK AGILITYCHAMPION
POLSK OCH TYSK CHAMPION
DANSK UTSTÄLLNINGS(VILTSPÅR & GRYTPROV)CHAMPION
LYDNADSPROV III & SVENSK LYDNADSCHAMPION
LYDNADSPROV I II III & SVENSK LYDNADSCHAMPION
SVENSK JAKTPROVS(GRYTPROV/FÖRL&DREVPROV)CHAMPION
BULGARISK & PORTUGISISK CHAMPION
RYSK U-CHAMPION & VITRYSK U-CHAMPION
LETTISK OCH LITAUISK CHAMPION
KORAD SVENSK & NORSK UTSTÄLLNINGSCHAMPION
AMERIKANSK & CANADENSISK CHAMPION
69
512
514
523
530
533
540
541
547
550
551
553
554
562
563
566
567
573
576
594
599
601
GI&MX CH
ES&PT CH
SE&NO LCH
US&DE CH
INT&DK CH
NO J(D&G)CH
FI J(DG)CH
C.I.B&NORD UCH
SE UCH&J(D)CH
SE UCH&J(G)CH
SE UCH&J(DG)CH
SE UCH&J(RÄV)CH
DK AG&SPCH
EE&LT CH
CH&LU CH
INT&FI UCH
NORD&DK&DE CH
SE&FI JCH
NORD&FI&EE&LV CH
SE&DK&EE&LV CH
SE&FI U(G)CH
603
604
607
609
SE&FI U(KV)CH
SE&FI U(V)CH
FR J(DG)CH
INT J(DG)CH
635
638
DE&FR&LU&NL CH
AT&FR&LU&VDH CH
644
SE&NO U(DV)CH
646
647
648
649
SE&NO U(KV)CH
SE&NO U(D)CH
SE&NO U(G)CH
SE&NO U(V)CH
650
SE&NO U(GKV)CH
651
652
653
655
SE&DK U(KV)CH
SE&DK UCH
SE&DK U(G)CH
DK&FI&US CH
MEXIKANSK & GIBRALTISK CHAMPION
SPANSK & PORTUGISISK CHAMPION
SVENSK & NORSK LYDNADSCHAMPION
AMERIKANSK & TYSK CHAMPION
INTERNATIONELL & DANSK CHAMPION
NORSK JAKTPROVS(DREV&GRYT) CHAMPION
FINSK JAKTPROVS(DREV&GRYT)CHAMPION
INTERNATIONELL UCH & NORDISK UCH
SVENSK UTSTÄLLNINGS&JAKTPROVS(DREV)CHAMPION
SVENSK UTSTÄLLNINGS&JAKTPROVS(GRYT)CHAMPION
SVENSK UTSTÄLLNINGS&JAKTPROVS(DREV&GRYT)CHAMPION
SVENSK UTSTÄLLNINGS&JAKTPROVS(RÄV)CHAMPION
DANSK SPRING & DANSK AGILITY CHAMPION
ESTNISK & LITAUISK CHAMPION
SCHWEIZISK & LUXEMBURGSK CHAMPION
INTERNATIONELL & FINSK UTSTÄLLNINGSCHAMPION
NORDISK DANSK & TYSK CHAMPION(VDH)
SVENSK & FINSK JAKTPROVSCHAMPION
SVENSK & FINSK UTSTÄLLNINGS(GRYTPROV)CHAMPION
SVENSK & FINSK
UTSTÄLLNINGS(KARAKTÄR,VILTSPÅR)CHAMPION
SVENSK & FINSK UTSTÄLLNINGS(VILTSPÅR)CHAMPION
FRANSK JAKTPROVS(DREV&GRYTPROV)CHAMPION
INTERNATIONELL JAKTPROVS(DREV&GRYT)CHAMPION
NEDERLÄNDSK & LUXEMBURGSK & FRANSK & TYSK
CHAMPION
FRANSK&LUXEMBURGSK&ÖSTERRIKISK&VHDH CHAMPION
SVENSK & NORSK
UTSTÄLLNINGS(DREVPROV&VILTSPÅR)CHAMPION
SVENSK & NORSK
UTSTÄLLNINGS(KARAKTÄR&VILTSPÅR)CHAMPION
SVENSK & NORSK UTSTÄLLNINGS(DREVPROV)CHAMPION
SVENSK & NORSK UTSTÄLLNINGS(GRYTPROV)CHAMPION
SVENSK & NORSK UTSTÄLLNINGS(VILTSPÅR)CHAMPION
SVENSK & NORSK
UTSTÄLLNINGS(KARAKTÄR&VILTSPÅR&GRYTPROV)
CHAMPION
SVENSK & DANSK
UTSTÄLLNINGS(KARAKTÄR&VILTSPÅR)CHAMPION
SVENSK & DANSK CHAMPION
SVENSK & DANSK UTSTÄLLNINGS(GRYTPROV)CHAMPION
FINSK & DANSK & AMERIKANSK CHAMPION
70
657
INT U(GV)CH
667
671
678
681
696
700
701
702
INT&NL&DE&LU&IL CH
INT&SE UCH
EE&FI UCH
SE AGCH&SE
AG(HOPP)CH
FI&EE&PL CH
FI&NO U(V)CH
SE&FI J(D)CH
SE&FI J(G)CH
703
704
725
SE&NO U(DG)CH
FI&DK UCH
CH&VDH CH
731
737
738
743
747
748
749
750
INT U(DV)CH
SE UCH&JCH
NO UCH&J CH
NORD J(DG)CH
SE&FI UCH
SE&NO UCH
SE&NO J(D)CH
SE&NO J(G)CH
751
INT&NORD U(G)CH
753
INT&NORD U(V)CH
754
INT&NORD U(D)CH
755
INT&NORD U(KV)CH
756
762
774
777
778
793
798
799
814
INT&NORD U(DG)CH
US&CA CH
SE L&NO L(ELIT)CH
AT&FR&IT CH
INT&BE&CH CH
C.I.E&DK&NO UCH
SE VCH LPII
INT&NORD J(G)CH
INT&DK&FI UCH
820
FI U(KVDG)CH
INTERNATIONELL
UTSTÄLLNINGS(VILTSPÅR&GRYTPROV)CHAMPION
INT&NEDERLÄNDSK&TYSK&LUXEMBURGSK&ISRAELISK
CHAMPION
INTERNATIONELL & SVENSK UTSTÄLLNINGSCHAMPION
ESTNISK OCH FINSK UTST CHAMPION
SVENSKT AGILITY- & AGILITY(HOPP)CHAMPIONAT
FINSK & ESTNISKT & POLSKT
NORSK & FINSK UTSTÄLLNINGS(VILTSPÅR)CHAMPION
SVENSK & FINSK JAKTPROVS(DREVPROV)CHAMPION
SVENSK & FINSK JAKTPROVS(GRYTPROV)CHAMPION
SVENSK & NORSK
UTSTÄLLNINGS(DREV&GRYTPROV)CHAMPION
FINSK & DANSK CHAMPION
SCHWEIZISK & VDH CHAMPION
INTERNATIONELL
UTSTÄLLNINGS(DREVPROV&VILTSPÅR)CHAMPION
SVENSK UTSTÄLLNINGS & JAKTPROVSCHAMPION
NORSK UTSTÄLLNINGS & JAKTPROVSCHAMPION
NORDISK JAKTPROVS(DREV&GRYT)CHAMPION
SVENSK & FINSK UTSTÄLLNINGSCHAMPION
SVENSK & NORSK UTSTÄLLNINGSCHAMPION
SVENSK & NORSK JAKTPROVS(DREV)CHAMPION
SVENSK & NORSK JAKTPROVS(GRYT)CHAMPION
INTERNATIONELL & NORDISK
UTSTÄLLNINGS(GRYTPROV)CHAMPION
INTERNATIONELL & NORDISK
UTSTÄLLNINGS(VILTSPÅR)CHAMPION
INTERNATIONELL & NORDISK
UTSTÄLLNINGS(DREVPROV)CHAMPION
INTERNATIONELL & NORDISK
UTSTÄLLNINGS(KARAKTÄR&VILTSPÅR)CHAMPION
INTERNATIONELL & NORDISK
UTSTÄLLNINGS(GRYT&DREVPROV)CHAMPION
AMERIKANSK & KANADENSISK CHAMPION
SVENSK & NORSK LYDNADS(ELIT)CHAMPION
ÖSTERRIKISK & ITALIENSK & FRANSK CHAMPION
INTERNATIONELL & BELGISK & SCHWEIZISK CHAMPION
SVENSK VILTSPÅRCHAMPION & LYDNADSPROV II
INTERNATIONELL & NORDISK JAKTPROVS(GRYT)CHAMPION
INTERNATIONELL FINSK DANSK CHAMPION
FINSK UTSTÄLLNINGS(KARAKTÄR&VILTSPÅR&DREV
&GRYTPROV)CHAMPION
71
833
834
835
844
FI&NO J(G)CH
DK&CS&NL&IT CH
DE&VDH CH
BE&FR&HU&LU&NL&PL
CH
INT&NORD UCH SE
B&LCH
871
INT&NORD U(GKV)CH
873
876
882
887
897
915
946
956
957
978
979
INT&NORD U(DV)CH
SE&FI LCH
INT&NORD UCH
JCH
DE&HU&PL CH
EE&GI CH
BE&DE CH
INT&NORD&NO&HU&SL
UCH
BE&DE&NL CH
AR&CL CH
BENELUX CH
985
987
1100
S BCH TJH(RH)
SE BCH&LCH
CIB&CIE
837
NORSK & FINSK JAKTPROVS(GRYT)CHAMPION
TYSK & VDH CHAMPION
BELGISK&NEDERLÄNDSK&LUXEMBURGSK&FRANSK
&UNGERSK&POLSK CHAMPION
INTERNATIONELL&NORDISK UTSTÄLLNINGS-&
SVENSK BRUKSPROVS-&LYDNADSCHAMPION
INTERNATIONELL & NORDISK
UTSTÄLLNINGS(KARAKTÄR&VILTSPÅR&GRYTPROV)
CHAMPION
INTERNATIONELL & NORDISK
UTSTÄLLNINGS(DREVPROV&VILTSPÅR)CHAMPION
SVENSK & FINSK LYDNADSCHAMPION
INTERNATIONELL & NORDISK UTSTÄLLNINGSCHAMPION
JAKTPROVSCHAMPION
ESTNISK & GIBRALTAR CHAMPION
TYSK & BELGISK CHAMPION
NEDERLÄNDSK & BELGISK & TYSK CHAMPION
ARGENTINSK & CHILENSK CHAMPION
BELGISK & NEDERLÄNDSK & LUXEMBURGSK CHAMPION
SVENSKT BRUKSPROVSCHAMPIONAT
TJÄNSTEHUND(RÄDDNING)
SVENSK BRUKS- & LYDNADSCHAMPIONAT
(The Table includes Championships that existed in the Swedish Kennel Club’s Data Base on
September 10th 2012. Queries were answered by Håkan Ericson, SKC, personal communication.)
72