Theriogenology 150 (2020) 20e26

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Theriogenology
journal homepage: www.theriojournal.com

The dog 2.0: Lessons learned from the past

Bart J.G. Broeckx
Laboratory of Animal Genetics, Faculty of Veterinary Medicine, Ghent University, Heidestraat 19, 9820, Merelbeke, Belgium

a r t i c l e i n f o a b s t r a c t

Article history: In recent years, concerns have been raised on the diversity, health and welfare of our (pedigree) dog
Received 15 January 2020 population. Somewhat justified, the popular sire effect, population bottlenecks, the founder effect and
Accepted 18 January 2020 inbreeding have left their marks on the dog as we know it. In order to improve the health and welfare of
Available online 21 January 2020
the canine population in general, individual breeding programs should adhere to the concept of ethical
breeding (i.e. “the use of healthy animals true to their species in behaviour and looks, and when applicable,
Keywords:
showing a sustainable performance”) when population-specific breeding goals are defined. Even though
Ethical breeding
every population has its own problems, the approach to get to possible solution(s) is similar. The starting
Genetic diversity
Population history
point will always be the identification of which (un)desirable pheno- and genotypes are segregating and
(Un)desirable phenotypes what their prevalence is, followed by an evaluation of the genetic diversity. Based on that information
and, when applicable, additional criteria like breed standards, breeding goals can be defined. It is of
critical importance that these goals are put forward with a long term vision in mind and with consensus
from the stakeholders to ensure collaboration. Upon prioritization of the most important goals, when
necessary with the help of specifically developed tools, the final step is choosing the most optimal
combination of breeding strategies. This paper aims to provide a stepwise approach to identify and tackle
population-specific problems encountered in breeding programs.
© 2020 Elsevier Inc. All rights reserved.

1. Introduction danger, it is clear that countermeasures should be put in place. As

On the 19th of August 2008, the BBC-documentary Pedigree Dogs
Exposed was aired on television, immediately resulting in quite
some commotion. Are pedigree dogs dangerously inbred? Do we
have to worry about their welfare? [1] As often the case, the answer
is not black or white. Whereas the morphological diversity of the
dog species in its whole is exceptional, the genetic diversity can be
dangerously low in some breeds [2e4]. Furthermore, whereas
diseases in dogs are often remarkably similar to conditions in
humans, the frequency at which they occur is far higher in dogs
[5e7]. Just one example is degenerative myelopathy and its human
counterpart, amyotrophic lateral sclerosis. Degenerative myelop-
athy has been found in three to six percent of the German Shepherd
Dogs, whereas amyotrophic lateral sclerosis in humans has a dis-
ease prevalence of seven to nine out of 100,000, which is around a
thousand times less [5,6,8]. Of course, this does not mean that every
dog’s welfare is harmed. A critical point however is that, in some
cases, the answer is yes to both questions.
Whenever the genetic diversity and/or welfare of dogs is in
problems and breeding goals are population-specific, this is not
always easy. The main aim of this paper is to provide a stepwise
approach to identify the main issue(s) in a specific breeding pop-
ulation and breeding strategies to resolve them. This starts by
explaining the mechanisms that can result in a reduced genetic
diversity and a high frequency of disorders. Whereas every
breeding program has one or more breeding goals, not every
breeding goal has been harmless as has been proven in the course
of history. Especially the breeding goals in certain breed standards
have been associated with disorders. The definition of “ethical
breeding” can help to evaluate the appropriateness of individual
breeding goals. The actual stepwise approach towards a solution
starts with the identification of (un)desirable pheno- and geno-
types and obtaining population-specific incidence and prevalence
estimates, next to an overview of the genetic diversity. When these
steps have been finished and breeding goals have been defined,
several tools are discussed to 1) reduce the frequency of disorders
and 2) increase the genetic diversity. Special emphasis has been
given to disorders related to breed standards as they require a
separate approach.

E-mail address: bart.broeckx@ugent.be.

https://doi.org/10.1016/j.theriogenology.2020.01.043
0093-691X/© 2020 Elsevier Inc. All rights reserved.
 B.J.G. Broeckx / Theriogenology 150 (2020) 20e26
2. What has caused the high frequency of genetic disorders
and reduced genetic diversity?
The central issue in the whole process is that no single animal,
even those that look entirely healthy, is free of disease-associated
variants. This is substantiated by the observation that when over
100,000 dogs were tested for a panel of 152 disease-associated
variants, > 40% of the dogs were found to have disease-associated
variant(s) in a hetero- or homozygous state [9]. Logic dictates that
this percentage would only go up when more variants would be
assessed. This is easy to understand for recessive disorders where a
carrier status (i.e. being heterozygous) is not associated with
symptoms. However, even being homozygous for disease-
associated variants (genetically affected dogs) responsible for
recessive diseases, or being heterozygous or homozygous for vari-
ants associated with dominant disorders (in both cases, the dogs
are genetically affected) does not necessarily result in clinical
symptoms due to for example reduced penetrance (i.e. not every
animal expresses the phenotype, even though the animal should do
so based on its genotype).
While having a disease-causing allele does not have to be
harmful for the dog itself, this variant can be passed on to future
generations. Every disproportionate contribution to future gener-
ations will as such affect the frequency of disease-causing alleles in
these generations. A common example is the popular sire effect
where popular studs, with popularity often associated with win-
ning dog shows, have a very large progeny (sometimes even over
2500 puppies) [2]. Similarly, population bottlenecks, where only a
small subset of the population remains to produce the future
generations and the so-called founder effect, i.e. the often very
small number of dogs that lie at the origin of for example a new
breed, have the same consequences: future generations will be a
genetic reflection of these initial dogs and that for both the desir-
able and undesirable characteristics [10]. Inbreeding and line
breeding, the mating of related individuals (or, more correctly,
more related than would be the case in random mating conditions
on average), increase the homozygosity at the genomic level and, as
such, traits that are recessive might all of a sudden surface where
they were previously hidden in heterozygous carriers [10,11].
Overall, these practices result in a decrease of the genetic diversity
of a population.
The enormous phenotypical diversity of the dog as we know it is
the resultant of all these practices. At the same time, inadvertently,
it also resulted in genetic diseases being far from rare.
3. Ethical breeding
It is clear that the concerns regarding dog breeding are related to
genetic diversity, health problems and animal welfare, with the
latter being defined as “the physical and mental state of an animal in
relation to the conditions in which it lives and dies” [12]. To address
these issues, it is important to determine the general concept of
what the aim of animal breeding is. A basic definition is that animal
breeding refers to the sexual reproduction of animals. Omitting
health and welfare, it is clear that this definition is not entirely
fitted for the job. This is where the concept of “ethical breeding”
comes into the picture. With the aim of being valid for both com-
panion and production animals, ethical breeding is considered to be
“the use of healthy animals true to their species in behaviour and looks,
and when applicable, showing a sustainable performance”. This
definition embraces these concepts and still allows breeding to-
wards aesthetic goals, if these goals are harmless [13,14]. As such,
this definition can be applied when it comes to all kinds of dog
breeding, irrespective of whether the goal is breeding towards
specific behavioural characteristics or towards a conformational
21
characteristic as for example those specified in breed standards.
This also means that breeding goals can differ between breeding
programs and that breeding practices should be tailored to the
population of interest.
4. Towards a solution
Whenever a breeding program is initiated, it is important to
determine the breeding goals upfront. The identification of health
and welfare issues should be central in every breeding program. A
breeding program for working dogs however is likely to contain in
addition some sort of performance characteristic(s) that allow(s) an
assessment of how suitable a certain dog is.
Before engaging in a breeding program, it is important to take
several additional remarks into account. Firstly, as measurable ge-
netic progress can only be expected after two to three generations,
breeding goals have to be maintained for several generations and
patience is necessary [15]. Secondly, easy to imagine, especially for
behaviour, but not necessarily easily implemented: environment(al
influences) can dramatically influence phenotypes [15]. As such,
emphasis should also be put on optimizing the environment.
4.1. Identifying (un)desirable pheno- and genotypes
The starting point is the identification of (un)desirable pheno-
and genotypes segregating in the population of interest. Several
sources of information are available. First and foremost, the pop-
ulation itself. This immediately also implies that some sort of record
keeping system should be available [15]. Records should be kept on
ancestry and both desirable and undesirable pheno- and genotypes.
Secondly, several online resources are available with the most well-
known being the Online Mendelian Inheritance in Animals data-
base, the Canine Inherited Disorders database and Inherited Dis-
eases in Dogs [16e18]. Additional literature searches using for
example PubMed provide further information [9,19,20]. While
listing all the phenotypes, details on the inheritance pattern and
the existence (and reliability) of DNA-tests have to be collected as
well.
4.2. Optimal diagnostic techniques: correctly assigning a phenotype
at the level of the individual animal
While it might seem obvious, it cannot be stressed enough that
the amount of genetic progress is directly related with how correct
the phenotypes are. This implies that the most optimal diagnostic
techniques should be used, ideally those with a perfect sensitivity
and specificity. For example, the introduction of laxity techniques
for canine hip dysplasia screening and of computed tomography for
elbow dysplasia screenings resulted both in a significant increase in
the number of dogs detected with either of these disorders [21,22].
Furthermore, for some phenotypes, the importance of the person
that performs the evaluation should not be neglected. For example,
for canine hip dysplasia, the interobserver agreement increases
with experience of the evaluator, whereas for canine cruciate lig-
ament rupture, experience does not seem to influence the agree-
ment on the diagnosis [23,24]. It is clear that expert advice should
be sought whenever necessary.
4.3. The population level: estimating the prevalence and the
incidence
Obtaining correct incidence and prevalence estimates is the
next step towards a healthier population. However, population-
specific data is often lacking and extrapolating data from other
studies is not without danger as even within a breed
22 B.J.G. Broeckx / Theriogenology 150 (2020) 20e26

subpopulations can exist [20,25]. For example, the population dif-
ferentiation values, expressed as Fst with calculations based on
single nucleotide polymorphism data, demonstrated that the
American and Dutch Golden Retrievers are genetically as divergent
from each other as European and East Asian human populations
[25,26].
An important factor to consider is the effect of selection bias.
This can be perfectly illustrated with canine hip dysplasia.
Routinely screened for with the standard ventrodorsal hip
extended radiographic view, several grading schemes exist world-
wide and prevalence estimates are generally based on the numbers
from the committees evaluating these radiographs. It has however
been observed that there is a tendency to submit for evaluation
only those radiographs that will receive passing scores [27,28]. The
obvious consequence is that the prevalence of canine hip dysplasia
is likely to be underestimated. It is important to realize that this
potentially also has consequences for breeding. The reason is that
often the 50% rule is applied: breeding stock should be selected
from the best 50% of the population [29]. Irrespective of whether it
is 25%, 50% or another cut-off, if this selection is based on a biased
prevalence estimate, it might result in a higher selection pressure,
as is the case for canine hip dysplasia. In more detail, for canine hip
dysplasia, diseased animals were omitted from the database, hence
the problem is underestimated and the cut-off is set too high at hips
that have to be too good. Whereas this might result in a higher
response for the phenotype under study at the population level, at
the same time, the selection might be that strong that it actually
results in the population being forced through a population
bottleneck with the associated negative consequences.
The converse is also possible: a database which contains too
many diseased animals relative to the truth might result in an
overestimation of the problem, a biased cut-off set too low, a se-
lection pressure that is lower than expected and, as such, a slower
response to selection for the entire population. An example is
canine hip dysplasia prevalence estimates based on an orthopaedic
clinic for which is it very likely that they mostly see animals with
clinical problems [28]. A worked-out example of both situations is
detailed in Fig. 1.
These over- and underestimations can also occur when preva-
lence numbers are based on other breeds or even species. Extrap-
olating canine hip dysplasia prevalence from the Dobermann (10%
affected) results in an underestimation from canine hip dysplasia in
the German Shepherd (23% affected), while both prevalence esti-
mates are two to 3 times higher than what has been found in the
Siamese cat [30,31].
These examples illustrate what might happen when prevalence
estimates are missing for a specific breed and results are extrapo-
lated from other breeds or species. Extrapolating results might
result in both over- and underestimations of the disease prevalence
and might affect the progress achieved for that specific disease and
the genetic diversity in the entire population. This stresses the
importance of getting as much information as possible from that
specific population/breed/ … where selection pressure is to be
applied on.
4.4. Genetic diversity
The genetic diversity of a population can be assessed with ge-
netic markers or based on pedigree data. At a relatively low cost,
genetic markers can be used in the absence of pedigree data and are
not susceptible to pedigree errors [4,11,32]. They can however be
biased when for example only a small number of animals and/or
markers are genotyped [4,33].
As a prerequisite for a successful breeding program is that ani-
mal records (including ancestry) are kept thoroughly, all informa-
tion should be available to immediately assess genetic diversity
based on genealogical data. It is however clear what the potential
downsides are of this method: pedigree errors have to be avoided
at all cost and a lack of knowledge on ancestry might bias the re-
sults [4,11]. On a side note, paternity testing (using the same
markers to calculate genetic diversity) can be used to assess
ancestry and correct pedigree errors.
A correct assessment of the genetic diversity is important to
determine the starting point, but even more to evaluate how it
evolves as that should be kept under control. This evolution is often
expressed in terms of the rate of inbreeding DF or the effective

Fig. 1. Comparison of the response to selection R and the population size selected for breeding when selection cut-offs are based on biased and unbiased sampling. The
laxity index is a measure that quantifies the amount of laxity which is the primary cause of hip dysplasia [21]. Three situations are compared: population estimates are correct
(situation 1, in grey shaded), diseased animals are selectively omitted (situation 2, “too many healthy”) and the proportion of healthy animals is underestimated (situation 3, “too
many diseased”). For each situation, only animals scoring better (i.e. that have lower laxity values) or equal to the sample average are retained for breeding. These sample averages
correspond to 0.44 (also the correct population mean value, middle vertical full line), 0.19 (left vertical dashed line) and 0.69 (right vertical dotted line) for situation 1 to 3,
respectively and only those animals from the grey population that are to the left of the situation-specific vertical line are selected for breeding. The response to selection (i.e. the
progress that is made), is equal to the product of the heritability (set at 0.66 [48]) and the selection differential, i.e. the difference between the mean value of the individuals selected
to be parents and the mean value of the population (i.e. 0.35, 0.15 and 0.43 for population 1 to 3, respectively) [34]. Practically, R equals to a decrease of 0.06, 0.19 and z 0.00 for
population 1 to 3, respectively. The proportion of animals from the population that fulfil the selection criterion and are allowed to breed is 50%, 1% and 99% for population 1 to 3,
respectively. In situation 1, a gradual progress is achieved, while the population remains reasonably sized. In situation 2, the sample average is set far too low, the laxity decreases
fast but the population is forced through a massive population bottleneck and this only after selection has been performed for one phenotype. In situation 3, the sample average (the
right vertical dotted line) is way too high, nearly no progress is made and nearly the entire population remains available for breeding.
 B.J.G. Broeckx / Theriogenology 150 (2020) 20e26
Fig. 2. The consequences on population size (x-axis) of three different breeder
strategies to deal with DNA-test results for recessive diseases. The breeder strategy
that is followed to deal with the results from genetic tests can have profound effects on
the proportion of the population that is considered suitable for breeding (and, as such,
on the genetic diversity). This is illustrated by subsequently performing two DNA-tests
for the autosomal recessive diseases exercise-induced collapse (EIC) and a specific type
of progressive retinal atrophy, i.e. progressive rod cone degeneration (PRCD), based on
a frequency study conducted in the Labrador Retriever [7]. After each test, the pro-
portion of dogs that remains as a breeder is depicted in light grey, the proportion that
is excluded is depicted in dark grey. The first strategy involves excluding all dogs that
are hetero- or homozygous for the disease-causing mutation (a). After two tests, only
55% of the original population remains. The second strategy involves excluding only
the dogs that are homozygous for the disease-causing mutation (i.e. the genetically
affected ones) (b). The reduction of the population is far less, 90% of the original
populations remains. The final strategy entails not excluding dogs but only allowing
specific combinations to make sure that no genetically affected dogs are born. Using
this strategy, not a single dog is excluded and the frequency of genetically affected dogs
(i.e. dogs homozygous for these disease-causing mutations) still can be immediately
reduced to zero. Based on these results, it is clear that the third strategy is the
preferred one. However, this strategy can only be followed if using genetically affected
dogs for breeding does not result in a reduced welfare for the dogs itself or the puppy.
23
population size Ne (which is defined as “the number of breeding
individuals in a population under random selection and random
mating, i.e. a so-called “ideal” population, that would show the
same decrease of genetic diversity as the population studied”
[11,34]). Mathematically, there is a direct link between the two of
them. Often used thresholds for the latter are 50 (corresponding to
a DF of one percent) and 100 (corresponding with a DF of 0.5%) as
these thresholds are generally considered to be sufficient to avoid
issues like inbreeding depression [10,35,36]. Above these thresh-
olds, selection can be applied with the stringency of selection
depending on the measured Ne values, but genetic diversity should
always be carefully monitored and maximized as much as possible,
especially if Ne values are close to 50. Once the Ne is
50, selection
should be stopped and the focus should lie entirely on increasing
genetic diversity [35]. Unfortunately, this situation is not rare as
illustrated in the next paragraph.
A recent study in 23 dog breeds in Belgium revealed that nine
had an Ne below 50, whereas an additional seven breeds had values
between 50 and 100 [4]. An older study from the UK revealed that
six out of 10 breeds had a value lower than 50 and three between 50
and 100, while in Australia, this was five and 12 out of 29, respec-
tively [2,3]. An example of a breed that consistently scores good in
all three studies is the Labrador Retriever with an Ne ranging be-
tween 107 and 153 [2e4]. Breeds with values beneath 50 vary
between studies but examples are the Bichon Frise
(Ne ¼ 18) [4], the
Greyhound (Ne ¼ 17) [2] and the Smooth Fox Terrier (Ne ¼ 40) [3].
An example of a breed where the numbers are quite variable is the
Boxer that is in the danger zone in the UK (Ne ¼ 45), whereas it
scores slightly better in Belgium (Ne ¼ 58) and good in Australia
(Ne ¼ 113) [2e4]. Combined, it is clear that the situation is dramatic
in certain breeds. At the same time, the values are highly breed- and
population-dependent. This indicates again that breed-specific or
population-specific breeding programs is what should be aimed for.
4.5. Getting priorities straight
It will seldomly be the case that only one phenotype is to be
improved in a breeding population. As genetic improvement nearly
always requires selection of a subset of the population, with one
notable exception when DNA-tests are available (see below), the
number of phenotypes that can be selected for at the same time is
limited, especially when genetic diversity is already low. Deter-
mining which of those phenotypes deserves priority is however not
so easy. Should one focus on a severely debilitating disorder that
affects only a small proportion of the population or a less severe
one that affects the majority? While the choice will always be
somewhat subjective and open for debate, several criteria have
been developed that might help to prioritize disorders. Part of the
actions undertaken after the release of Pedigree Dogs Exposed, the
Generic Illness Severity Index for Dogs (GISID) was developed. For
every disease, the GISID tries to numerically value prognosis,
treatment, complications and how it affects behaviour to get to a
disease-specific overall score from zero to 16 [19,20]. Combining
this with prevalence estimates and disease-duration, a welfare-
index that ranges between zero and 100 can be calculated for
each disorder at the population level with higher values being
associated with a more severe impact on the welfare of the dog
[37]. An example based on hip and elbow dysplasia demonstrates
that the former is associated with a higher welfare-index and
should receive a higher priority (Table 1). An alternative score for
working dogs, the so-called work score, was developed specifically
If that would be the case, the second strategy or a combination of strategy two or three
should be aimed for.
24 B.J.G. Broeckx / Theriogenology 150 (2020) 20e26

Table 1
Comparison of the welfare-index for hip and elbow dysplasia in a population of Labrador Retrievers.

Phenotype Absolute/relative GISID scorea Prevalenceb Proportion of life afflictedb Welfare-indexc

Hip dysplasia 10/0.625 12 0.90 7

Elbow dysplasia 6/0.375 7 0.90 2
d
Calculated as welfare-index ¼ relative GISID score  prevalence  proportion of life afflicted.
a
The absolute Generic Illness Severity Index for Dogs (GISID) score ranges from zero to 16, the relative GISID score is this score divided by the maximum score of 16. As the
GISID score often is a range, the maximum GISID score was used for each disorder [19].
b
Based on the formula ¼ (number of affected individuals/total population size) x 100.
c
The disease duration or proportion of life afflicted is based on the age at diagnosis (i.e. 1 year for both diseases) [22] and the median life span for the Labrador Retriever (i.e.
10.5 years) [59] and calculated with the formula ¼ (life span e age of diagnosis)/life span.

for working dogs as it takes the impact on the (reduction of the)
working life into account [38]. This and another study also
demonstrate again the importance of a broad view which is not
limited to diseases sensu stricto as behavioural rejections are at the
top of the list [22,38].
4.6. Breeding strategies
4.6.1. DNA-tests
Selection becomes far more easy when a reliable DNA-test is
available. Several diseases are known for their reduced penetrance,
albeit that they are late-onset (e.g. degenerative myelopathy) or
only expressed when dogs undergo strenuous exercise (e.g.
exercise-induced collapse) and might remain phenotypically un-
detected as such [39,40]. With DNA-tests for autosomal recessive
disorders, carriers can easily be identified and basically any dog can
still be used for breeding, if carriers and genetically affected dogs
are combined with dogs free from the mutation [29,41]. It goes
without saying that this is a big advantage, especially in those
populations where the genetic diversity is dangerously low, as
illustrated in Fig. 2. A remark is that a dog homozygous for a
recessive disease-causing variant should only be mated (with a dog
homozygous for the normal allele) when it does not negatively
influence the welfare of that individual dog or its puppies. As a
practical example, given the late age-of-onset of degenerative
myelopathy (more than five years of age), a young dog (e.g. two to
four years of age) homozygous for the disease-causing mutation,
can still be included in the breeding program if the dog is symptom
free and does not have any other debilitating disease [42].
Three precautionary remarks should be made. The advantage of
not having to exclude an animal is unfortunately less present for
autosomal dominant, X-linked recessive and X-linked dominant
disorders as in all three cases, affected animals can be born when a
dog having the disease-causing variant (heterozygous or homozy-
gous) is used. Secondly, the reliability of DNA-tests is an important
point of consideration. Not every DNA-test that is commercially
available is indisputable and upon validation, sometimes even
opposite associations between genotypes and phenotypes have
been observed [43e45]. This might be the case when a variant is
not the causal one but for example a marker allele that is linked to a
causal allele. Upon recombination, the initial association can be
reversed at that moment [10]. It might also be a consequence of
erroneous associations due to for example population stratification
[46]. A thorough literature check to evaluate the evidence that
supports the association is important, together with consulting
genetic experts. Thirdly, there is an increasing trend to simulta-
neously perform DNA-tests for a wide range of diseases [9]. In
terms of cost, it might indeed be cheaper to order such a test
compared to performing several individual tests. It is however not
necessarily guaranteed that the “omnibus” tests assess every dis-
ease important for that specific breed. Furthermore, tests are often
performed irrespective of whether the association between the
genotype and the phenotype has already been established for that
specific breed. If mutations associated with disease are detected in
a breed where it was not previously reported, this might indeed
indicate that the phenotype is also segregating in that breed [9].
However, at the same time, the association with the phenotype
might depend on the breed-specific genetic background, as has
been reported for mice, making the test futile [47]. Either way, the
implementation of novel DNA-tests in breeding programs should
always be considered carefully while it is also the responsibility of
the scientific community to keep a watchful eye.
4.6.2. Test matings and pedigree analysis
Unfortunately, for quite some Mendelian diseases, a genetic test
is not (yet) available. At that moment, one has the option to perform
test matings [10]. A downside is that it is based on deliberately
trying to create dogs affected by the disorders, which is ethically
debatable. Furthermore, it takes quite some time to get the result,
i.e. the time between conception and normal onset of the symp-
toms, which can be long for some phenotypes. Finally, it is impor-
tant to realize that one can never prove that an animal is
homozygous normal from test matings: the absence of progeny
with disease can also be due to coincidence. As such, it is only with
a certain probability that one can state that an individual is free and
this probability of being normal increases when the number of
offspring increases. A more theoretical approach, based on a known
mode of inheritance and pedigree data, involves the calculation of
the probability that a prospective parent is homozygous for the
wild type allele. In the next step, one can retain those individuals
that have the lowest probability of having an undesired genotype
[10]. While this can be quite complex mathematically, commercial
software is available to solve this problem [10].
4.6.3. Estimated breeding values
The complexity of multifactorial disorders is illustrated by the
fact that each phenotype is the sum of the combined effect of ge-
netic determinants and environmental influences. The fact that the
phenotype is blurred makes it difficult to select the “best” dogs. As
the true (breeding) value of an individual dog is unknown, we can
estimate it based on own performance and (close and/or distant)
family members, with all information weighted depending on the
relation with that dog, which results in “estimated breeding values”
(EBVs) [10,48,49]. The more information from relatives that is
added in the equations, the more accurate these EBVs are. Instead of
selecting the animal based on its own performance alone (the so-
called “mass selection”), EBVs employed correctly allow a far
faster progress, as recently again demonstrated for e.g. canine hip
dysplasia in a guide dog population [49]. An additional advantage is
that when selection is to be applied on more than one phenotype,
EBVs can be combined into a selection index allowing simultaneous
selection [15].
 B.J.G. Broeckx / Theriogenology 150 (2020) 20e26
4.6.4. Disorders related to breed standards
Special attention should be given to disorders directly or indi-
rectly related to the breed standards. Examples are numerous and
include the association between the dorsal hair ridge and dermoid
sinus in the Rhodesian Ridgeback, brachycephalic obstructive
airway syndrome in brachycephalic dogs and deafness and patch-
ing in the Dalmatian [19,50e53]. Whereas unwanted phenotypes
not linked to the breed standard can be selected against within the
context of ethical breeding, this is far more difficult when a
phenotype is directly related to the actual breed standard. At that
moment, there is a direct conflict between that what makes an
animal “true to their species” (or breed, in this case) and the
remainder of the definition where health and welfare are central.
Luckily, health and welfare seem to outweigh the former, with the
recommendation to revise breed standards if they compromise
either of those two [1,37].
Some work still needs to be done however. Just one example is
the ridge from the Rhodesian Ridgeback mentioned earlier on.
Although a clear association has been found between the ridge and
dermoid sinus, the ridge is still part of the breed standard,1.2 In
more detail, a 133-kb duplication segregated perfectly with the
ridge with an autosomal dominant inheritance pattern [52]. At the
same time, the dermoid sinus also only occurred in dogs that were
hetero- or homozygous for this duplication [52]. As a dermoid sinus
can result in significant disease (associated with a score of up to 14
out of a maximum score of 16 according to GISID) and a solution is
easy (avoid breeding dogs with a ridge), there still seems room for
improvement [19]. For this specific case, this improvement means
altering the breed standard towards breeding Rhodesian Ridge-
backs without ridges.
4.6.5. Strategic choices to increase the diversity
To achieve the breeding goals, selection pressure in the desired
direction should be applied. At the same time, genetic diversity
should be maximized (or conversely, the rate of increase of
inbreeding each generation should be minimized) as much as
possible as it is the basis of a healthy population [11,15]. There are
several approaches that can be used to achieve this and they can all
be combined whenever necessary.
Firstly, increasing the number of animals that are available for
mating. With only five percent from the entire population involved
in breeding, only a small subset of potential dams and sires is
actually used [54]. In an attempt to solve this, the “CanIFreeze”
project was recently initiated at the Faculty of Veterinary Medicine
of Ghent University with the aim to encourage semen donation and
storage in a public semen bank [54]. To convince even those owners
that did not have breeding plans, a free insemination is offered,
with health check-ups included [54]. The end goal is to increase the
number of dogs that can be used for reproduction and reduce the
loss of valuable genetic material [54]. Secondly, as mentioned
earlier on, whenever a DNA-test is available, the focus should lie on
careful combination instead of exclusion of dogs (Fig. 2). Thirdly, to
avoid the overuse of (especially male) breeding dogs, the

de
Fe
ration Cynologique Internationale recommends to avoid that
any dog has more offspring than five percent of the number of
puppies registered over a five-year period [11]. While this general
rule is a good start, breed-specific rules taking the genetic diversity
of the population of interest into account, would be a further
advance [11]. Software algorithms can aid to optimize the number
of offspring from specific combinations that should be used to
1
http://www.fci.be/Nomenclature/Standards/146g06-en.pdf.
2
https://www.thekennelclub.org.uk/services/public/breed/standard.aspx?
id¼1026.
25
contribute to future generations tailored to the population-specific
situation [55]. Finally, whenever several dogs meet the selection
criteria for breeding, it is best to combine those dogs that are the
least related [15,36].
Taking the effective population size cut-offs mentioned earlier
into account, it is clear that relatively small breeding programs are
possible, but only when performed in collaboration with other
breeding programs. Luckily, advances like artificial insemination
make the (inter)national exchange of genetic material far more
easy.
5. Concluding remarks
It is clear that only a subset of the techniques currently available
have been described here. The reason to focus on these techniques
is that they provide solutions for all kinds of phenotypes, ranging
from a Mendelian to a complex mode of inheritance, and that all
these techniques are feasible as they only require solid record
keeping which is either way a prerequisite when one wants to set
up an at least reasonably sized breeding program with a clear di-
rection. In the future, it is likely that more DNA-based techniques
will be employed with genomic selection being the most well-
known example already widely implemented in production ani-
mals [56e58].
Overall, it should be clear that certain concerns regarding dog
breeding are justified. It is however way too easy to just dismiss
(pedigree) dog breeding as bad for welfare. Instead, an individual
breed-specific approach is of paramount importance. Where the
focus should lie entirely on increasing genetic diversity in one
population, other populations can focus far more on selection to-
wards prespecified breeding goals and, luckily, there are good tools
to solve each of these problems. The word “prespecified” is critical
in the previous sentence: it stresses the importance of thinking
ahead, but also on a collaboration to define these breeding goals
and openness between all stakeholders to identify the issues at
hand. The approach described here should aid in achieving these
goals.
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