Theriogenology 150 (2020) 20e26

Contents lists available at ScienceDirect

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

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

E-mail address: [email protected].

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 21

2. What has caused the high frequency of genetic disorders characteristic as for example those specified in breed standards.
and reduced genetic diversity? This also means that breeding goals can differ between breeding
programs and that breeding practices should be tailored to the
The central issue in the whole process is that no single animal, population of interest.
even those that look entirely healthy, is free of disease-associated
variants. This is substantiated by the observation that when over 4. Towards a solution
100,000 dogs were tested for a panel of 152 disease-associated
variants, > 40% of the dogs were found to have disease-associated Whenever a breeding program is initiated, it is important to
variant(s) in a hetero- or homozygous state [9]. Logic dictates that determine the breeding goals upfront. The identification of health
this percentage would only go up when more variants would be and welfare issues should be central in every breeding program. A
assessed. This is easy to understand for recessive disorders where a breeding program for working dogs however is likely to contain in
carrier status (i.e. being heterozygous) is not associated with addition some sort of performance characteristic(s) that allow(s) an
symptoms. However, even being homozygous for disease- assessment of how suitable a certain dog is.
associated variants (genetically affected dogs) responsible for Before engaging in a breeding program, it is important to take
recessive diseases, or being heterozygous or homozygous for vari- several additional remarks into account. Firstly, as measurable ge-
ants associated with dominant disorders (in both cases, the dogs netic progress can only be expected after two to three generations,
are genetically affected) does not necessarily result in clinical breeding goals have to be maintained for several generations and
symptoms due to for example reduced penetrance (i.e. not every patience is necessary [15]. Secondly, easy to imagine, especially for
animal expresses the phenotype, even though the animal should do behaviour, but not necessarily easily implemented: environment(al
so based on its genotype). influences) can dramatically influence phenotypes [15]. As such,
While having a disease-causing allele does not have to be emphasis should also be put on optimizing the environment.
harmful for the dog itself, this variant can be passed on to future
generations. Every disproportionate contribution to future gener- 4.1. Identifying (un)desirable pheno- and genotypes
ations will as such affect the frequency of disease-causing alleles in
these generations. A common example is the popular sire effect The starting point is the identification of (un)desirable pheno-
where popular studs, with popularity often associated with win- and genotypes segregating in the population of interest. Several
ning dog shows, have a very large progeny (sometimes even over sources of information are available. First and foremost, the pop-
2500 puppies) [2]. Similarly, population bottlenecks, where only a ulation itself. This immediately also implies that some sort of record
small subset of the population remains to produce the future keeping system should be available [15]. Records should be kept on
generations and the so-called founder effect, i.e. the often very ancestry and both desirable and undesirable pheno- and genotypes.
small number of dogs that lie at the origin of for example a new Secondly, several online resources are available with the most well-
breed, have the same consequences: future generations will be a known being the Online Mendelian Inheritance in Animals data-
genetic reflection of these initial dogs and that for both the desir- base, the Canine Inherited Disorders database and Inherited Dis-
able and undesirable characteristics [10]. Inbreeding and line eases in Dogs [16e18]. Additional literature searches using for
breeding, the mating of related individuals (or, more correctly, example PubMed provide further information [9,19,20]. While
more related than would be the case in random mating conditions listing all the phenotypes, details on the inheritance pattern and
on average), increase the homozygosity at the genomic level and, as the existence (and reliability) of DNA-tests have to be collected as
such, traits that are recessive might all of a sudden surface where well.
they were previously hidden in heterozygous carriers [10,11].
Overall, these practices result in a decrease of the genetic diversity 4.2. Optimal diagnostic techniques: correctly assigning a phenotype
of a population. at the level of the individual animal
The enormous phenotypical diversity of the dog as we know it is
the resultant of all these practices. At the same time, inadvertently, While it might seem obvious, it cannot be stressed enough that
it also resulted in genetic diseases being far from rare. the amount of genetic progress is directly related with how correct
the phenotypes are. This implies that the most optimal diagnostic
3. Ethical breeding techniques should be used, ideally those with a perfect sensitivity
and specificity. For example, the introduction of laxity techniques
It is clear that the concerns regarding dog breeding are related to for canine hip dysplasia screening and of computed tomography for
genetic diversity, health problems and animal welfare, with the elbow dysplasia screenings resulted both in a significant increase in
latter being defined as “the physical and mental state of an animal in the number of dogs detected with either of these disorders [21,22].
relation to the conditions in which it lives and dies” [12]. To address Furthermore, for some phenotypes, the importance of the person
these issues, it is important to determine the general concept of that performs the evaluation should not be neglected. For example,
what the aim of animal breeding is. A basic definition is that animal for canine hip dysplasia, the interobserver agreement increases
breeding refers to the sexual reproduction of animals. Omitting with experience of the evaluator, whereas for canine cruciate lig-
health and welfare, it is clear that this definition is not entirely ament rupture, experience does not seem to influence the agree-
fitted for the job. This is where the concept of “ethical breeding” ment on the diagnosis [23,24]. It is clear that expert advice should
comes into the picture. With the aim of being valid for both com- be sought whenever necessary.
panion and production animals, ethical breeding is considered to be
“the use of healthy animals true to their species in behaviour and looks, 4.3. The population level: estimating the prevalence and the
and when applicable, showing a sustainable performance”. This incidence
definition embraces these concepts and still allows breeding to-
wards aesthetic goals, if these goals are harmless [13,14]. As such, Obtaining correct incidence and prevalence estimates is the
this definition can be applied when it comes to all kinds of dog next step towards a healthier population. However, population-
breeding, irrespective of whether the goal is breeding towards specific data is often lacking and extrapolating data from other
specific behavioural characteristics or towards a conformational 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- These over- and underestimations can also occur when preva-
ferentiation values, expressed as Fst with calculations based on lence numbers are based on other breeds or even species. Extrap-
single nucleotide polymorphism data, demonstrated that the olating canine hip dysplasia prevalence from the Dobermann (10%
American and Dutch Golden Retrievers are genetically as divergent affected) results in an underestimation from canine hip dysplasia in
from each other as European and East Asian human populations the German Shepherd (23% affected), while both prevalence esti-
[25,26]. mates are two to 3 times higher than what has been found in the
An important factor to consider is the effect of selection bias. Siamese cat [30,31].
This can be perfectly illustrated with canine hip dysplasia. These examples illustrate what might happen when prevalence
Routinely screened for with the standard ventrodorsal hip estimates are missing for a specific breed and results are extrapo-
extended radiographic view, several grading schemes exist world- lated from other breeds or species. Extrapolating results might
wide and prevalence estimates are generally based on the numbers result in both over- and underestimations of the disease prevalence
from the committees evaluating these radiographs. It has however and might affect the progress achieved for that specific disease and
been observed that there is a tendency to submit for evaluation the genetic diversity in the entire population. This stresses the
only those radiographs that will receive passing scores [27,28]. The importance of getting as much information as possible from that
obvious consequence is that the prevalence of canine hip dysplasia specific population/breed/ … where selection pressure is to be
is likely to be underestimated. It is important to realize that this applied on.
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 4.4. Genetic diversity
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, The genetic diversity of a population can be assessed with ge-
as is the case for canine hip dysplasia. In more detail, for canine hip netic markers or based on pedigree data. At a relatively low cost,
dysplasia, diseased animals were omitted from the database, hence genetic markers can be used in the absence of pedigree data and are
the problem is underestimated and the cut-off is set too high at hips not susceptible to pedigree errors [4,11,32]. They can however be
that have to be too good. Whereas this might result in a higher biased when for example only a small number of animals and/or
response for the phenotype under study at the population level, at markers are genotyped [4,33].
the same time, the selection might be that strong that it actually As a prerequisite for a successful breeding program is that ani-
results in the population being forced through a population mal records (including ancestry) are kept thoroughly, all informa-
bottleneck with the associated negative consequences. tion should be available to immediately assess genetic diversity
The converse is also possible: a database which contains too based on genealogical data. It is however clear what the potential
many diseased animals relative to the truth might result in an downsides are of this method: pedigree errors have to be avoided
overestimation of the problem, a biased cut-off set too low, a se- at all cost and a lack of knowledge on ancestry might bias the re-
lection pressure that is lower than expected and, as such, a slower sults [4,11]. On a side note, paternity testing (using the same
response to selection for the entire population. An example is markers to calculate genetic diversity) can be used to assess
canine hip dysplasia prevalence estimates based on an orthopaedic ancestry and correct pedigree errors.
clinic for which is it very likely that they mostly see animals with A correct assessment of the genetic diversity is important to
clinical problems [28]. A worked-out example of both situations is determine the starting point, but even more to evaluate how it
detailed in Fig. 1. 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 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
Fig. 2. The consequences on population size (x-axis) of three different breeder been developed that might help to prioritize disorders. Part of the
strategies to deal with DNA-test results for recessive diseases. The breeder strategy
actions undertaken after the release of Pedigree Dogs Exposed, the
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, Generic Illness Severity Index for Dogs (GISID) was developed. For
on the genetic diversity). This is illustrated by subsequently performing two DNA-tests every disease, the GISID tries to numerically value prognosis,
for the autosomal recessive diseases exercise-induced collapse (EIC) and a specific type treatment, complications and how it affects behaviour to get to a
of progressive retinal atrophy, i.e. progressive rod cone degeneration (PRCD), based on
disease-specific overall score from zero to 16 [19,20]. Combining
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
this with prevalence estimates and disease-duration, a welfare-
is excluded is depicted in dark grey. The first strategy involves excluding all dogs that index that ranges between zero and 100 can be calculated for
are hetero- or homozygous for the disease-causing mutation (a). After two tests, only each disorder at the population level with higher values being
55% of the original population remains. The second strategy involves excluding only associated with a more severe impact on the welfare of the dog
the dogs that are homozygous for the disease-causing mutation (i.e. the genetically
[37]. An example based on hip and elbow dysplasia demonstrates
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 that the former is associated with a higher welfare-index and
specific combinations to make sure that no genetically affected dogs are born. Using should receive a higher priority (Table 1). An alternative score for
this strategy, not a single dog is excluded and the frequency of genetically affected dogs working dogs, the so-called work score, was developed specifically
(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 If that would be the case, the second strategy or a combination of strategy two or three
dogs for breeding does not result in a reduced welfare for the dogs itself or the puppy. 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) genotype and the phenotype has already been established for that
working life into account [38]. This and another study also specific breed. If mutations associated with disease are detected in
demonstrate again the importance of a broad view which is not a breed where it was not previously reported, this might indeed
limited to diseases sensu stricto as behavioural rejections are at the indicate that the phenotype is also segregating in that breed [9].
top of the list [22,38]. 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
4.6. Breeding strategies implementation of novel DNA-tests in breeding programs should
always be considered carefully while it is also the responsibility of
4.6.1. DNA-tests the scientific community to keep a watchful eye.
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
4.6.2. Test matings and pedigree analysis
only expressed when dogs undergo strenuous exercise (e.g.
Unfortunately, for quite some Mendelian diseases, a genetic test
exercise-induced collapse) and might remain phenotypically un-
is not (yet) available. At that moment, one has the option to perform
detected as such [39,40]. With DNA-tests for autosomal recessive
test matings [10]. A downside is that it is based on deliberately
disorders, carriers can easily be identified and basically any dog can
trying to create dogs affected by the disorders, which is ethically
still be used for breeding, if carriers and genetically affected dogs
debatable. Furthermore, it takes quite some time to get the result,
are combined with dogs free from the mutation [29,41]. It goes
i.e. the time between conception and normal onset of the symp-
without saying that this is a big advantage, especially in those
toms, which can be long for some phenotypes. Finally, it is impor-
populations where the genetic diversity is dangerously low, as
tant to realize that one can never prove that an animal is
illustrated in Fig. 2. A remark is that a dog homozygous for a
homozygous normal from test matings: the absence of progeny
recessive disease-causing variant should only be mated (with a dog
with disease can also be due to coincidence. As such, it is only with
homozygous for the normal allele) when it does not negatively
a certain probability that one can state that an individual is free and
influence the welfare of that individual dog or its puppies. As a
this probability of being normal increases when the number of
practical example, given the late age-of-onset of degenerative
offspring increases. A more theoretical approach, based on a known
myelopathy (more than five years of age), a young dog (e.g. two to
mode of inheritance and pedigree data, involves the calculation of
four years of age) homozygous for the disease-causing mutation,
the probability that a prospective parent is homozygous for the
can still be included in the breeding program if the dog is symptom
wild type allele. In the next step, one can retain those individuals
free and does not have any other debilitating disease [42].
that have the lowest probability of having an undesired genotype
Three precautionary remarks should be made. The advantage of
[10]. While this can be quite complex mathematically, commercial
not having to exclude an animal is unfortunately less present for
software is available to solve this problem [10].
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 4.6.3. Estimated breeding values
point of consideration. Not every DNA-test that is commercially The complexity of multifactorial disorders is illustrated by the
available is indisputable and upon validation, sometimes even fact that each phenotype is the sum of the combined effect of ge-
opposite associations between genotypes and phenotypes have netic determinants and environmental influences. The fact that the
been observed [43e45]. This might be the case when a variant is phenotype is blurred makes it difficult to select the “best” dogs. As
not the causal one but for example a marker allele that is linked to a the true (breeding) value of an individual dog is unknown, we can
causal allele. Upon recombination, the initial association can be estimate it based on own performance and (close and/or distant)
reversed at that moment [10]. It might also be a consequence of family members, with all information weighted depending on the
erroneous associations due to for example population stratification relation with that dog, which results in “estimated breeding values”
[46]. A thorough literature check to evaluate the evidence that (EBVs) [10,48,49]. The more information from relatives that is
supports the association is important, together with consulting added in the equations, the more accurate these EBVs are. Instead of
genetic experts. Thirdly, there is an increasing trend to simulta- selecting the animal based on its own performance alone (the so-
neously perform DNA-tests for a wide range of diseases [9]. In called “mass selection”), EBVs employed correctly allow a far
terms of cost, it might indeed be cheaper to order such a test faster progress, as recently again demonstrated for e.g. canine hip
compared to performing several individual tests. It is however not dysplasia in a guide dog population [49]. An additional advantage is
necessarily guaranteed that the “omnibus” tests assess every dis- that when selection is to be applied on more than one phenotype,
ease important for that specific breed. Furthermore, tests are often EBVs can be combined into a selection index allowing simultaneous
performed irrespective of whether the association between the selection [15].
 B.J.G. Broeckx / Theriogenology 150 (2020) 20e26 25

4.6.4. Disorders related to breed standards contribute to future generations tailored to the population-specific
Special attention should be given to disorders directly or indi- situation [55]. Finally, whenever several dogs meet the selection
rectly related to the breed standards. Examples are numerous and criteria for breeding, it is best to combine those dogs that are the
include the association between the dorsal hair ridge and dermoid least related [15,36].
sinus in the Rhodesian Ridgeback, brachycephalic obstructive Taking the effective population size cut-offs mentioned earlier
airway syndrome in brachycephalic dogs and deafness and patch- into account, it is clear that relatively small breeding programs are
ing in the Dalmatian [19,50e53]. Whereas unwanted phenotypes possible, but only when performed in collaboration with other
not linked to the breed standard can be selected against within the breeding programs. Luckily, advances like artificial insemination
context of ethical breeding, this is far more difficult when a make the (inter)national exchange of genetic material far more
phenotype is directly related to the actual breed standard. At that easy.
moment, there is a direct conflict between that what makes an
animal “true to their species” (or breed, in this case) and the 5. Concluding remarks
remainder of the definition where health and welfare are central.
Luckily, health and welfare seem to outweigh the former, with the It is clear that only a subset of the techniques currently available
recommendation to revise breed standards if they compromise have been described here. The reason to focus on these techniques
either of those two [1,37]. is that they provide solutions for all kinds of phenotypes, ranging
Some work still needs to be done however. Just one example is from a Mendelian to a complex mode of inheritance, and that all
the ridge from the Rhodesian Ridgeback mentioned earlier on. these techniques are feasible as they only require solid record
Although a clear association has been found between the ridge and keeping which is either way a prerequisite when one wants to set
dermoid sinus, the ridge is still part of the breed standard,1.2 In up an at least reasonably sized breeding program with a clear di-
more detail, a 133-kb duplication segregated perfectly with the rection. In the future, it is likely that more DNA-based techniques
ridge with an autosomal dominant inheritance pattern [52]. At the will be employed with genomic selection being the most well-
same time, the dermoid sinus also only occurred in dogs that were known example already widely implemented in production ani-
hetero- or homozygous for this duplication [52]. As a dermoid sinus mals [56e58].
can result in significant disease (associated with a score of up to 14 Overall, it should be clear that certain concerns regarding dog
out of a maximum score of 16 according to GISID) and a solution is breeding are justified. It is however way too easy to just dismiss
easy (avoid breeding dogs with a ridge), there still seems room for (pedigree) dog breeding as bad for welfare. Instead, an individual
improvement [19]. For this specific case, this improvement means breed-specific approach is of paramount importance. Where the
altering the breed standard towards breeding Rhodesian Ridge- focus should lie entirely on increasing genetic diversity in one
backs without ridges. population, other populations can focus far more on selection to-
wards prespecified breeding goals and, luckily, there are good tools
4.6.5. Strategic choices to increase the diversity to solve each of these problems. The word “prespecified” is critical
To achieve the breeding goals, selection pressure in the desired in the previous sentence: it stresses the importance of thinking
direction should be applied. At the same time, genetic diversity ahead, but also on a collaboration to define these breeding goals
should be maximized (or conversely, the rate of increase of and openness between all stakeholders to identify the issues at
inbreeding each generation should be minimized) as much as hand. The approach described here should aid in achieving these
possible as it is the basis of a healthy population [11,15]. There are goals.
several approaches that can be used to achieve this and they can all
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