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Puppies from a breed cross will have the health problems of both breeds: T or F?

3/22/2022

 
By Carol Beuchat PhD
I keep seeing the statement in the title, usually in the context of a discussion about the need to improve genetic diversity of a breed with a cross-breeding program.

The people that say this reveal their poor understanding some basic principles of genetics that should be elementary level stuff for every dog breeder. But apparently not. This statement is false, and here's why.
Most of the hundreds of genetic disorders identified in dogs are caused by single, recessive mutations. A dog with one copy of the normal allele and one copy of the mutation will usually be unaffected and healthy. A dog that inherits two copies of the mutation will not, of course, have a copy of the normal allele, so whatever that gene is supposed to do in the body isn't going to happen. It will either be apparent as a disorder of some sort, or it will not be evident at all if the effects are subtle or do something like reduce fertility, or slow down some enzymatic reaction, or slow growth rate. But apparent or not, it can be expected that if a dog gets two copies of a mutation, there will be some sort of functional deficit.​
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​Of course, not all mutations are recessive, but problems caused by dominant genes are easily managed by removing the carrier from the breeding population. The action of a gene can also be affected by the mix of genes in the genome of that particular dog (i.e., polygenic). How these genes affect the health of a dog can be complex and unpredictable, but in dogs polygenic disorders are 
far outnumbered by the problems caused by simple recessives. 

So, let's just consider the case of the simple recessive mutation.
Most breeds do not share mutations (Donner et al 2018). That is, mutations tend to be breed specific either due to founder effect or because they occurred after a breed split away from the ancestral dogs from which it was developed. A dog of breed A might be homozygous and affected by a recessive mutation, but when crossed to breed B will likely produce offspring that are heterozygous. Because of this, the offspring will not be affected by the disease. In fact, the puppies produced by a cross breeding should be expected to be unaffected by any of the disorders of either parent that are caused by recessive mutations. This of course assumes that the two breeds being crossed are not so closely related that they could share some mutations because of a common origin.
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A "borgi", offspring of a Corgi x Boxer cross. (Cattanach)
Now, the offspring of Breed A x Breed B will inherit some of the mutations of both parent breeds. Doesn't this make the offspring worse off than the parents if it carries mutations from both parents? Remember that recessive mutations are only expressed if an animal inherits two copies. The way to prevent mutations from becoming a problem, regardless of origin, is to breed in a way that keeps the risk of a puppy inheriting two copies as low as possible. What does that mean? Related dogs will share some mutations, and the closer the relationship, the more mutations could be shared. To avoid the risk of producing affected puppies, just avoid breeding closely related dogs. You might say that we can do DNA tests to avoid this problem, but in fact we can't. We can only test for the mutations that we know about and have a test for. What about all those other mutations lurking in the dogs that we can't detect? The risk of problems from them is also proportional to the relatedness of the parents. If you have DNA tests for both parents and they do not share mutations, you nevertheless embrace a risk of producing a genetic disorder if the sire and dam are related. If you want to avoid problems from recessive mutations, don't breed closely related dogs.
The fact that different breeds rarely share the same mutations is also the reason why mixed breed dogs are, on average, healthier than purebred dogs. While they might carry more mutations, those mutations are much less likely to be homozygous and therefore be expressed as disease (Donner et al 2018).

​The offspring of a cross breeding will produce offspring that will carry some of those mutations. If those dogs do lots of breeding, they will produce many copies of those mutations packaged in puppies that will enter the breeding population. The way to keep those mutations from being a problem, is to not make hundreds of copies and distribute them throughout the population. Keep them few and rare by nixing those popular sires.
The answer to the question in the title is "false". Make sure you understand the explanations, and next time somebody makes this claim, call them out. The statement is usually made to derail a discussion about how breeders should deal with high levels of inbreeding in their breed. Definitely you should have the discussion, but make sure everybody is armed with facts and a decent understanding of the relevant genetics.

For that matter, tackle the folks that claim that mixed breed dogs are not - and should not be - healthier than purebreds. If we get rid of all the problems caused by recessive mutations, then maybe. But in fact, from the simple facts of genetics, mixed breed dogs are less likely to suffer from disorders caused by recessive mutations than purebreds. Believe in genetics; the world will make so much more sense.

REFERENCES

Donner J and others. 2018. Frequency and distribution of 152 disease variants in over 100,000 mixed breed and purebred dogs. PLoS Genetics  14(4): e1007361.  DOI: 10.1371/journal.pgen.1007361

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Do you know what you need to save your breed?

3/20/2022

 
By Carol Beuchat PhD
​I asked the members of my ICB Breeding for the Future Facebook group to rate their understanding of genetic management and that of the people in their breed.

Like the folks that live in the mythical town of Lake Wobegon, where everyone is “above average”, most people responded to the "Rate Yourself" post with a score of 3 or more on a scale of 1 to 5. And pretty much everybody said that the overall level of understanding of the people in their breed was low (lots of 1s for this).
 
The latter response is very worrisome. Here’s why.
 
 Find your breed on this graph, which is the genomic (from DNA) inbreeding of a large number of purebred dog breeds. These data are consistent with data from several other studies of different populations, so we can assume that this is a fair representation of inbreeding in these breeds.
 
The green line is inbreeding of 6.25% (mating of first cousins), yellow is 12.5% (mating of half sibs), and red is 25% (full-sib mating). (I made this graph to highlight the data for Cavaliers for another post; the black line at about 41% is the average inbreeding of this breed.)
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If your breed’s average inbreeding is 25%, that means that, on average, the parents of a litter are as genetically similar as full siblings, even if they appear to be relatively unrelated on pedigrees. Most breeders would not breed littermates together. Yet, in many breeds, the typical sire and dam are more closely related than this.
 
Inbreeding in dogs is FAR higher than in any other mammal, wild or domestic. Inbreeding of wild animal populations is usually in the very low single digits. Breeders of livestock begin to panic as inbreeding approaches 10% because the negative effects are so significant. In fact, they worry about every percentage point of increase; on this chart, the livestock people are wringing hands because "in all three breeds the inbreeding coefficients are the highest they have ever been," and they haven't even cracked 10% yet. 
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Think about this. You cannot "breed for health" when levels of inbreeding are higher than about 5%, because above this the negative consequences and risk of genetic disorders increases linearly with inbreeding. In a closed gene pool, inbreeding can ONLY increase over generations, and the gene pool can ONLY get smaller. So, despite the best efforts of breeders to improve health, the quality of the gene pool deteriorates inexorably over time, as alleles that were in the gene pool 50 years ago, or 10 years ago, or even in the last generation, are lost to the breed.
​This means that, because of the facts of basic genetics, you cannot “preserve” a breed in a closed gene pool. You might breed in a way that attempts to limit the damage to the gene pool, but you cannot preserve a breed if alleles necessary for function and health are lost from the gene pool every generation. You can be a “responsible” breeder," and make choices that attempt to limit the damage, but you cannot be a ”preservation” breeder, not when more genes necessary for the body to function are being lost every generation. 

Can we at least say that we are breeding responsibly, i.e., making breeding decisions that will limit the damage to a breed’s gene pool? Let’s look at some data.

These graphs are from Lewis et al (2015) and are based on the pedigree records of the UK Kennel Club. Note that the data were not digitized before 1980, so the graphs start there, and the COIs are much lower than actual values because the ancestors from 1980 back to founders are not included in the calculation. Also, ban on importing dogs into the UK was lifted in 2000, and the incomplete pedigree data for those dogs make it look like the average population inbreeding is going down after that, which is probably not the case.

The blue line is the average COI computed from the pedigree data. The red line is the level of inbreeding that would be expected if the dogs in the population were breeding randomly. If breeders were making a strong effort to avoid inbreeding, the blue line would be below the red line; if breeders are preferentially breeding dogs that are more closely related than average, the blue line would be above the red line. 

These graphs tell us about the overall breeding strategies being used in each breed. Breeders are preferentially inbreeding. (I have grabbed a few of the breeds that have a population large enough to show a trend instead of a line that goes all over the place.)

The name of each breed is on the gray bar at the top.
(Graphs from Lewis et al 2015, Additional Files)
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We want to preserve breeds. We want to produce healthy, long-lived dogs. But look at the data. How are we going to do this?

In response to the ban on breeding Cavaliers and Bulldogs in Norway, the clubs have responded that the breeders are in the best position to solve the problems and are working hard to do this. But inbreeding will continue because it is unavoidable in a closed gene pool. DNA testing can prevent disorders caused by a single, recessive mutation for which we have a test, but we do nothing to control the many other recessive mutations we know are lurking in the gene pool, and selection is doing a poor job of managing the problems that are likely polygenic. Plus, we are preferentially inbreeding, increasing the risk of producing genetic disorders from mutations we don't yet know about.

I noted up at the top that, in a survey of the people in my Facebook group, ICB Breeding for the Future, most people rated their understanding of the principles of genetic management and breeding for health at a 3 or higher on a scale of 1-5, where 5 is highest. They also overwhelmingly rated the average understanding of the people in their breed at 1. 

If we want to have purebred dogs, we need to solve some serious problems, we need to get it right the first time, and we need to do it soon. The kennel clubs say “We can do this,” but breeders assess the general level of genetic management expertise of their colleagues as rock bottom. 
 
I can probably count on one hand the number of dog breeders I know that have enough expertise in population genetics to “know what they don’t know,” and all of those people are professional scientists that happen to also breed dogs. Beyond that, there is an army of “Facebook experts” - people that might know something about little bits of a topic but dispense advice as if expert. Invariably, they say things that are incorrect, because they don’t know enough to appreciate the nuances, complications, and depth of concepts. They don’t know what they don’t know, and most people don't know the difference. These experts don’t do any topical coursework (e.g., I don't see them in ICBs online courses for breeders), and they usually have no background in science at all. What they “know” has mostly come from things they read on Facebook written by other people with no expertise. 

If you are tackling a very difficult problem, and if getting it wrong could result in catastrophe, these Facebook experts are extremely dangerous. Most breeders in my survey judged the expertise in their own breed as very poor. Most probably wouldn’t know good advice from bad; they are likely to be most swayed by things that sound “logical” or “make sense”. But their perspective is on managing the genetics of individual dogs. The genetics of populations are quite different, and indeed “the right thing to do” can often be counter-intuitive. You’ve heard that you should only “breed the best to the best”, but this will actually make it harder to improve traits and will ultimately lead to extinction of the population. In fact, this is why we are in this difficult spot, and continuing to use this breeding strategy is the hammer that will sink the last of the nails into the coffin. This is not an opinion; this is a necessary consequence of the mathematics behind population genetics. If you don't know this, then the "best to the best" advice seems like a good thing to do. But it's not.

The Norwegian kennel and breed clubs argue that they can fix the health problem of Cavaliers and Bulldogs by continuing to do the things they think will work. They haven’t worked so far, and they won’t. But apparently they don’t know that.

The Norwegian court offered that crossbreeding to solve the health issues would be allowed, but the feedback on Facebook has been adamantly opposed to even considering cross breeding programs. So, if the Norwegians have a plan to fix this without crossbreeding, I would like to hear how they will do it. 

The breeds in the spotlight in Norway have to come up with a plan to address the issues that put them in violation of the Norwegian Animal Welfare Act. The Norwegians are on the hot seat right now, but every breed has an inbreeding problem that is incompatible with sustainable breeding, incompatible with “preservation” breeding, and incompatible with health. What breeds have a plan to address their growing list of genetic health issues, which will only continue to grow? How will they know if their plan will work? What will they do if it doesn’t?
Purebred dog lovers face two huge challenges. First, we must fix the significant inbreeding problem that imperils  essentially every breed.

Then, once we have inbreeding down to a reasonable level, we need to breed sustainably, which means we have to  control inbreeding and loss of genetic diversity. To do this, breeders will need to understand population genetics, which provides the tools used for the genetic management of animal populations.

Are you thinking you already know a lot about population genetics? Among the essential topics you should be able to explain and discuss are these, for example: linkage disequilibrium, founder genome equivalents, effective population size, the Hardy-Weinberg equation, heritability, fitness, mean average kinship, observed and expected heterozygosity, and genetic drift.
If these terms don't trip off your tongue, if you you are not confident that you could easily explain them, then you won't be able to follow the discussion and rationale of the breeding plans your breed will need to follow. To be fair, these are not terms the average dog breeder would ever run into in general discussions about breeding. People don't usually sit around the ring discussing the effective number of founders of their breed. Even if you have a degree in biology, most of these terms would be unfamiliar. So these will probably be unfamiliar to you and your fellow breeders. But if you want to be part of implementing a breeding program to improve the health of your breed, the sooner you work on building a sound understanding of population genetics, the better. 
There aren't many ways for breeders to learn population genetics, which is mostly advanced topics based on mathematics. When I was unable to point breeders towards a resource for learning about population genetics at a basic but useful level, I created some online courses specifically for dog breeders with no background in science. While I realize this looks self-serving, it really is the only option available to dog breeders without a degree in biology. Find the time to invest in education; the payoff will be immediate and continue for as long as you breed. Be an education advocate within your breed; you and your fellow breeders all must share a single gene pool, and breeders won't support a breeding strategy they don't understand.

The next ICB course for dog breeders about genetic management is "Strategies for Preservation Breeding," which starts 1 July 2022. Register now!


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LEARN MORE

REFERENCES

Bannasch E et al 2021. The effect of inbreeding, body size and morphology on health in dog breeds. Canine Medicine and Genetics 8:12. 
doi.org/10.1186/s40575-021-00111-4

Lewis et al 2015. Trends in genetic diversity for all Kennel Club registered pedigree dog breeds. Canine Genetics & Epidemiology 2:13. DOI:10.1186/s40575-015-0027-4

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The genetic status of the Cavalier King Charles Spaniel (part 1)

3/4/2022

 
By Carol Beuchat PhD
In an earlier post, I noted that the level of inbreeding in Cavaliers is roughly 40%, as reported in two independent studies. Remember that puppies produced by cross of first cousins will have expected inbreeding of 6.25%, a cross of half siblings produces offspring with an average of 12.5% inbreeding, and a full-sib cross results in 25% inbreeding. For Cavaliers with average inbreeding of 40%, this means that, on average, the parents of a litter are more closely related than littermates. On the chart in that previous blog post, the green line is at 6.25%, yellow is 12.5%, and red is 25%. The black line is the average level of inbreeding in Cavaliers (about 41%). 

I have copied below the high end of the breed rankings from the chart from my previous Cavalier ​post. You can see where Cavaliers sit relative to the other breeds with the highest levels of inbreeding. Note that inbreeding in the King Charles Spaniel (aka English Toy Spaniel) is essentially the same as in CKCS (43%). ​
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Please join our Facebook group about the genetics of the CKCS HERE.
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The inbreeding coefficient reflects the homozygosity that results from breeding together related dogs. Because relatives share some of the same genes, breeding related dogs will result in inheritance of two copies of the same allele for some loci; i.e., a particular locus on the chromosome will have two copies of the same allele, one inherited from each parent. As a result, all of a dog's offspring will inherit the same allele from all loci that are homozygous. As I pointed out in my earlier post, effective selection requires genetic diversity; homozygosity reduces the genetic variation available to breeders for selective breeding, limiting their ability to make choices that will improve quality and health. 
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One basic measure of the health of a breed is the size of the population. Large populations are likely to have more genetic variation than small ones (but not always!), and the large number of individuals buffers the population to rapid genetic changes.. This graph shows data for registrations by the UK Kennel Club from founding (1945) to the present. My data for AKC registrations are limited, but I have included them here for information.

The data for the UK Cavaliers reveal details about the history of the breed in that country. The population size increased after it was recognized by the Kennel Club, slowly at first, then very rapidly from about 1970 to 1989, when yearly registrations reached 15,833. From 1990, registrations have generally decreased through about 2010, and since then the decline has been steady and steep. In 2020, 2,967 dogs were registered, a level not seen in the breed since about 1970, a half century ago.

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​There is no indication in these data that the rate of decline in the yearly registrations is slowing. In fact, the trajectory of the line reaches zero in about 2030 (the dashed blue line in the figure below). This projected decline should be a matter of concern to breeders, especially as this is the country of origin of the breed. Smaller populations are genetically less stable, and the risk of inadvertently losing genetic diversity from lines that die out is high.

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One concern about a declining population is loss of genetic diversity. This can be mitigated if breeders are careful to avoid inbreeding and they balance breeding across the population.  

The graph below displays the observed level of inbreeding in the UK breed population between 1980 and 2015 (in blue). The red, fuzzy line is the expected level of inbreeding in this population if the animals were breeding randomly over the same period of time. The pedigree database for this analysis (which is from Lewis et al 2015) only extends back to 1980, when digital records began. While this graph is useful to detect patterns in inbreeding levels in the breed population over time, the levels of inbreeding on the graph are much lower than what we know to be more accurate inbreeding from DNA analysis, which, as noted above, currently average about 41%

On this graph, if the observed level of inbreeding is higher than the inbreeding expected from random breeding, this indicates that breeders are preferentially inbreeding; i.e., choosing to pair dogs that are more closely related to each other than the average level of relatedness in the population. This also reveals that breeders could be producing puppies with lower levels of inbreeding by pairing individuals that are less closely related.

Note on the graph that the mean inbreeding coefficient decreases after 2000. This is the result of dogs imported after the restrictions to imports were lifted in the UK in 2000. These dogs have only three generations of ancestry in the UK pedigree database, so offspring they produce will appear to be much less inbred than they really are. Remember - in a closed population, the average level of inbreeding can ONLY increase over time. 

(These data are from Lewis et al 2015, and are slightly different from the registration records I have.) 
​
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Inbreeding results from mating related dogs. Nothing can damage the genetic health of a population faster and more dramatically than a popular sire. This is a dog that produces a disproportionate number of offspring, populating the breed with a large number of offspring that all share half of his genes; i.e., they are all half-siblings. But, just like every other dog, the popular sire carries unknown mutations, and these will invariably result in a genetic defect a few generations down the road. Not all of these defects will be apparent to breeders; mutations that reduce fertility, shorten lifespan, or affect behavior are just a few examples of the ways these unidentified mutations can burden the health of the breed. 

​As in most breeds, the CKCS has popular sires that produce more than their fair share of offspring. These tables show that the most prolific sire in 2020 produced 30% more litters than the next most prolific sire, and 100% more than the dogs ranked 3 through 5. In terms of lifetime contribution, the top sire in 2020 produced twice as many litters as the second  ranked dog (111 vs 60). To understand the true consequences of popular sires on the genetics of a population see my article The Pox of Popular Sires. 

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This chart also reveals the impact of the most popular sires in the breed. For instance, the top 5% of sires produce on average about 20% of the puppies in each year. Likewise, the top 50% of sires produce about 80% of the puppies, so the lower 50% of sires account for only 20% of the puppies.
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Relating to the unbalanced use of sires is the tendency to restrict breeding of sires more than dams. This is revealed in this graph of the number of sires and dams producing the puppies of a particular year. In recent years, the number of females producing litters in a year has declined dramatically, which probably reflects at least in part the decline in the size of the population. The number of males producing litters has been relatively stable for most of the last 30 years, but in the last decade has been falling.
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With the exception of the first graph, which includes data for AKC registrations for a few years, the data analyzed here are from the registry of the UK Kennel Club. However, this breed is popular in many countries in the world, and we cannot assess the true genetic status of the breed without including those data (or as much as possible) as well. If you have access to data for other countries, please contact me so I can incorporate them in these analyses. 

This is the first of what will be multiple installments that will shed some light on the genetic status of the Cavalier King Charles Spaniel. This information is essential to understand the history of the breed, and is even more critical or sound genetic management into the future. There are a few things already evident here that breeders should consider, perhaps most importantly, the declining registrations in the UK. As the country of origin, a healthy representation of the breed in the country has cultural importance. 
Related to questions about my previous Cavalier post, I still do not have the data necessary to determine the original size of the gene pool of the breed. I am chasing down ancestors and trying to connect ancestors, and I will let you know when have an estimate. 

Stay tuned - part 2 is coming soon!

REFERENCES

Lewis et al 2015. Trends in genetic diversity for all Kennel Club registered pedigree dog breeds. Canine Genetics & Epidemiology 2:13. DOI:10.1186/s40575-015-0027-4

To learn more about the genetics of dogs, check out
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