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  • Preventing Uterine Inertia

Hitting the bottle: the genetics of boom and bust

12/17/2014

 
By Carol Beuchat PhD

Every breed has a history that has shaped the population of dogs we have today. For breeds recognized by kennel clubs, some number of animals were selected to be the founders of the "pure breed" and registered in a stud book. All subsequent members of the breed must be able to trace their lineage directly to these original dogs, and this is assured by the requirement that only dogs with registered parents can be registered themselves. The nice thing about this is that we should have very complete records of a breed's history that can be used to understand how a breed has changed genetically over time. (In fact, there are surprisingly few complete pedigree databases that are publicly available, much to the detriment of effective management of the  breed. A topic for another day...)

One of the first things we do at the Institute of Canine Biology as part of the genetic analysis of a breed is look at how the population has changed over time. (You can see several of these ongoing analyses under "Breed Projects" on the ICB website.) They are always very revealing and often there are some real surprises.
These are data (see graph below) for the number of Afghan Hounds born per year from the early 1920's to the present day from ICB's analysis of the breed's pedigree database. In the early years, a few hundred dogs were registered per year, with occasional increases and decreases in popularity through the 1950s. In 1957, an Afghan Hound, Ch Shirkhan of Grandeur, won best in show at Westminster, and - coincidence or otherwise - the popularity of the breed exploded. In 1960, there were about 1,000 registrations per year, in 1970 it had risen to 5,500/yr, and in 1975 it was close to 12,000/yr.  Registrations didn't double, or even triple, in those 15 years -they increased by twelve-fold.

Then, even more rapidly than they increased, Afghan registrations dropped, to about 5,000/yr by 1980 and half that by 1990.  Over a period of just 30 years, the breed experienced a boom and bust of truly epic proportions.
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The domestic Afghan was never bred to be a working dog. It was a lovely bauble, prized for its beauty and noble demeanor. So when the population exploded, it was no doubt the "best" dogs that did most of the breeding, rather than a representative cross-section of the dogs in the gene pool at that time. And when the population crashed, it probably wasn't with the foresight of assuring that breadth of the gene pool be preserved.

You've probably heard about founder effects, popular sires, and bottlenecks. A few popular dogs become overrepresented on the increase, and less popular lines die out on the downslide.  These dramatic swings in the size of a population can wreak havoc on genetics.

When a population grows by balancing the contributions of all of the dogs to the next generation, the frequency of alleles in the gene pool stays about the same as it grows. But if there is selection on a particular feature, or a popular sire, the genetic balance of the gene pool will shift, with the frequencies of some alleles increasing while other alleles become rare or are lost entirely. The nature of the gene pool of the population at the peak of its growth can be dramatically different than it was before the surge in popularity.
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From the height of the Afghan hound's popularity, breeding dropped dramatically. Only a fraction of the available dogs were bred, so the genes of some dogs were carried on but many were not. It's as if you reached into a large bowl of Jelly Bellies, selected 8 at random, and replicated just those to create a new bowl of candy. Chances are that new bowl is missing a lot of the great flavors in the original mix, so the population of beans in the new bowl will look very different from the one it was sampled from.
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Lest you think that the history of the Afghan Hound is unusual, there are plenty of other examples of breeds that have very similar histories. The Standard Poodle also has an interesting story. From its early history in the late 1800's, it gradually increased in popularity until the start of WWI, when the population dropped by about 70% (from the ICB Poodle analysis). After the war there was a resurgence of popularity until WWII when once again there was a decrease in breeding. After that, however, things really picked up and the number of dogs produced per year quadrupled in the three decades between the mid-1940s to the 1970s. That's a pretty impressive increase in popularity as you can see in this graph, but it pales in comparison to the explosion in growth that followed.
This is a bottleneck as the population crashes, followed by the founder effect as the population subsequently carries on from that subsample of its original gene pool. This is what happened in Afghans. There is clear evidence that the changes in population size of the breed were unbalanced genetically. Over the history of the breed, only about 25% of the dogs were bred (19% of males and 32% of females), which is typical of many breeds. This is like a little hole in the bottom of a bucket; you're slowly losing water, but not so fast that you can't ignore it if you're busy with other things. But for Afghans, the hole is getting bigger; for the period 2005-2013, 12,000 dogs were recorded in our pedigree database, but only 1,200 have produced offspring. That's barely 10% of the population. With every passing generation, the breed's genetic pantry - in fact, its heritage - is slipping away. A full 90% of the dogs being bred will pass nothing on to the next generation. (Note that we don't have a "complete" database for this and many other breeds. In the absence of cooperation from Kennel Clubs in making their registration records freely available, breeders have taken on the onerous task of constructing databases by hand, and complete or not these are what we have to work with.)

One thing that's important to remember is that the larger the swings in population size, and the faster they occur, the more dramatic the consequences can be for the gene pool. A gradual increase in population size is more likely to include a broader mix of animals, and likewise for a slower decline. Explosive growth and rapid crashes can change the composition of the gene pool dramatically.
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The axes on the graph below are difficult to read so I've labeled some strategic points for you. First, the spot marked "1970", is the rightmost end of the axis on the graph above - that is, the graph above of the dramatic population explosion before 1970 is just a few little bumps in the same years of the graph below. Beginning in about 1970, the number of poodles produced went from about 1,000/yr to 8,000/yr only 35 years later in 2005. Just as in Afghans, however, the peak in Poodle popularity might now be waning, as registrations appear to be dropping dramatically in the last 10 years. This might reflect incomplete data in the most recent years, and time will tell. But if this drop in popularity is real, we know there will be repercussions for the gene pool. The danger of losing less common lines as the population contracts is very real.
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Those familiar with Poodles know that tucked into the pages of the breed's history is a bottleneck caused by the sensational Wycliffe poodles of the late 1950s and 1960s. (Armstrong gives an excellent summary of the impact of this period on the genetics of the breed in a collection of papers here.) The impact of these dogs on the breed is so huge that nearly every poodle in the world has a pedigree that goes back to those dogs. The effect on today's dogs is obvious. One of the famous dogs of this era, Annsown Gay Knight of Arhill, is indicated by the arrow in the pedigree below of a contemporary dog, and all of his subsequent descendants are in red. Half of the breed - the dogs that should have been populating the left side of this chart - just slipped out of the gene pool and disappeared as breeders rushed to the Wycliffe lines. The unfortunate consequence is predictable; much genetic diversity was lost and the average level of inbreeding is relatively high, and the breed now suffers increasingly from genetic disorders and especially autoimmune diseases. Poodle breeders contemplating a potential breeding not only compute the coefficient of inbreeding, but also "% Wycliffe", as they try to reduce the predominance of these dogs and their descendants in their puppies. Ongoing DNA studies at UC Davis are are establishing the patterns of genetic structure in the breed, including the DLA haplotypes (the genes of the immune system), so that breeders can take advantage of the existing genetic diversity in the breed to reduce the level of inbreeding and improve the heterozygosity of genes in the immune system. The breed's large population size and global distribution make constructing its genetic landscape difficult, but they also make it more likely that pockets of genetic diversity do exist that can be used strategically by breeders to improve the genetic health of the breed. If the popularity of the breed is falling as suggested by the available data, these efforts could not be more timely.
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Pedigree chart of a contemporary poodle, which is the single box at the top. The base of the pedigree is at the bottom. Annsown Gay Knight of Arhill is indicated by the arrow and all of his descendants are colored in red.
If we dig into their histories, we would find that many dog breeds have surges in popularity like the ones we've seen in Afghans and Standard Poodles. Changes in hunting styles that resulted from improvements in guns fueled surging populations of retrievers who could fetch birds shot on the wing. Overland fox hunting on horseback as (mostly) sport required large packs of hounds of various shapes and sizes. Development of rocky farmlands in the British Isles produced an array of terrier breeds suited to digging out vermin in the cairns, and larger terriers were developed to dispatch the badger and fox. Military dogs to assist in the tasks of war popularized the Doberman and German Shepherd. Popular culture transformed 121 Dalmatians the movie into a lovefest that put Dalmatians in thousands of homes in suburban America, far from the nearest horse-drawn fire wagon. Similarly, Lassie transformed a working breed into every boy's companion. The popularity of Mexican food and Chihuahuas rose together in the southwest US, thanks to a certain fast-food chain, and a fascination with wrinkles made the Shar Pei the unlikely cover shot on hundreds of gift cards and calendars. 

For these and many other breeds, explosive surges in population size are usually followed sooner or later by a fall that can be equally dramatic, and the gene pool we're left with isn't the same as the one we started with. The dogs might look the same, because we have been carefully selecting for the genes for type, but the reservoir of genes that run the rest of the dog - physiology, immune system, organ function, temperament - can be only a tiny subset of what we had before. Today's breeders, trying to use the husbandry methods handed down from generations of dog breeders, find themselves in genetic cul-de-sacs from which there seems to be no escape, or engaged in a game of genetic whack-a-mole, defeating one nasty recessive mutation only to have another pop up in what was thought to be a "healthy" line.

For most breeds, It's not your grandpa's gene pool any more. Like the cheetah and Przewalski's horse, the populations might appear robust and healthy, but because of their history, the genetics that support them are precarious. Protecting these breeds will require more vigilance now, and more cooperation among the breeders who have a collective desire and responsibility to protect the genetic heritage of our breeds. At the very least, we should be monitoring breed populations in the same way that we keep an eye on the gray whale and Mountain Gorilla. We should be able to identify in real time impending bottlenecks developing from popular sires, genetic lines in danger of extinction, dangerous levels of inbreeding, the emergence of new genetic disorders long before they are epidemic, and the booms and busts that can drive the genetics of a breed in an unwanted directions.

Think about the history of your own breed, and how your genetic landscape has changed over the generations. Assess what you have today, the problems that need to be tackled, and the path breeders need to take in the future to protect and improve on what we have. Collective efforts can be very powerful, and the payoff will come in securing the genetic resources of the breed for the future.


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