IN PURSUIT OF STYLE:

Consequences of Line Breeding in Horses

Eohippus (meaning "dawn horse"), the ancestor of the modern horse, originated in North America approximately 55 million years ago. During the Miocene epoch, some of the descendants of Eohippus migrated across the Bering Sea, colonizing Eurasia (Bourdelais 1997). These Eurasian lines developed into all known Equus species, including: the zebra (E. zebra), native to southern Africa; the wild ass (E. hemionus hemionus), native to western Asia and the Middle East; the donkey (E. asinus), native to North Africa; and the modern horse (E. caballus) (Edwards 1993). Approximately 10,000 years ago, the horse became extinct in its native North America, but it persisted in three main forms, each adapted to its own environment: "Arabian" types in the Middle East, "Barb" types in Northern Africa, and "Spanish" types in South Western Europe (Edwards 1993). It is from these three types that we have derived hundreds of separate breeds of horses.

During the 16 th century, Spanish conquistadores reintroduced horses to North America (Edwards 1993). These horses were mostly of the Spanish type, and those that escaped or were set free or left behind by the Spanish became the feral horses of North American - the mustang (Edwards 1977). The same Spanish stock that produced the mustang also helped produce the two breeds of interest in this paper. The American Paint Horse originated in the 16 th century and is directly descended from the Spanish horses of the conquistadores (Edwards 1993). The breed is characterized primarily by its coat colour which consists of several variations and combinations of patches of white and non-white hair. These coat patterns will be discussed in detail later (also see Appendix A: American Paint Horse Coat Patterns). In the 17 th century in Virginia and the Carolinas, Spanish horses were being out-bred to imported English stock, mainly Thoroughbreds. This crossing eventually led to the formation of the American Quarter Horse (Edwards 1977).

The American Quarter Horse Association (AQHA), the governing body of the Quarter Horse breed, holds an annual international competition - the AQHA World Championship Show. With only 86 classes consisting of several go-rounds, it covers two full weeks in November. The winners of each of these 86 classes will split the total of $1.6 million in prize money and awards – an average of just over $18,600 per class! Clearly, breeding and training horses is big business. In this competitive world, there is tremendous pressure for breeders to produce animals with "popular" characteristics such as correct (breed dependant) conformation and athletic talent as well as more style dependant characteristics such as colour and "looks." To obtain and preserve these characteristics within bloodlines, horses are often bred to close relatives with the same characteristics. This is known as line breeding. However, should a mutation occur in an individual for any reason, line breeding can become a major disadvantage as it tends to be passed on to not only a few individuals, but to potentially hundreds of offspring and their offspring, and so on. To put in perspective how many foals a popular sire may produce, the famous Two Eyed Jack, produced 1,416 AQHA registered foals (Stud Book AQHA). Thus, while line breeding does tend to produce reliable characteristics in the foal, it also tend to lead to the perpetuation of undesirable characteristics and detrimental genetic conditions.

It is important to note that a horse's lineage is usually expressed in the terms of the sire and the maternal grand-sire. This is because a mare has a limited reproductive potential - she can only produce one foal per year (at least until foals from surrogate mares are allowed to be registered). This, combined with the freedom to choose any sire (while you may only own one mare), means that sires contribute more to the make-up of the genetic pool and dispersion of genes than dams. Thus, genetic defects and line breeding are usually discussed as a function of the sire, grandsires, et cetera.

Hyperkalemic Periodic Paralysis

A horse's conformation refers to how "well built" it is. This includes both the basic mechanical requirements on a horse's body - for example, straight legs that move more efficiently and are less prone to injury - and the stylistic characters of the breed. Each breed has specific conformation standards that define the breed, and breeders usually strive to achieve "perfection" by this standard. In a conformation or "halter" class, a horse is expected to show excellent conformation, as placings are based solely on it (AQHA Handbook, Section 448). In recent years, it has become "fashionable" for horses bred specifically for halter competitions to be heavily muscled; it has even progressed to the point where many halter horses are kept in varying degrees of obesity in attempt to make them look larger.

In this effort to breed halter horses with heavy musculature, the Quarter Horse sire Impressive (AQHA #767246) became a key sire, producing an incredible 2,251 registered Quarter Horse foals in his lifetime. However, Impressive possessed a point mutation which caused a single guanine molecule to replace a cytosine molecule (Reynolds Equine HYPP). This results in a substitution of leucine for phenylalanine during the synthesis of the sodium channel proteins used by muscle cells. In a normal nervous response, sodium channels open allowing Na+ ions to flow into the cell and invert the charge across the membrane (depolarization). In the defective sodium channel, the leucine residue, which is more compact than the normal aromatic phenylalanine residue, allows Na+ to "leak" into the cell, depolarizing it and causing a spasmodic and uncontrollable nerve impulse (Reynolds Equine HYPP). This random depolarization most commonly is observed as muscle tremors such as localized shaking, trembling and weakness (Spier 1999), but also manifests itself as paralysis of the larynx and pharynx (Spier 1999), drooping membrane nicitans (3rd eyelid), stiffness, weakness, yawning (Reynolds Equine HYPP), and in some circumstances paralysis that leads to collapse (often of the hind end, resulting in "dog-sitting") and cardiac or respiratory failure (Spier 1999). This condition, being associated somewhat extraneously with potassium levels in the blood stream (Reynolds Equine HYPP) was dubbed hyperkalemic periodic paralysis, or HYPP.

HYPP is inherited as an autosomal, dominant trait with two alleles: the normal allele (N) and the defective allele (H) (Spier 1999). Thus, there are three genotypes possible, N/N, N/H, and H/H. Although it is a dominant trait, the HYPP gene's effect is somewhat cumulative; that is, a homozygous positive (H/H) horse is generally more severely affected than a heterozygous (N/H) horse (Reynolds Equine HYPP). A study of rate of HYPP appearance in Quarter Horses by Groves (1996) helps to support Impressive as the source of this allele. In a general sample of 1000 Quarter Horses taken between 1989 and 1991, the distribution of genotypes was 96% N/N, 4% H/N, and 0% H/H. However, 27,000 blood samples of horses tracing their bloodlines back to Impressive showed 63% N/N, 36% H/N, and 1% H/H (testing at University of California at Davis - Veterinary Genetics Lab, between 1992 and 1996). While this is far from a perfect experimental setup, the numbers are so drastically different as to lend support to the theory that Impressive was indeed the source of this mutation. Dr. Sharon Spier, the leading researcher of HYPP at the UC Davis lab, draws further conclusions from this in an interview with the AQHA:

However, although HYPP and muscle mass do seem to be closely associated, further research by Dr. Spier (Interview) showed no difference in the muscle fibre belly diameter of positive versus negative horses and concludes that heavy musculature is controlled by a group of genes other than the HYPP gene.

Since identifying and realizing the seriousness of this genetic defect, the AQHA has imposed means of tracking the genotypes of all horses with Impressive bloodlines, especially breeding stock. The AQHA has listed HYPP among the "conditions commonly considered undesirable traits or genetic defects" (Brewer HYPP). Further, all registered foals born 1 January 1998 or later and tracing to Impressive must have their HYPP genotype listed on their registration papers (under "Markings"). Otherwise, the statement "This horse has an ancestor known to carry HYPP, designated under AQHA rules as a genetic defect, AQHA recommends testing to confirm presence or absence of this gene," will appear in its place (Brewer HYPP). Hopefully, this will encourage breeders to be aware of this condition and aid in the attempt to select against it and ideally breed it completely out of the gene pool.

Hereditary Equine Regional Dermal Asthenia

Cutting is an extreme test of a horse's physical ability and inherent "cow sense," or natural talent for working cattle. In a cutting competition, a horse is required to enter a herd of cattle, cut one cow (selected by the rider) out and drive it a distance from the herd. As a cow will almost always try to go back to the rest of the herd, the horse must keep itself between the cow and the herd for two and a half minutes (NCHA Handbook). While there is a certain amount of training involved in cutting competitions, cow sense and the natural ability and athleticism required to stop, or turn, or run almost instantaneously in any direction, is something that must be in the horse to begin with. One of the top sires for such competitions was Poco Bueno (AQHA #3044). Born in 1944 on the famous Waggoner Ranch, home of his sire, the famous Foundation Quarter Horse King (P-234), Poco Bueno changed the cutting world the way Hollywood Jac 86 would later change the reining world. It was said that in a 1948 competition "Poco Bueno headed a cow and turned so quickly that he left his rider standing on the ground" (Gaines 1982). This helped his trainer, Pine Johnson, to revolutionize the cutting seat into what we see today.

In recent years however, a dark cloud has come over Poco Bueno's name. A genetic condition known as hereditary equine dermal regional asthenia (HERDA) has been linked to him (FQHA 2004). Based on the way the condition is transmitted, it appears to be an autosomal recessive gene which results in defective collagen within the deep dermal layers (Lowder 2004). A recent study by White et al. (2004), found that collagen fibres of affected individuals were typically thin and shortened, although they could not assure a definitive diagnosis based on analysis of dermal collagen. Because of its symptoms, HERDA was originally dubbed "hyperelastosis cutis." However, evidence supports that it is not an excess of elasticity, but rather the dysfunction of collagen that causes a weakness (asthenia) of the skin leading to seromas, haematomas, and generally "loose skin" that lifts and tears away from the underlying tissue leaving a lasting fold if the skin itself is undamaged or sloughing of the skin and open lesions if even small amounts of trauma are introduced (White et al. 2004). Ongoing research into the exact chromosomal location of HERDA by Bannasach et al. is taking place at the UC Davis Center for Equine Health. Given the rarity of the disorder and the amount of line breeding seemingly required to have expression, HERDA may require multiple alleles (more than two) in order for it to sufficiently reduce the effectiveness of the collagen fibres. This may be an interesting topic for future research.

Overall, HERDA is a very rare disease, mostly owing to its recessive nature but also to the fact that many affected horses are euthanized when mild trauma leads to wounds that resist healing (Lowder 2004). Despite this, I have had personal experience with HERDA in a Quarter Horse in Cape Breton . He was accidentally line bred, his sire and dam being half-siblings out of the same mare, a great-granddaughter of Poco Bueno. Tracing twice to Poco Bueno is mildly convincing of line breeding and could suggest him as a source of the mutation. However, given the particular pedigree, we may also need to look seriously at King P-234 as a potential source as this horse traces five times to King, Poco Bueno's sire. This correlation covers not only the maternal/paternal grandmother's lineage, but also the paternal grandsire as a link to King. This may be an interesting topic of study in the future, but it will likely never be absolutely determined, as we cannot test the original sires and the degree of inbreeding and cross breeding has made it nearly impossible to elucidate the exact origin of genes.

The AQHA and the Foundation Quarter Horse Association (FQHA) are only just beginning to make the public aware of HERDA and its effects and consequences. Only time will tell whether preventative measures will be taken in the future to identify HERDA carriers. However, it is important to note that while HERDA symptoms cannot be maintained as HYPP can, HERDA is not as serious a problem as HYPP for three reasons. First and foremost, HERDA is a recessive condition and requires multiple alleles for expression where as HYPP is a dominant condition and symptoms are expressed in heterozygotes. Second, the Waggoner Ranch restricted breeding of Poco Bueno primarily to their own mares. Thus, Poco Bueno only produced 405 registered foals (compared to Impressive's 2,251). So while Poco Bueno is still in the bloodlines of many horses, his genes have been diluted by out breeding much of the time. Finally, Poco Bueno was born in 1944 and died in 1969, the same year Impressive was born. This means that many young horses and horses in their prime (approximately 8 to 14 years) that are descended from Impressive are still very closely related to him (2 to 4 generations), while Poco Bueno's descendants are generally four or more generations removed from him. This strongly suggests that HYPP is of more concern to the Quarter Horse world than HERDA, at least until more is known about it.

Overo Lethal White Syndrome

Probably the most recognized genetic misfortune in the horse world does not take place in the world of the American Quarter Horse, but in the closely associated American Paint Horse. While the American Paint Horse Association (APHA) does have its own registry, it accepts not only horses with Paint parents but also the Quarter Horses and Thoroughbreds born with "unfortunate" paint colouration, as their respective associations (the AQHA and the Jockey Club) will not register coloured horses. An American Paint Horse is primarily recognizable by its flashy patches of colour and white markings; and because the breed is so vitally linked to this trait, breeders tend to breed for "colour" or the presences of white body markings. There are basically three major types of coat patterning - tobiano, overo, and sabino — although combinations of the three can occur (see Appendix A for a full description of coat patterns).

The desire to produce foals with the splashy paint colouration is plagued however by the occurrence of overo lethal white (OLW) syndrome. This condition is caused by a dinucleotide mutation that results in the substitution of isoleucine for lysine in the endothelin receptor B (EDNRB) protein (Lightbody 2002). This protein is normally responsible for the regulation of the cell differentiation and migration from the neural crest of the cells that develop into ganglia and melanocytes. The mutation results in reduced protein functionality which has two major consequences: melanocytes do not migrate throughout the body, resulting in a completely white foal; and nerve cells do not form properly in the lower digestive tract, leading to impaired nervous development of the intestine (ileocolonic agangliosis) (Lightbody 2002). Although the foal is often carried to term, it begins showing signs of colic, usually within the first 12 hours, as it cannot pass waste through the colon. At this point, the foal is usually euthanized, as the condition is always fatal (Walker 1997).

Being a commonly known and discussed issue, OLW syndrome is associated with any number of "explanations." Arguments are most often made that it is a dominant characteristic, while others claim that it is a recessive characteristic, and some say that the mutation is not linked to all overo genes. Lightbody (2002) suggests that the amount of white on a horse's body can be used as a signal to whether it may have the OLW mutation. I've even heard of the old horsemen saying that you'll never get a lethal white foal as long as you don't breed two blue-eyed horses together. Much of the difficulty in pinning down an exact model is that paint colour patterns are so complex; often two different coat patterns combine or a pattern isn't expressed clearly (minimal white horses). Thus, how can you be sure that you are truly studying a horse from an overo-overo cross and not an overo-tovero cross? Future research should look into the possibility of incomplete dominance of overo genes, especially as the phenotypic coat patterns show three variations: solid, white and a combination of the two. This could be further investigated by studying the nervous development of the lower intestinal tract of solid paint horses and phenotypic overos. Assuming that melanocytes and the nerve cells are truly connected, incomplete dominance of the overo gene should theoretically result in an intermediate degree of nervous development in the lower intestines of heterozygous individuals.

There is a lot of time and money invested in breeding and caring for a pregnant brood mare and a lost season can mean a significant monetary loss as well. So Paint Horse breeders walk a fine line between breeding for colour and avoiding a lethal white foal. The only sure way to avoid producing an OLW foal is to always out breed an overo to a solid coloured horse. It boils down to genetics, and genetically, you have the same chances of getting a coloured horse from this cross (50% overo, 50% solid) as you do by breeding two overos (25% solid, 50% overo, and 25% lethal white).

Conclusions

We live in a time when the AQHA must enforce rules to keep competitors from altering their horses' tails in order to be "perfect" (AQHA Handbook). Owners and trainers have been known to anesthetise their horses' docks to prevent them from moving while the horse is showing and tail extensions are quickly becoming the norm. Clearly "winning at all costs" has come to the point that many people are willing to sacrifice not only their horses' health, but also the essence of being a horse in order to bring home a trophy. Thus, it should be of no surprise that the degree of line breeding in performance horses has reached an incredible level.

There are definite advantages to line breeding within selective breeding programs such as the Quarter Horse industry. It helps to maintain quality stock suitable for the jobs we ask them to do as well as allowing us to find a line of horses tailored to our individual needs and desires. However, when taken to extremes especially in ignorance of known genetic defects associated with the lines, line breeding can make a very small problem into a potential tragedy. Vanity and a desire to maintain "purity of the breed" are compounding the problems, especially with HYPP, where people are still breeding to horses who are not only untested for HYPP genotype, but in some cases proven heterozygotes! With the considerable attention that the condition has been receiving and the availability of information from the AQHA, this should not be happening. However, as long as judges are awarding high marks to bulky halter horses, those owners and breeder who are only showing for the money are going to continue to breed for these characteristics without consideration of the consequences associated with line breeding.

References

American Quarter Horse Association Handbook of Rules and Regulations. 2004. 52 nd Edition [Electronic Version]. Available online at http://www.aqha.com/association/registration/handbook.html.

Bannasach, D.L. et al. Search for the precise chromosome location of an inherited skin disease in the American Quarter Horse Breed. UC Davis Center for Equine Health Research Preview 2004-2005. [Electronic Version]. Retrieved 13 October 2004 from http://www.vetmed.ucdavis.edu/ceh/respreview.html.

Bourdelais, S. 1997. The 55 Million-Year-Old Horse. Horsepower Magazine, August – September, 35-36.

Edwards, E.H. 1977. Encyclopedia of the Horse. London: Octopus Books Ltd.

Edwards, E.H. 1993. Horses (Eyewitness Handbooks). Don Mills, ON: Stoddart Publishing Co. Ltd.

Foundation Quarter Horse Association Position Statement on HERDA. 2004. [Electronic Version] Available online from http://www.fqha.com/Articles/fqha_statement_on_herda.htm.

Gaines, D. 1982. Poco Bueno: Dead for more than a decade he lives through his genes. Quarter Horse Journal, Feb 1982, 36-39.

Groves, L. 1996. HYPP: Someone else's problem? Quarter Horse Journal, 1: 52-59. Cited in Reynolds Equine Hyperkalemic Periodic Paralysis (HYPP).

Lightbody, T. 2002. Foal with overo lethal white syndrome born to a registered quarter horse mare. Canadian Veterinary Journal, 43, 715-717.

Lowder, M. 2004. Hyperelastosis cutis or HERDA. HorseCity.com. Retrieved 22 November 2004 from http://horsecity.com/stories/061404/hea_herda_ML.shtml

Reynolds, J.A. Equine Hyperkalemic Periodic Paralysis (HYPP): Overview & Management Strategies. Retrieved 11 October 2004 from http://www.admani.com/AllianceEquine/TechBulletins/HYPP.htm.

Spier, S.J. 1999. Current Facts About Hyperkalemic Periodic Paralysis (HYPP) Disease. Retrieved 11 October 2004 from http://www.vgl.ucdavis.edu/~lvmillori/hypp/hypp_facts.html.

Spier, S.J. Interview. AQHA.com. Retrieved 11 October 2004 from http://www.aqha.com/association/registration/hypp.html.

Stud Book of the American Quarter Horse Association. Available to AQHA members online at http://www.aqha.com/association/benefits/records.html, or from the AQHA Office, P.O. Box 200, Amarillo, Texas 79104.

Walker, D. 1997. Lethal Whites: A light at the end of the tunnel. Paint Horse Journal [Electronic Version], Feb 1997. Retrieved 11 October 2004 from http://www.apha.com/breed/lethalwhites01 .html.

White, S.D., et al. 2004. Hereditary equine regional dermal asthenia ("hyperelastosis cutis") in 50 horses: clinical, histological, immunohistological and ultrastructuralfindings. Vetrinary Dermatology, 15(4), 207-217.