Culture: Science & History
Dogs are more than the sum of their parts
After years of flattering inquiries about our canines (“Oh, what a beautiful… what is he?”) and faltering replies (“Maybe…a Cocker/couch-potato mix?”), I decided to explore the new mixed-breed DNA testing.
Not that I couldn’t hazard some serious guesses about their ancestry. Upon rescue, Ticker appeared to be tan, but once rinsed of an entire puppyhood’s worth of dirt and neglect, his coat was actually white: white with faint ticking that, with age, has returned to the original dirty tan. Since our home already included two Retrievers, we thought to train this stray for my parents. Dad had just endured heart surgery, and Ticker could be the perfect cardiac rehab dog: Ticker for his own ticker. Within a week, we concluded that our own hearts needed a third dog.
Guesses as to Ticker’s lineage began with an inventory of the canines we recognized from 10 years of twice-daily walks: Dachshund? Neapolitan Mastiff? A few cheerful mixes? Our urban gene pool mostly offered “Pits.” Even our Golden Retriever and our Labrador-mix —according to the kids who came over to ask, “Those dogs bite?”—were guessed to be a “Pit,” a “Rott” or a “Rott-Pit mix.”
True enough, Ticker’s chest and legs are a bit stocky, but not massive. His shoulders and head are slight as a sighthound’s. And, if we’re going by bad PR and stereotypes, he is a biter. (A three-time, never-breaks- the-skin nipper, actually.)
Taking into consideration his Whippet-like waist, markings that suggest a Brittany or English Setter, and an early penchant for shredding upholstery and relieving pillows of stuffing (not sure which breeds were built for that), we announced him as a Whipbull Terrier.
So what did DNA testing reveal about Ticker? That he’s a remixed mixed-breed. Only 15 percent of dogs tested have as much miscegenation (perhaps you’d prefer the term “well-socialized heritage”?). The one hint of a progenitor the report offered: Dalmatian. And yet, the firehouse in our old neighborhood didn’t keep a dog, and the only “heats” on those blocks were barbecue grills and insurance fires.
“Looking at Ticker,” the test states we “should see”: [blank]. Okay, no clear parentage. It suggests we “might see”: [blank]. Okay, so no grandparents from the Old World. It does allow “a chance of seeing” traits from: Flat-coated Retriever, French Bulldog, Labrador Retriever.
Whipbull Terrier clearly needs amending: Ticker is a French Labation. A Bullcoated almador. Indeed, Ticker possesses a Dalmatian’s intelligence, stamina and family-oriented fixation. From the Flat-coated Retriever, he could have inherited his food motivation and eagerness to fetch. From the Lab? Perhaps his love of swimming, car rides and licking dinner plates. And from the French Bulldog? A comical personality? An ability to put up with endearing diminutives and humans blowing raspberries on his pink belly? It all feels a bit like gerrymandering personality quirks to fit a zodiac sign, or attributing character flaws to “precognitive memories.”
Barrett’s analysis provides a different perspective. A rescue from rural Ohio, he’d been bounced among a few homes for being “just too much dog.” At first, we took him to be an overly blond Golden Retriever. Lithe, but with an exceptionally broad head and prominent nose, he is affable surfer dude. A canine Owen Wilson.
As he’s aged, he’s thickened to 115 pounds and his feathering, especially on his tail, sports hairs that easily reach 10 inches. Some Newfoundland? Part Great Pyrenees? There was a slight mottling in the face and ears to suggest the latter. But zero instinct to herd. Zero interest in pulling carts. (True, we’ve never offered him any carts, although there is the occasional promise of a pet donkey if he finishes his homework.)
As for behavior, Barrett is a people person, preferring to supervise gardening from the truck’s back seat, watch from the porch for the last-to-arrive home, flop on the carpet and amuse himself by repeatedly triggering the songs in his stuffed songbird collection. Sure, he chases deer like a Foxhound, sniffs out rabbits like a Beagle and stands chest deep in our pond like a water buffalo—but this hardly illuminates his lineage.
Barrett’s DNA test reveals one clear progenitor. We “should see” aspects of: Chinese Shar-Pei.We read these words with the same quizzical amusement with which we read the fortune cookies our pan-Asian carry-out tosses in the bag along with the won-tons. His parent or grandparent was a dog that in 1978 was considered by Guinness to be the rarest in the world? A dog introduced to the U.S. in 1966 and only recognized by the AKC 17 years ago had found its way to Appalachian Ohio and evinced itself in a dog possessing nothing like the breed’s “short, harsh coat…loose skin covering the head and body…small ears… ‘hippopotamus’ muzzle shape”? But even more curious, Barrett shares none of the Shar-Pei’s “independence, wariness around strangers, or possible aggression with pets and people.”
Barrett’s report concedes that his other ancestors are as remote as Ticker’s. Oddly, the Labrador Retriever and Flat-coated Retriever rear their handsome, promiscuous heads in his case, as well.
So has this genetic information enriched our understanding, changed the doting, ever-watched-over lives we offer our companions, tempted us to collect new breed-specific knick-knackery? Bark readers, I suspect, know (and share) our conclusion: Dogs are beyond a single, double, or even motley, answer. Rather, each companion is an ongoing question, a partner with whom we share our mixed-up, muddled, ever-more-hybridized planet.
Good Dog: Studies & Research
BBC’s Pedigree Dogs Exposed strikes a chord
In August 2008, a powerful BBC documentary, Pedigree Dogs Exposed (PDE), rocked the dog world when it claimed to reveal the “greatest animal welfare scandal of our time.” Following its premiere, a review in a national newspaper said the show had “gone off like a bomb in quite a few British living rooms.” Four million British people watched, and the BBC received its biggest-ever viewer response to a single program. Middle England was outraged.
For decades, the details of dog breeding and showing had been closeted from the critical view of the outside world. While the comedy Best In Show famously took a peek and pointed a finger of fun at some breeders and exhibitors, PDE portrayed the pedigree dog world in a much more sinister light, and left the previously passive pet owner feeling furious and sad in equal measure. The eccentricity of the show world didn’t seem quite so amusing when people could see and hear that it apparently made dogs suffer.
It took filmmaker and dog lover Jemima Harrison two years to make PDE, but in just one hour, the scientific eye she cast over the dog-show world and the images she captured burned into people’s retinas as well as their minds. We saw a poor, beautiful Cavalier King Charles Spaniel screaming in pain because her skull was the wrong size for her brain, a Boxer having seizures, a German Shepherd hobbling around the show ring on strangely exaggerated limbs, a sweet show-winning Pug with a long line of Crufts winners in his pedigree and an equally long list of deformities. For many, it was an “Emperor’s New Clothes” moment as the program revealed how the show world had contorted some breeds into increasingly hideous and illogical shapes.
As Mark Evans, chief veterinary advisor at Britain’s biggest and oldest animal welfare charity, the Royal Society for the Prevention of Cruelty to Animals (RSPCA), said to the camera, “We are extremely concerned at the very high levels of disability, deformity and disease in pedigree dogs.” When he watched Crufts, he said, he saw a “parade of mutants.”
The exposure left England’s Kennel Club reeling. It hadn’t come over well in the documentary, and Chairman Ronnie Irving had made some off-the-cuff remarks that would come back to haunt him.
For example, on the subject of inbreeding, he said, “I don’t want a bunch of scientists telling me they know more about it.” When pressed on the ethics of mother-to-son matings, he defended it and said it “depended on the individual mother and son.” (I’m sure I heard the sound of jaws dropping across the country at that moment.) Not long after the show aired, the KC rushed to ban such matings—it also launched a complete review of every pedigree dog breed in the UK and required breed clubs to adopt its Code of Ethics, which includes a clause that explicitly forbids the compulsory culling of healthy puppies—but the damage had already been done with that throwaway remark.
The Kennel Club says it was hit by a tsunami of hate after the program. At the recent KC Annual General Meeting, Irving said they had had “literally thousands of letters, emails and calls—some of them extremely aggressive and some actually threatening our staff in a very frightening way.” Irving went on to say that “maybe worse were the many letters that we received from otherwise apparently sensible, intelligent people who had obviously swallowed the content of that program hook, line and sinker.” On their own forums, dog breeders complained of being spat at in the street.
The dog show world closed ranks, licked its wounds and waited for PDE to become yesterday’s news. But the program had opened Pandora’s box, and there was no going back.
The domino effect was staggering. After more than 40 years of televising it, the BBC dropped Crufts, the KC’s own dog show. Three powerful welfare charities—the RSPCA, Dogs Trust and PDSA—spectacularly pulled out of attending the show due to adverse supporter pressure, and Pedigree withdrew its meaty sponsorship, although it claims this was a coincidence and wasn’t connected to the documentary. A marketing guru simply said that as a brand, Crufts had become toxic.
But was the program unfair to the KC? Could the club have done anything more to protect pedigree dogs from suffering? Was the public simply expecting far too much of it?
At this point, I have to confess that I used to work there. It was 20 or so years ago and in quite a minor role. It may sound like hindsight, but I did try my best to warn them that there might be a tidal wave approaching. I grew up at dog shows, and even then, it occurred to me that the concepts of pedigree dogs and kennel clubs were relatively recent in historical terms, and no one seemed to have a plan for what to do as the gene pools shrunk ever further.
One of the studies referred to in the documentary was a groundbreaking Imperial College, London, investigation into inbreeding by Calboli, Sampson, Fretwell and Balding (“Population structure and inbreeding from pedigree analysis of purebred dogs.” Genetics 179 [May 2008]: 593–601). The researchers studied 10 breeds and found that these breeds had lost more than 90 percent of the genetic variation they had had 35 years ago. Decades of overuse of popular sires and linebreeding (breeding of dogs who share a common ancestor) had led to the sort of genetic erosion that made the giant panda look like a much safer bet for avoiding extinction than the Pug.
World-renowned geneticist Professor Steve Jones at the University College, London, was the voice of doom on the film. “If the dog breeders insist on going further down that road, I can say with confidence, really, that there is a universe of suffering waiting for many of these breeds—and many, if not most, of these breeds will not survive. They will get so inbred that they will be unable to reproduce and their genes will come to a dead end.”
Earlier in its history, the KC seemed to have gotten off on the right foot. Their hip-scoring scheme was revolutionary and promised to help the growing problem of hip dysplasia (HD) in many breeds. But when the scheme was still in its infancy, the KC made a decision that, on the face of it, made no logical sense. In breeds with significant HD problems, they decided not to make these tests a condition of using the registration system, while at the same time, opting to publish all the results—even the failures. Previously, they’d only publicized the successes; if anyone made a false claim about a dog that had failed, there’d be trouble.
World hip expert Dr. Malcolm Willis, senior lecturer in Animal Breeding and Genetics at Newcastle University, told me at the time that he thought it was madness. The number of breeders testing did indeed drop steeply—sadly, it’s human nature. If testing weren’t mandatory, why would all but the most altruistic breeders risk a very public failure with a winning dog?
Thankfully, elsewhere, others were thinking more deeply and strategically. In no time at all, the KC was getting left behind. Case in point: the Swedish Kennel Club—a nonprofit association of regional clubs, founded in 1889—which I visited back in 1992. I recall noting at the time that it lacked the pomp of the UK version but rather, felt very forward-looking and modern.
For a start, it was refreshingly democratic—anyone who owned a Swedish KC registered dog was a member—and it was welcoming to mongrels as well as pedigrees. Even back then, it was very customer-facing, employing lots of people to give advice over the phones. It offered a 24-hour helpline for lost dogs, one of the perks of having a registered dog.
But the real difference between the Swedes and the English was in their registration system. Long ago, the Swedish KC decided to make health testing mandatory. For example, back in 1992, 80 particularly afflicted breeds had to have both parents hip-tested if the breeder wanted to use the KC registration system; they’d already seen huge improvements in Newfoundland hips. They also decided to simplify the scoring system so it was clear to everyone how to interpret the results. They created three bands to encourage improvement: If your dog scored a grade 2, you couldn’t breed on. If your dog got a 0, you could choose a mate with either a 0 or a 1 score. But if your dog had a 1, he/she had to be mated to a dog with a 0.
It was the organization’s first step toward making its registration a mark of quality rather than a mere record of parentage. As more and more health tests became available, they were slotted into the existing system and again made conditional for breeders using the system. It seems so obvious now that this was in everyone’s best interests and provided a firm framework for improvement.
When the English KC is asked why it didn’t do the same thing, it says it was because it was afraid of losing breeders, of not taking them with them on the road for health reform. But the best English breeders already did all these tests, and more, without compulsion. Unfortunately, the public had no way of spotting the good guys as they rubbed shoulders in the same system with the inexperienced and the plain shoddy.
The KC also claimed it was afraid of breeders breaking away and forming alternative registries. Ironically, another registry saw and exploited a weakness: If the KC was providing expensive bits of paper that meant very little, why couldn’t it do the same thing, but charge less? By not being the best it could be, the KC allowed others an opening in which to compete for a slice of its registration revenue. The fear of taking the lead had lost it the race.
As inbreeding increasingly became an area of concern, the Swedes again were quick to break new ground. If any of you with purebred dogs have ever tried to calculate the level of inbreeding for your own dog, you’ll know how complex it is, and how time-consuming. The logical Swedes built the calculation into their pedigree database and made it freely accessible to all over the Internet. Using this information, breeders could see instantly how inbred any registered dog was and could create test matings and determine the level of inbreeding they might produce.
The Swedish KC also produced tables showing how inbred each breed was and charting trends, which allows the viewer to see if a breed is improving or not. It set bands for acceptable levels of inbreeding and started limiting the number of times a stud dog could be used in his lifetime.
While elsewhere around the globe, the cult of the top-winning show dog was dramatically shrinking the gene pool, the Swedes stopped some very inbred dogs from being brought into their country. (The big problem in Sweden now is dogs being smuggled into the country from Eastern Europe.) They made dog showing and breeding as meaningful as possible by adding temperament tests for some breeds before they could claim their titles, and required Border Collies to pass a herding test before being bred. They discussed how to reduce exaggerations caused by fashion and educated their judges without being provoked to do so by a national television exposé.
More good work: The Swedish Kennel Club worked closely with its government to pass a significant piece of consumer law, one that ensured that health and welfare were always at the top of every breeder’s agenda. In Sweden, if anything goes wrong with the health of a pup in the first three years, the breeder is financially responsible. With a system like that, who is going to have a litter from an untested pet Labrador just to fund a summer holiday? Who would want to be a puppy farmer if the breeder pays for a pup’s ill health?
Apart from having what I consider the best kennel club in the world, Sweden also seems to have cracked many other significant welfare problems that continue to plague other nations. By being strong, forward-thinking and logical, they’ve made dog breeding a respectable and professional thing to do, and made dog shows less like beauty pageants and more relevant to today’s society. In Sweden, they don’t have puppy mills. In Sweden, they don’t have pups for sale in pet shops. The few rescue shelters there are almost empty. No puppy is sold or labeled as “pet quality,” since the supposition is that they are all “pet quality”—family dogs or companion dogs first and anything else second.
In the past, could the English Kennel Club have done anything to avoid that tsunami of hate? What do you think?
Post-PDE, there have been several significant scientific reviews into dog breeding, and I’m hopeful that legislative changes will result that will give England a system as good as the Swedish model.
This little documentary may ultimately have saved the dog from extinction.
Editor’s Note: We understand that Pedigree Dogs Exposed may be slated to run on BBC America later this year; we’ll be watching for it and will announce the date on thebark.com when it’s confirmed. And in July 2009, the RSPCA bestowed their highest accolade, The Richard Martin Award, on Jemima Harrison for her work on this groundbreaking and influential documentary. It is the first time the award has been given to a filmmaker.
UPDATE: Pedigree Dogs Exposed premieres Thursday, December 10, 8:00 p.m. ET/PT on BBC America.
MORE: A report recommending new standards of pedigree dog health in the UK to be released following an independent inquiry. Read more about it here.
Culture: Science & History
A female Boxer provides the DNA for the first complete sequence of the dog genome—what will it mean to the health of man and dog?
“The dog is everywhere what society makes him,” wrote Charles Dudley Warner in the January 1896 issue of Harper’s New Monthly Magazine. Elaine Ostrander and Heidi Parker update that message in the November 2005 issue of the online journal, Public Library of Science—Genetics: “The domestication of the dog from its wolf ancestors is perhaps the most complex genetic experiment in history, and certainly the most extensive.” Undeniably, the results of that experiment are directly manifest in the appearance and behavior of the dog.
Since hitching its evolutionary fate to that of humans some 9,000 canine generations ago, the dog has proven the most adaptable, versatile and steadfast of companions, serving as a guard; draft animal; hunter; herder; warrior; entertainer; finder of explosives, contraband, disease and lost souls; healer, therapist; physical and spiritual guide; and friend. With the public unveiling last month of the fully sequenced and richly annotated dog genome—the approximately 2.4 billion base pairs of DNA (A [adenine], which always binds with T [thymine], and C [cytosine], which binds with G [guanine]) that form its genetic code—the dog might now also add to its monikers, shall we say, “genomic consort.”
Of course, the dog is not the first mammal other than humans to have its genome fully sequenced—the mouse, rat and chimp got theirs first—but because of its architectonic breed structure, it might prove the most illuminating. To shift metaphors: geneticists can now use the dog genome sequence like a combination zoom and telephoto lens, zeroing in on specific genes and even minute changes within genes, or jetting back to examine broad patterns and interrelationships within it and between it and other genomes that reveal the evolutionary history of an individual, a breed, a population, or the entire species and genus.
Dog as Cultural Construct
By most estimates, there are today more than 400 breeds worldwide, many with specialized morphologies and behaviors, nearly all genetically isolated. The majority of those breeds are also susceptible to one or more of more than 400 genetic disorders, approximately 350 of which are also found in humans, including epilepsy, kidney cancer, deafness, blindness, auto-immune disorders, congenital heart disease, skeletal malformations, neurological abnormalities, bleeding disorders and neuropsychiatric disorders.
Because traits and diseases often cluster according to breed and because breeders maintain extensive pedigrees, canine geneticists have long argued that the dog represents an ideal natural model for examining how genes shape appearance, function, behavior and health. In 1991, Jasper Rine, a geneticist at the University of California, Berkeley, with two researchers in his lab—Mark Neff, a postdoctoral fellow, and Elaine Ostrander, a staff scientist—started the Dog Genome Project to study those issues and in the process create a map of the dog genome they could link to that of the human genome for comparative study. [Ed. Note: See interview with Mark Neff.] From that effort was born a cottage industry, under the informal leadership of Dr. Ostrander (now at the National Human Genome Research Institute of the National Institutes of Health) and involving a small group of scientists worldwide, devoted to sequencing the dog genome, segment by segment. The researchers also lobbied to have the dog genome sequenced as part of the continuing Human Genome Project, in order to complete the task quickly and accurately.
In 2003, scientists at the Institute for Genomic Research and what is now the J. Craig Venter Institute in Rockville, Md., published a proprietary sequence covering 75 percent of the genome of a Standard Poodle, Shadow. On the other hand, sequences prepared as part of the Human Genome Project are posted in public data banks in the US, Europe and Japan as soon as possible after they are completed, so researchers can have access to them.
In July 2004, without fanfare, researchers from the Broad Institute at MIT and Harvard and Agencourt Bioscience Corp., of Beverly, Mass., led by Kerstin Lindblad-Toh, deposited in those public data banks their “first draft” sequence of 98 percent of the genetic code for “dog” in general and Tasha, an inbred Boxer from upstate New York, in particular. Their sequence was more complete and considerably more detailed than that of Shadow.
Then came a pause—of the seemingly interminable sort that occurs between the time certain dogs are called while snorfling in the park and the time they decide to respond—that was devoted to revision, analysis and assigning chunks of the sequence to their appropriate chromosome. The dog has 38 pairs of autosomal chromosomes—inheriting one from each parent—and two sex chromosomes. Lindblad-Toh’s team did not sequence the Y (male) chromosome.
Finally, at a press conference in Boston on December 7, 2005; in a lengthy article in the prestigious journal Nature on December 8; and in supplemental articles in the December issue of Genome Research, Lindblad-Toh and her team, along with Ostrander and dog genome scientists, officially unveiled the by then 99 percent complete sequence of Tasha and a SNP (pronounced “snip”) map showing 2.5 million “single nucleotide polymorphisms,” or mutations, in the genomes of Tasha, nine other purebred dogs, four wolves and a coyote. This map is useful for finding genes and examining interrelations between groups and individuals. The Nature article also contained an analysis by Lindblad-Toh’s research team of the dog genome’s structure and a new look at the dog’s family tree, origins and transformation by humans. (Full disclosure: Bark deadlines being what they are, I did not attend the press conference, which was designed to receive maximum coverage in the daily media.)
The Dog Genome
From a certain perspective, the dog is just another mammal, albeit with a genome slightly smaller and “cleaner”—“there is less junk,” Lindblad-Toh said—than that of its human companion or the ubiquitous lab rat, to which the researchers also compared it in Nature. Tucked within the 2.4 billion base pairs of the dog’s DNA are some 19,300 genes. By comparison, the human genome consists of approximately 2.9 billion base pairs of DNA and, at most recent count, approximately 22,000 genes. Approximately 72 percent of the dog genes are orthologous, meaning they correspond on a one-to-one basis with genes found in the human and rat genomes, although their functions might differ.
Comparison of mouse, human and dog genomes have identified a core 812,000,000 base pairs (5.3% of the total human genome) of ancestral sequence common to all three species. This DNA encodes proteins (1-2% of the total genome), and includes specific sequences that control gene expression. This portion of the genome is under what biologists call purifying selection, wherein variations on a gene or changes in a sequence are selected against, or weeded out. The sequencing of additional mammalian genomes, including those of Rhesus monkey, cow, opossum, elephant, rabbit, cat and shrew, should help to sharpen the focus on the DNA definition of mammal-ness.
Despite the similarities between all three species, it appears the genome better reflects the social reality of dogs and humans than does taxonomy, which places the rat closer evolutionarily to humans than the dog. The researchers reported in Nature that some sets of functional genes, like those involved in brain development, showed signs of having evolved similarly in dogs and humans—and more rapidly than in rats. It is a suggestive finding.
The dog’s value in comparative genomics lies in large measure in its breed structure, and here the researchers offer some support to a couple of recent suggestions that repetitive segments of DNA are somehow tied to the dog’s physical plasticity, its ability to assume so many different shapes and sizes, as well as to fall victim to various inherited diseases. Geneticists have focused not only on SNPs—changes in a single base—but also on repetitive blocks of DNA, including “short interspersed nuclear elements” and “tandem repeats.”
SINE elements, as they are known, are repetitive segments of DNA between 150 to 750 bases long. Interspersed throughout a genome, they move around over time, and some are species-specific.
On the whole, the dog genome has fewer SINE elements than the rat or human. But it has a “highly active carnivore-specific SINE family” that is full of mutations that vary between breeds, Lindblad-Toh and her co-authors wrote in Nature. These SINE elements are greater in frequency by a factor of at least 10 than any found in humans, and are believed to play a role in gene expression. When inserted into genes, they can cause diseases, like narcolepsy in Doberman Pinschers and centronuclear myopathy (a muscle disease) in Labrador Retrievers.
Wei Wang and Ewen F. Kirkness of the Institute for Genomc Research, writing in Genome Research, argue that SINE elements are a major source of genetic diversity in the dog. Citing their research, Lindblad-Toh and her colleagues speculate in Nature that the variation from SINE elements “has provided important raw material for the selective breeding programs that have produced the wide phenotypic variations among modern breeds.” In that event, SINE elements may have been what has allowed humans to produce everything from the Pug to the Irish Wolfhound.
But no one knows. In December 2004, John W. Fondon, III, and Harold R. Garner of the University of Texas Southwestern Medical Center proposed in the Proceedings of the National Academy of Sciences—in a paper that caught the attention of scientists, if not the press—that changes in the length of “tandem repeats” found within genes are responsible for the phenotypic variation between breeds and the speed with which breeders can change a breed’s appearance. Once called “junk DNA,” like so many other parts of the sequence whose purpose was then unknown, these “tandem repeats” occur when two or more nucleotides form a pattern that repeats itself over a short stretch of the genome.
Simply, tandem repeats are shorter than SINE elements. Both are suspected of playing a role in creating the plethora of dog breeds. But changes in the timing of development are also believed to be involved. Sorting that out is where the Dog Genome Project began and where it still must go. In that sense, the genome sequence represents a beginning rather than an end.
A Genomic Look at History
It is thus poetically fitting and perhaps scientifically significant that genetically, dogs show a similar pattern of homogeneity and variability between and within breeds, especially the modern breeds. In general, they were formed through extensive inbreeding and the use of favored sires, both of which serve to limit genetic diversity. Yet, despite that, or perhaps because the genetic isolation of breeds has not been long enough or as extensive as breeders sometimes claim, those breeds continue to possess a surprising amount of genetic diversity.
It is easier to assemble the genomic sequence of highly inbreed animals because of the genetic homogeneity of the pairs of chromosomes being sequenced. Compared to other Boxers, Tasha’s genome has one SNP—one change in one letter, or nucleotide – every 1,600 base pairs. Less inbred breeds would have more SNPs. Such changes or mutations appear randomly throughout the genomes of all animals, primarily in non-coding regions outside genes, where their purpose, if any, is uncertain, and far less frequently within genes where they can cause lethal mutations.
SNPs persist for hundreds of generations and form distinctive, inheritable clusters or blocks of genetic code on chromosomes that are known as “haplotypes.” Because they are passed on through generations, haplotypes are useful for exploring the evolutionary history of individuals, groups and species, and seeking out clusters of genes involved in inherited diseases, in morphology and, it is hoped, behavior. Probing the differences between individuals with congenital heart disease, for example, and those without, researchers would use their SNP map to identify the haplotypes of sufferers against those who are disease-free in an effort to find a region or regions on a chromosome that seemed involved. There, they would focus the search for genes.
To create a densely detailed SNPs map of the dog genome, Dr. Lindblad-Toh’s team partially sequenced the genomes of nine additional dog breeds, four kinds of wolf, and a coyote: German Shepherd, Rottweiler, Bedlington Terrier, Beagle, Labrador Retriever, English Shepherd, Italian Greyhound, Alaskan Malamute, Portuguese Water Dog, Chinese gray wolf, Alaskan gray wolf, Indian gray wolf, Spanish gray wolf, and California coyote. They also had the genome sequence from the French Poodle, Shadow. The researchers found 2.5 million cases where there were differences in a single nucleotide between the various canine genomes.
Comparing the Boxer to the other breeds and the five wild canids, the researchers found that while the SNP rate between different Boxers was 1 for every 1,600 base pairs, it was around 1 for every 900 base pairs between the Boxer and every other breed but the Malamute, which was 1 for every 787 base pairs. According to the breed identification system developed by Elaine Ostrander and Leonid Kruglyak of the Fred Hutchinson Cancer Research Center in Seattle, the Malamute belongs to a class of “ancient dogs” and thus would be expected to be more distant from the modern Boxer than other modern breeds—the shorter the distance between SNPs, the more distant the relationship. The other dogs represented breeds created or consolidated within the past 300 years, like the Boxer. Compared with the Boxer, the wolves had ratios of around 1 SNP for every 580 base pairs, and the more distantly related coyote stood at 1 for every 420 base pairs.
The Boxer’s genome represents “a mosaic of long, alternating regions of near-total homozygosity and high heterozygosity,” the researchers reported in Nature. The homozygous regions, wherein both chromosomes in a pair have identical haplotypes, cover 62 percent of the genome; the heterozygous regions, in which the haplotypes are not identical due to SNPs or genetic variations, 38 percent.
The researchers then scanned the genomes of 20 dogs from each of 10 other breeds, and one dog from each of 24 breeds, ranging from the ubiquitous Labrador and Golden Retrievers to the rare Glen of Imaal Terrier, but always limiting themselves to purebred dogs registered by the American Kennel Club. The analysis by Lindblad-Toh’s team reported in Nature that most dog breeds were similar to the Boxer in terms of number of SNPs, and the relative proportions of heterozygosity and homozygosity were also similar.
The one aberration was the Akita, a Japanese breed created, by Lindblad-Toh’s estimate, some 10,000 years ago for hunting, which passed through a bottleneck in the 1940s in America. The first official Akita in America was a gift from Japan to Helen Keller in 1937.
Using mathematical models that postulated an effective population of 13,000 dogs with an inbreeding coefficient of .12—meaning basically that they are cousins—the researchers concluded that in achieving its current blend of sameness and difference, the dog passed through a major genetic bottleneck 9,000 generations ago, and another 30 to 90 (sometimes given as 50 to 100) generations ago. Assuming a generation time of three years for dogs, they pegged the origin of the dog at 27,000 years ago from perhaps as few as two wolves. Lindblad-Toh said in an e-mail that the founding population of wolves might have been larger—and some geneticists say there must have been several hundred animals involved—but the genome does not appear to record any contribution from them. She also said that there may have been multiple domestication events and back-crosses with wolves at various times and places, as other genetic studies have shown.
I am a fan of ancient dates when it comes to dog origins, and the older the better, but this new offering—a sort of compromise between 15,000 years ago in East Asia, proposed by Peter Savolainen of the Royal Institute of Biotechnology in Stockholm and his colleagues in 2002, and 40,000 to 135,000 years ago that Robert K. Wayne and his lab team at the University of California, Los Angeles (including Savolainen), proposed in 1997.
Geneticists are divided, but archaeologists are not. Darcy Franklin Morey, an archaeologist at the University of Kansas specializing in the dog, says that 27,000 years ago, like the older dates, fails to coincide with the archaeological record, which dates to around 12,000 to 14,000 years. Morey has a paper forthcoming in the Journal of Archaeological Science arguing that the proliferation of dog burials at the time marks the origin of the dog. He does have a point in that as a cultural construct, the dog has left natural history and entered human history. Arguably, then, the molecular clocks used to calibrate its age should be set to human, as well as geologic time. Beyond that, the choice of three years as the generation time for dogs is unexplained and possibly long.
A notable change in the dog from the wolf is that females enter first estrus at six months to one year of age. Breeders in the rural South have long bred their dogs at first heat, and it may well be a custom dating back centuries. Australian dingoes, living in packs independent of men, start breeding around two years of age, according to dingo expert Laurie Corbett in The Dingo in Australia and Asia. Beyond that, my searches fail to pull down any calculation for the generation time for dogs. Clearly, that needs more examination.
In a commentary accompanying Nature’s presentation of the genome, Hans Ellegren, an evolutionary biologist at Uppsala University, raised another qualifier, saying that if “repeated back-crossing has occurred” between dogs and wolves, Lindblad-Toh’s model of the dog’s origins “would have to be revised.”
The Broad Institute team’s analysis appears on firmer footing when it comes to placing breed formation within the past 200 to 300 years. Breeds are formed through consolidation of working dogs of an existing type into a more consistent form, through hybridization and inbreeding to reconstruct a breed, and through building on a small number of imported animals. Early dogs bred rather freely, and—because in sexual reproduction, the chromosomes from the sire and the dam are recombined to form the single chromosome passed on from each and because alignments are not perfect—haplotypes were broken up, becoming shorter and more scattered over the generations of random breeding.
Through inbreeding from a small gene pool to create their particular breed, humans unknowingly selected a small group of overlapping chromosomes carrying the genes for the traits they wanted—and for some diseases they didn’t want. From that came the breed’s distinctive pattern of large homogeneous haplotype blocks and shorter heterogeneous ones, which selective breeding has sustained.
A notable exception to this model appears to be the Labrador Retriever, which replaced the “old yellow dog,” or cur dog, as America’s most abundant big dog and so is less inbred than other breeds, except in some lines. The English Springer Spaniel and Golden Retriever are more inbred than Labs but less than most other breeds. But all three show the pronounced influence of “favorite sires,” whose overuse also serves to limit diversity. In an interview, Elaine Ostrander said research in her lab has indicated a clear genetic break between show Labs and field-trial Labs, and between show and hunting Beagles.
Breeds that passed through a formation bottleneck typically have four of around 10 possible haplotypes, the researchers said. Although the haplotypes and their proportions vary from breed to breed, haplotypes are also shared between them. As the Akita indicates, this arrangement might not extend beyond breeds of western dogs. But it means that researchers can use 10,000 SNPs, a relatively small number, to scan the genomes of dogs within the breed and compare them with those of other dogs in the same breed in order to find genes.
“We now have a whole new tool kit for looking at the evolutionary history of canines and the origins of dogs, where they originated and how they spread, and how often they interbred with local wolf populations,” said Robert K. Wayne, an evolutionary biologist at the University of California, Los Angeles. A 60,000-SNP GeneChip (similar to a computer chip but incorporating DNA) soon to be available from Affymetrix should speed the search for genes that regulate a dog’s phenotype, he added.
Wayne and his lab contributed a new family tree, or phylogeny, of 34 canid species for the Nature paper, showing the time of their emergence during the past 40 million years and solidifying the already strong argument that the wolf is the dog’s nearest relative, while the wolf’s wild kin are, in order, the coyote, golden jackal, Ethiopian wolf, dhole and African wild dog.
A small group of scientists believes that one of the dog’s more distant relatives, the fox, specifically a colony of tame foxes in Siberia, might hold the key to the genetic changes underlying domestication. They are using the dog genome, said one of the leaders in that quest, Gregory M. Acland, a geneticist with the James A. Baker Institute for Animal Health at Cornell. Like a number of other geneticists, Acland predicts that within 20 years, SNP maps will be rendered obsolete as chips and programs are developed that allow the entire genome of an individual, or parts thereof, to be sequenced cheaply and quickly.
He likens genomics to a sophisticated video game. “You start playing this game,” he said, “killing everything you see or collecting things, and after you’ve killed and collected everything there is and the game seems over, a little box appears in an upper corner. You click on it, and suddenly you’re in a whole new, more complicated level.”
Culture: Science & History
Dr. Mark Neff and his team uncover the surprising origin of a potentially deadly mutation
Until the mid-19th century, any hodge-podge of similar-looking dogs performing similar tasks was awarded the right to be called a breed. However, as inventions (such as guns) mechanized jobs that dogs normally performed, many breeds—like the tumbler, who “tumbled and turned” to mesmerize prey—simply sank back into the ancestral soup, taking their unique traits with them.
One of these ancient breeds, the glacier-climbing Lundehund with its unusual polydactyl triple-jointed toes, survived, but its current population is so small that the breed teeters on extinction’s edge. And a few, like the ubiquitous working collies and spaniels of Great Britain, spawned a number of the breeds created during the prosperous, class-conscious Victorian era. In the age of upward mobility, those on the way up claimed many of the privileges of the upper class, including the luxury of breeding and showing dogs.
More than one-quarter of the world’s estimated 375 breeds were created between 1859, when the first dog show was held in the UK, and 1900, when Westminster and Crufts were well established; even the most subtle differences in weight or color were enough to allow registry of a new breed type. In many cases, the subdivision of farm dogs was an unintended consequence of competitive exhibition in dog shows.
Responding to the shows’ strict criteria for body type, size and color, breeders drew from an increasingly smaller number of founder populations to create dogs who conformed to these standards. Breeding closely related dogs to one another became a popular way to refine a breed, which today means a group of dogs with a common gene pool and characteristic appearance and function.
Unfortunately, the down-side of homozygosity (having two identical genes at a specific location on the DNA strand) is disease and unsoundness. As a consequence of this intense concentration on form, modern dogs suffer from more than 350 genetic illnesses, and today’s breeders bear the burden of restoring their lines to health.
There are no easy answers. Removing affected individuals from breeding populations may decrease the incidence of a particular disease, but smaller gene pools create opportunities for other congenital problems. In cases where an entire breed is afflicted, out-crossing with other breeds means running the risk of losing truly unique traits, such as the Lundehund’s joint flexibility.
Recent research has shown that a single mutated gene, unnoticed for over a century, is responsible for sensitivity to several modern medicines, ranging from ivermectin (a common ingredient in heartworm preventatives) to anticancer agents such as vincristine. These adverse drug responses can cause illness or death in the breeds that harbor the mutation.
A team of researchers led by Professor Mark Neff at UC Davis expanded the results of earlier research by demonstrating that the mutation probably originated in a single generic herding dog who lived in Great Britain in the mid-1800s. This dog must have been a common ancestor of founding dogs for nine different breeds, all of which were found to possess the mutation. Moreover, scientists involved in this study were able to describe the frequency of the mutation in these various breeds, further defining the inherited risk of adverse drug response: Collie (54.6%), Long-haired Whippet (41.6%), Miniature Australian Shepherd (25.9%), Silken Windhound (17.9%), McNab (17.1%), Australian Shepherd (16.6%), Shetland Sheepdog (8.4%), English Shepherd (7.1%) and the Old English Sheepdog (3.6%).
Dr. Neff talks about his research and the implications of genetic testing on the health and well-being of dogs.
Jane Brackman: In addition to helping breeders make informed decisions, your findings provide an opportunity for veterinarians to treat dogs based on their individual genetic profile. What do you mean when you say dogs can be treated with personalized medicines?
Mark Neff: The study of how individuals respond differently to medicines due to their genetic makeup is called pharmacogenetics, and it’s an intense area of investigation in human genetics. Probably all of us are aware of instances where one person responds positively to a medicine and is cured, while another person responds negatively or not at all. These differences are often tied to variation in genes. If we knew the genes that were responsible for side effects, we could identify the individuals at risk and prescribe the medicine that avoids a reaction and still provides relief. The same opportunity exists for dogs. Not all Collies have the mutation; those that don’t can be treated with ivermectin, which is an effective drug for its purpose. The Collies who do have the mutation can be treated with a different medicine.
JB: In dogs with the mutation, what happens?
MN: The normal product of this gene is a protein pump that can eliminate toxic chemicals from the central nervous system, thereby protecting the brain. The mutation causes the pump to be defective. If both copies of the gene are mutated, no functional pump is produced at all, which is the worst scenario. When the dogs are given a drug like ivermectin, which is toxic to neurons in high doses, the drug accumulates in the central nervous system, killing nerve cells. However, dose-sensitivity is an important issue. The smaller dose of ivermectin used to prevent canine heartworm infection, for instance, does not appear to be a problem for these dogs regardless of the mutation, but the higher dose used to treat mange can be fatal in a dog with two defective genes. The dose sensitivity varies by drug as well, so there’s still a lot to be sorted out.
JB: You’ve said that you think there is currently a disconnect between canine genetic research and the application of genetic knowledge. What do you mean?
MN: Breeders and owners are beginning to be inundated with DNA test results, which will only increase in the next few years. There’s an unmet need of genetic counseling that ideally would accompany DNA test results. In addition, we as researchers typically don’t have all the information we need to advise breeders on integrating test results with their breeding strategies. For example, based on our data, we think that both copies of the gene need to be mutated to acquire supersensitivity to ivermectin, but this may pertain to only some of the breeds with the mutation. Sighthounds have very different physiologies from Collies, for instance, and this could alter the effects of the mutation. Science always involves uncertainty, and it’s difficult to convey the ambiguity that remains. Katrina Mealey, our collaborator at Washington State, is continuing the research and adding a lot more detail to this particular story.
JB: In the research article, you advise re-examining how a breed is defined genetically. Would you elaborate?
MN: This is a statement more for academic geneticists than for breeders and owners. There’s a lot of scientific work going on now that neglects the fundamental fact that dog breeds are not natural species, but rather, have evolved through selective breeding and intentional outcrossing to produce new combinations of traits and hence new breeds. Most studies describing breed relationships use statistical and computational tools that were developed to describe relationships between species with distinct lineages. These tools are inappropriate for analyzing breeds of dog. Our paper showed that an identical mutation existed in two very different types of dog, two sighthounds and seven herding breeds. Conventional tools would have almost certainly missed the relatedness of these breeds.
JB: Your research identified seven affected herding breeds, which were mostly developed after the mid-19th century, and provided evidence that these breeds are in fact closely related. How did you draw those conclusions?
MN: The herding breeds, whose origins were in Great Britain, all shared the mutation, indicating that they had common ancestors. This implies that these types of dogs were mixing, presumably before registries were established. If the mutation was shared by these breeds, there probably are many other genes also shared. Great Britain in the 1800s appears to have been a real melting pot for dog genes, and this has been substantiated by subsequent work in our laboratory.
JB: Why is it important to know the history of a genetic mutation?
MN: Because the information may tell us something about the distribution of the mutated gene, and key us into where we might look to find additional affected breeds. For instance, if this particular mutation had been ancient, we would have predicted that many more breeds would have had it. Given all the breeds that exist worldwide, and that only a small fraction of these were affected by the mutation, we can infer that the mutation is relatively young. The mutation probably arose in the mid-1800s, but this is speculative. Reconstructing history, genetic or otherwise, always involves an incomplete data set—you never know what’s been lost.
JB: Should breeders genetically test their breeding stock, and if so, how should they apply the test results?
MN: Breeders have it hard—when they make decisions, they have to consider what’s good for the breed, their bloodline and individual dogs. If the mutation frequency is high in the breed, like it is with Collies and Long-haired Whippets, testing and selective breeding is certainly worthwhile to reduce the frequency and decrease the breed’s risk of drug sensitivity. In a breed where the mutation is relatively rare, such as the Old English Sheepdog, the owner might test only those dogs that are scheduled for treatment with one of the interacting drugs. But it gets complicated when a single breeder’s bloodline is heavily affected; breeders cannot give up their entire breeding stock, so a more gradual approach must be taken. What a breeder should do really depends on the specific situation.
I certainly believe that eliminating mutations from gene pools requires greater debate. Many scientists have suggested that a mutation should be removed from a gene pool gradually so as to preserve genetic diversity in the breed. I think ulterior motives are sometimes at work, as this is most strenuously advocated by service laboratories that offer these kinds of tests. DNA tests should be targeted for obsolescence—ultimately, a mutation should be eliminated from the gene pool, which of course renders the test meaningless. Don’t get me wrong—there is enormous value in preserving genetic diversity across breeds, but most of the diversity in one breed exists in related breeds, so conservation genetics within a breed is not a critical issue. I’m certain that far more genetic diversity is lost from “popular sire” effects and line breeding than from adherence to DNA testing.
JB: When I think of conservation genetics, I think of bringing a species back from the brink of collapse, or more generally, the practice of making a species healthy again. Do you mean that preserving genetic diversity in dog breeds is not critical because the way you create a breed in the first place is by eliminating diversity?
MN: That’s right. The normal rules of conservation genetics don’t apply to artificially selected populations. For instance, there appears to be an advantage in nature for individuals to have a lot of genetic variation in at least one region of the genome—the MHC—that arms the body’s self-defense. It appears that individuals may actually select mates in part based on being genetically different for genes at the MHC. In dogs, we have obliterated this selection because dogs don’t get to choose their mates.
There is an enormous difference between a species that breeds and evolves naturally and one whose breeding and evolution are controlled by humans. The irrefutable fact of closing a gene pool by enlisting dogs to a closed registry to suspend change in a breed is that diversity is being lost, and there’s little or no opportunity to create new diversity. Mutations are incredibly rare, at least those that have effect, and there isn’t any new blood coming into these populations.
JB: So trying to “conserve” diversity, for instance, by not strictly adhering to a DNA test result, doesn’t make much sense to you?
MN: There’s nothing more important to the survival and adaptability of a species than genetic diversity. What I’m saying is that it seems incongruous to hold adherence to DNA testing to a different standard when the gene pools of these breeds have been closed and breeders are striving for conformation to a standard. I’m not sure I’m aware of a single instance where dogs have been brought in to add new “blood” to a breed.
JB: You said that in many cases, even when breeds are crossed with a dissimilar breed, it doesn’t take too long to re-establish the breed’s classic look and behavior. Why is that so?
MN: Most breed-defining traits are shared by multiple related breeds. For example, I would predict that the genes for pointing behavior are common to perhaps a dozen or more pointing breeds. So one could resurrect a breed by bringing together the right combination of genes from related breeds. This won’t always work because there are some characteristics that truly are unique, such as polydactyly in the Lundehund.
What makes breed development rapid is that most selected traits are tied to genes of big effect. So instead of moving a hundred genes of small effect through selective breeding, one only needs to move two or three. I’m speculating on this last part. We don’t entirely know this, but it’s a reasonable guess.
Culture: Science & History
How a special little dog made America’s house his home
Arguably the most important dog in World War II never saw combat; in fact, he was one of the breeds deemed unfit for duty by virtue of his stubby legs and long coat. But he was also of a breed that had been considered suitable for a gentleman to keep in town since the mid-19th century, and in President Roosevelt he met the perfect human companion.
Roosevelt’s cousin, Margaret “Daisy” Suckley, brought a small six-month-old black puppy, a gift from Katharine Davies, to the White House on November 10, 1940, just after Roosevelt’s historic third victory. Suckley had already trained the Terrier, named Big Boy, to sit, roll over and jump in exchange for food, and those seem to have remained his only tricks. Charm he doubtless learned from the dog-loving Roosevelt, who had long desired a canine companion in the White House after his big dogs were deemed safer in Hyde Park than in Washington, where they might have threatened government employees and diplomats, as his distant cousin Teddy’s had a quarter of a century earlier. Roosevelt renamed the Scottie Murray the Outlaw of Falahill, after an ancestral Scottish rogue, and soon shortened that to Fala.
The dog became Roosevelt’s inseparable companion, according to Doris Kearns Goodwin in her book on Eleanor and Franklin during the war years, No Ordinary Time. He slept in a chair at the foot of the bed, camped out in the study, and traveled around the country and various parts of the world. Around the White House and even on the road, Fala often served as a herald for the president. Goodwin reported that while Roosevelt toured the Midwest and South in 1943, Suckley tended Fala on his walks from the president’s private train car, the Ferdinand Magellan, and crowds actually watched for the dog. His appearance alone seemed to give many people a sense of security, because it was a sign that Roosevelt was on the move, present and vital, watching over the country and them. Although most Americans were unaware of the extent of Roosevelt’s paralysis, he could not walk freely among them, so in a sense Fala, although on a scale much smaller but oddly more intimate than that of the indefatigable Eleanor, was a physical projection of Roosevelt into the world, another small element in the illusion of vigor.
The dog was spoiled from the start. Shortly after joining the White House, he was hospitalized for digestive problems, due, it was said, to a surfeit of rich snacks from the White House staff, not to mention the Roosevelts and their many guests. After Fala’s return, Goodwin said Roosevelt decreed that no one but he could feed the dog, to prevent a relapse and obesity, but the edict must have been largely honored in the breach, for other reports reveal that Eleanor fed Fala cake when he performed, and in the fall of 1942 a movie crew making a film of his life as the “first dog” seduced him with bacon, which made him sick. The crew was not banned as a result. Roosevelt did use “feeding time” and Fala in general as a way to choreograph his entry to meetings—imagine the reaction of dignitaries kept waiting for Fala.
On October 15, 1944, at the height of Roosevelt’s final presidential campaign, John Crider wrote in the New York Times that “what is difficult for some folks to understand is that Fala is no longer just a dog; he is a personage.” Fala, he explained, attended international conferences, wrote letters, greeted guests, and had an “official biographer in the person of Miss Margaret Suckley.” A visitor to the White House on at least one occasion saw the door open, heard the steward announce “the President of the United States,” and watched Fala enter the room, tail wagging. Fala was friendly toward everyone, Crider said, without adding that the trait is invaluable in a politician. Many of the thousands of letters Fala received involved requests for his services as a stud—politely couched, of course—for the writer’s dog. Although Fala’s attendants rejected all such requests, in late January 1945, Suckley did mate him successfully with her Scottish Terrier Buttons. But there was no postcoital bliss; the two fought so viciously afterward that both ended up in the veterinary hospital for sutures.
Often perched on the backseat of the president’s open car, by Roosevelt’s shoulder, Fala campaigned in cities around the county. He was aboard the Prince of Wales when Roosevelt and Churchill signed the Atlantic Charter in 1941, bringing the United States closer to open war. At the first Quebec Conference, on August 17, 1943, Fala rode in an open car with a Secret Service agent, right behind the car carrying Roosevelt and Canada’s governor general and just ahead of the one with Churchill and Canada’s prime minister, W.L. Mackenzie-King. The following summer, Roosevelt and Fala traveled by train and ship to Honolulu and on their return, stopped at the Aleutians, secured just the year before. Fala then attended, less visibly, the second Quebec Conference, where Roosevelt and Churchill discussed the future of Germany, whose defeat was clearly in sight.
That secret stop at Adak Island in the Aleutians set in train a series of events that led to Fala’s finest moment, a speech that opened and arguably ended the 1944 presidential election. In a speech to the Teamster’s Union in Washington, D.C., Roosevelt cut loose with this salvo: “These Republicans have not been content with attacks on me, my wife or on my sons. No, not content with that, they now include my little dog, Fala. Well, of course, I don’t resent attacks, and my family doesn’t resent attacks, but Fala does resent them. You know, Fala is Scotch, and being a Scottie, as soon as he learned that the Republican fiction writers in Congress and out had concocted a story that I had left him behind on the Aleutian Islands and sent a destroyer back to find him—at a cost to taxpayers of two or three, or eight or twenty million dollars—his Scotch soul was furious. He has not been the same dog since.” The comments on Fala had brought down the house and everyone listening on the radio. Although some pundits attempted to keep the election close, it was clear that Roosevelt and Fala had turned the tide, exposing the pettiness of the Republican campaign, making a mockery of Dewey and his minions.
In the wake of what became known as the Fala Speech, the Scottie became an icon as well as a “personage.” At a White House Conference on Rural Education that drew 200 educators to the East Room on October 5, Austin R. Meadows of Alabama abruptly laid aside his text in mid-speech and said, “The folks back home really only wanted me to say hello to Fala.” After 15 minutes, Fala appeared, accompanied by a steward who gave Eleanor a plate with pieces of sponge cake while the educators scattered chairs, clapped, laughed and squealed with delight. “A group of dignified school officials had suddenly become a bunch of care-free high school kids,” the New York Times reported. Fala ignored Eleanor until he got a snort of the cake, and then came running. He rolled over and stood up on his legs to beg, but the floor proved too slick for him to jump successfully.
Roosevelt received 53.5 percent of the popular vote, for 432 electoral votes, a smashing victory that Fala, apparently upset by the election night crowd at Hyde Park, did not greet with his usual aplomb. Roosevelt did not live to experience the greater victory in war. He died on April 12, a month before Germany’s surrender and four months before the atomic bombs forced Japan’s capitulation and ushered in a new age. Fala went briefly to live with Suckley, as Roosevelt had requested before his death, but she soon returned him to Eleanor, who enjoyed his company and ultimately took in one of his grandsons to be his companion in old age. The two lived at Val-Kill, the cottage on the Hyde Park estate she had donated to the government, and Fala appeared periodically in the news. He was present when dignitaries like the victorious Eisenhower and the imperious Charles de Gaulle visited Hyde Park to lay wreaths on Roosevelt’s grave.
In July 1946, Eleanor, the great champion of equal rights and integration, traveling with her dog in the grand American tradition, found herself at a Portland, Maine, hotel that refused to let her keep Fala in her room. She promptly canceled the reservation and spent the night in a “tourist cabin.” That bit of Fala and Eleanor lore capped the front-page New York Times obituary announcing the death on April 5, 1952, of “the rakish little black Scotty who sat in on the making of history …” Euthanized just shy of his twelfth birthday, and of the seventh anniversary of Roosevelt’s death, Fala was buried in an unmarked grave in the Hyde Park rose garden at the feet of his “master and constant companion for five years.”
The language underscored Fala’s particular and general significance. Despite people and establishments who refused to welcome dogs, they had made the transition, like America itself, from the country and the yard to the city and the home. They had become not just dogs but personages, and their masters and mistresses were “companions.” Fala was an exceptional dog, of course, and the dog wars are not over to this day. People continue to abuse and abandon their animals and to breed dogs to satisfy their own vanity or to make profit. But a shift in perception, long underway, had become fixed in the collective psyche, as surely as America had changed from a predominately rural society through the Depression to an urban and suburbanizing society after World War II.
Extracted and adapted from A Dog’s History of America: How Our Best Friend Explored, Conquered, and Settled a Continent by Mark Derr; published by North Point Press, a division of Farrar, Straus and Giroux, LLC. © 2004 by Mark Derr. All rights reserved. Used with permission.
Culture: Science & History
Breeding for looks, not function, threatens dogs’ well-being
Like many people, my wife Diana and I had long been in the habit of buying purebred dogs without bothering to learn much about their breeding beforehand. And so it was in 1977, when we made an impulse purchase of a Jack Russell Terrier named Phineas.
Despite the many other wonderful dogs who’d blessed our lives, we’d never known another like Phineas. Though short-legged and weighing barely 15 pounds, he thought he was 10 feet tall. And never had we known such a hunter! He became our “Orkin Man,” dispatching gophers more efficiently than any other predator.
Yet it turned out that Phineas wasn’t purebred after all. He was what old-time Terrier people called a sporting dog—a mixed-breed of indeterminate ancestry whose forebears had been bred and judged not on beauty, conformation or pedigree but on their ability to hunt. In fact, many JR owners in those days called their dogs “glorified mongrels.” And indeed, Phineas seemed to be a generic mutt who represented the wonderful qualities of all dogs: He was “Pete the Pup” in the 1920s Our Gang movies, with a painted black circle around one eye, and “Nipper,” the Fox Terrier who listened to “His Master’s Voice” on old RCA Victor records.
We loved this mutt-like quality. And although Phineas lived just a year—tragically falling victim to a coyote trapper’s poison—we were smitten with JRs. Five more generations would follow him into our hearts during the next 30 years. And while none was exactly like Phineas, each embodied the same “doggie” qualities we loved. JRs, we realized, don’t just look like generic dogs, they share all dogs’ past and future as well.
Bred for the Task
Fox hunting required dogs: long-legged Fox Hounds to chase the fox and smaller Terriers to go underground after the fox when it dove into its den. The Terrier’s job was not to kill the fox but to drive him out of his hole so the chase could continue. This was the Terrier’s vocation. The name, derived from the Latin word terra, meaning “earth,” signified the dog’s function. But it also symbolized the role that land played in the ancient and ubiquitous partnership between dogs and humans.
While there is no consensus among scientists as to just when or how this partnership began, somewhere between 27,000 and 12,000 years ago (depending on the estimate), dogs and people first learned the mutual advantages of cooperation. Some believe it occurred after early people discovered how to breed wolves for tameness. Others say that the wolflike ancestors of modern dogs simply found that scavenging in villages and joining human hunts were more reliable ways to find food than killing game themselves. But however this relationship began, people soon learned it was to their advantage to take dogs as hunting partners. A few thousand years later, the advent of agriculture offered still more ways to cooperate. In exchange for food and shelter, dogs herded and guarded livestock and killed varmints that threatened crops. And by working on the land together, dogs and people became companions.
Over time, the land shaped the dogs. Bred by farmers, herders and hunters from different regions, they developed varying skills and conformations. But these early people did not create breeds in the modern sense. They didn’t insist that dogs only mate with others descended from the same foundation ancestors. Rather, they kept types of dogs, such as Shepherds, Hounds, Spaniels, Retrievers and Terriers—dogs defined not by pedigree but by what they did and where they lived.
Such was the evolution of Terriers, as their owners custom-bred dogs to fit their own requirements. By 1800, this crossbreeding had produced, among others, a type of dog known as the Fox Terrier. But although its long legs were perfect for chasing foxes overland, they were a disadvantage for underground work. Fox Terriers who spent too long in a hole suffered terrible cramps and even crippling disabilities.
Russell saw this problem. Even while a student at Oxford, he realized that fox hunters needed a special kind of Terrier—one tough and brave, an expert excavator able to stay underground for extended periods, with short legs and a narrow chest that could squeeze through tight spaces. Then one day in May 1819, Russell met a milkman with just the dog he was looking for. Her name was Trump, and during the remainder of his life, Russell bred Trump and her descendants to any Terrier he could buy or borrow who approximated his ideal. He didn’t care about pedigree or papers. He just wanted dogs who did the job. This produced a line of small, brave Terriers perfectly suited to go to ground after badger, otter and fox.
Indeed, as every “MFH” (Master of Fox Hounds) had his or her own idea of the best Terrier for the locality, depending on soil, weather, kind of quarry and style of hunting, each—like Russell—experimented with various crosses to produce the best dog for the conditions. In Derbyshire, where hunts covered great distances, longer legs were favored. In the wintry Lake Country, rougher coats predominated. Huntsmen accustomed to carrying the Terrier in a saddle-mounted bag until they put him to ground preferred shorter dogs.
Given the various needs and conditions and the variety of bloodlines introduced, Terrier strains proliferated. Besides types known today, many others, now rare or extinct, appeared as well, including Jones Terriers, Trumpington Terriers, West Wilts Hunt Terriers, HH Hunt Terriers, Scorrier Terriers, Hucclecote Terriers, North Devon Terriers and Ynysfor Terriers.
The genes of many of these strains eventually found their way into the Jack Russell as well, producing a dog who came in virtually infinite variations. But whether short or tall; bowed- or straight-legged; “smooth”-, “broken”- or “rough”-coated; long-muzzled or short-muzzled—they shared a reputation for bravery and endurance that captured the respect and attention of an entire generation of English sportsmen.
Soon, American fox hunters discovered Reverend Russell’s Terriers and began acquiring them. And they, too, outcrossed to produce those best suited for local conditions. They did not adhere to a “closed stud book,” which stipulated that dogs could only be mated with others descended from the same foundation ancestors. So local differences proliferated and the little dog’s genes became progressively more diverse.
Among the casualties of this whirlwind were hunting and working dogs. Without a rural culture, there was little left for them to do; so, with the death of one came the transformation of the other. A new kind of dog buyer emerged, an urbanite who wanted pets and companions, not farm animals or hunters.
The earliest visible sign of this change were dog shows, the first ever held in England in 1859 at Newcastle-on-Tyne. Three years later in Birmingham, England, Fox Terriers competed prominently for the first time. By the 1880s, dog shows were wildly popular on both sides of the Atlantic. And as they multiplied, so did breeder associations, which set conformation standards and kept pedigree registries. These groups joined to form national kennel clubs to coordinate their activities, promote their dogs and organize shows. England’s Kennel Club was formed in 1873 and the American Kennel Club (AKC) in 1884. (The first U.S. show—New York’s Westminster—was held in 1877, sponsored by the Westminster Kennel Club.)
With the advent of dog shows and breed clubs came a whole new idea of what the perfect dog should be. Whereas sporting dogs were judged by their stamina, hunting ability and courage, show dogs were measured by their beauty, style and how closely they supposedly resembled their progenitors. Breeders sought to produce dogs with perfect form. They wanted uniformity in appearance, which could only be achieved by closing the stud book. A Sealyham or Scottish Terrier must have parents who are Sealyhams or Scotties, and so on back to their foundation stock, somewhere in the mists of time.
Unfortunately, closing the stud book inevitably leads to what biologist Raymond Coppinger would later call “an evolutionary dead-end”:
Sexual isolation from the greater population of dogs leads almost inevitably to dire consequences for those dogs that get trapped in a pure breed .... Once the stud book is closed on a breed, it is unbelievable how fast they become inbred …They are caught in a genetic trap.
The purpose of such close breeding was to replicate dogs, ensuring that they resembled their parents as closely as possible by reducing genetic variability. But rather than preventing change, this hastened it. By reinforcing familial genes, close breeding not only increased chances the pups might share desired characteristics—the same head shape or coat color, for example—but also made it more probable that they’d share undesirable traits as well, such as the same allergy or propensity for kidney disease. And since no one knew what all the genes did, reducing their diversity put affected animals at risk in the same way that today, the lack of genetic diversity threatens cheetahs with extinction, or declining biological diversity imperils the health of natural ecosystems.
Consequently, Pearce noted, many purebred Terriers had become “poor, craven, shivering, shy, nervous animals, destitute of any qualification for the active, hustling, neck-or-nothing life of a country gentleman’s companion.”
Pearce and his contemporaries had a right to worry. Show breeders were changing the character, conformation and abilities of dogs as they sought to follow the fluctuations of fashion. “The better bred [Fox and Sealyham Terriers] are, of less value they are for work,” wrote J.C. Bristow-Noble, author of Working Terriers in 1919. Few of his “well-bred” dogs were “of use for real work,” he wrote. “Their noses were far from true, all grew to too large a size, particularly the Sealyhams; all lacked stamina, courage, and intelligence … so at length I gave up the attempt of making workers out of pedigree Terriers and confined myself to building up a strain of workers from crossbred Terriers.”
In 1931, the famed Terrier expert, Sir Jocelyn Lucas, noted that “the show bench is ruining Sealyhams as a worker” and lamented the “post-[First World] war craze for enormous heads.” Cairn and West Highland Terriers bred for show, Lucas reported, had become too “nervy to be a success underground.” The “show bench” he also said, has “ruined” Dandie Dinmonts and they, along with Cairn, West Highland and Scottish Terriers, are “chiefly known for show or as companions, for which latter purpose they are well suited, since they are very nice dogs, take up little room and require little exercise.”
To be sure, many nonsporting dogs were nice. In fact, they often made better pets. Sporting dogs were not for everyone—not even for most people. Bred to find, chase or kill game or varmints, they were too aggressive. They had more energy than their owners could tolerate, requiring virtual marathon runs to give them sufficient exercise to prevent their tearing the family sofa to shreds.
Jack Russells had all these faults. What concerned people like Lucas was not that show dogs were undesirable but that they threatened the future of sporting dogs. As more dogs were bred for pets and show, sporting-dog numbers declined. Would, they wondered, sporting dogs—and most important, their qualities of courage, strength, stamina, hunting ability and genetic diversity—eventually disappear altogether?
Driven by Demand
Each breed club began to promote theirs as “ancient”—a living relic of an earlier time. Making these claims required maintaining the myth of direct descendancy from the “original” dogs. Yet such “original” dogs never existed. The very concept of a breed—dogs whose reproduction was carefully restricted via a closed stud book to dogs descended from the same foundation stock—was an invention of the breeder associations.
However mythical, these claims of old lineage tapped the wellspring of show dogs’ appeal. For while we may love our dogs whether they’re deemed “ancient” or not, imagining them as relics of an early, pastoral way of life resonates within us. No matter where we live or what we do, love of the land is in our blood. For millennia, dogs and people lived on the land, working, herding, hunting, defending, rescuing. And when people began moving to cities, they yearned for the pastoral way of life all the more. They still do. Dogs preserve for us an emotional connection to our bucolic past that remains in memory and imagination. And when they demand that we take them for walks, they reawaken this connection. They become guides in a journey to rediscover our own genetic roots.
By the 1950s, the working- and show-dog cultures were following entirely separate paths, isolated from—and often hostile toward—each other. But demographics were on the side of the show dog. As the century wore on, show dogs waxed as working dogs of all kinds, from Shepherds to Terriers, waned.
Meanwhile, paradoxically, in England, JRs were becoming wildly popular. Even while they remained favorites of fox hunters, the feisty Terriers had been discovered by the working classes as well. Some took them as pets and others put them to work killing rats, stoats and rabbits. The new owners began breeding them for such a variety of jobs that “the mongrelly Jack Russell,” as Terrier historian D. Brian Plummer put it, “became even more mongrelly.”
“The first hunt Terrier shows I attended in the 1950s,” Plummer wrote, “were indeed extraordinary sights, with the most amazingly variable types of dog being proudly shown as genuine Jack Russells; some of them displayed hints of Collie, or, not infrequently, Dachshund, in their lineage. Many were quite hideous, but handsome is as handsome does, and some of those monstrosities proved to be incredibly good workers.”
Nevertheless, this mongrelly drift troubled many Jack Russell fanciers, and in 1974, to counter it, they formed the Jack Russell Terrier Club of Great Britain (JRTCGB), appointing Plummer as its first chairman. The club’s first task was to define the breed and set conformation standards. And the result was chaos. “Near-riot prevailed” at those early meetings, Plummer later recalled. Nevertheless, they did set a “standard of sorts.” At the beginning, Plummer wrote, “any dog that conformed to a rough description of a Jack Russell Terrier was eligible for registration in the initial register.”
Likewise, two years later in America, Terrier enthusiast Mrs. Harden L. Crawford III, having acquired her first Jack Russell from a friend at the Essex Hunt and fallen in love with the little dog, founded the Jack Russell Terrier Club of America (JRTCA), dedicated to preserving the sporting qualities of the Terrier. Recognizing the importance of diversity, the club refused to close the stud book or set narrow conformation standards, and resolutely opposed recognition by the AKC, whose breeding practices would turn the JR into a show dog.
But neither of the original English and American clubs was entirely successful in fending off those determined to transform the JR into a pure breed. In 1983, in England, some of these advocates founded their own club, closed the stud book, drew up conformation standards and applied for Kennel Club membership. Likewise, a year later, some American JR advocates founded a similar organization, eventually called the Parson Russell Terrier Association of America (PRTAA); according to its website, this was done “in response to growing concerns that the breed was being misrepresented as a short-legged Terrier.” Dedicated to “continuance of the traditional, purebred Parson Russell,” it closed its stud book, established breed standards and applied for membership to the AKC.
“After some 90 years,” wrote Reverend Russell’s biographer, Gerald Jones (using the pen name “Dan Russell”) in 1979, “there can be none of the original Russell blood left today. Even if one could trace a Terrier’s pedigree back to Russell’s dogs, there must have been so many outcrosses that the original blood would have been thinned to the vanishing point. If one had bred true, one would now be producing half-wits.”
Certainly, none who knew Russell believed any such thing as a “pure” or “original” Jack Russell ever existed. As Lord Paltimore (whose father and grandfather had been close friends of Russell) explained to Lucas, “It is entirely misleading to talk of a ‘Jack Russell’ Terrier. Mr. Russell always said that he had no special strain of Terrier. If he saw a likely dog he would acquire it, and if suitable in his work he would breed from it, but he never kept any special strain.”
But although the breed clubs’ depiction of the “Parson Russell” rested more on myth than on historical fact, the image it created—of the leggy dog as the “original” JR—continued to build. In 1992, the television sitcom Frasier debuted, featuring a Jack Russell named “Eddie,” and in 1995, the PBS children’s program Wishbone appeared, about a JR who traveled through history wearing period costumes. These programs showed Jack Russells as terribly appealing, but by depicting them living in apartments and wearing skirts, they also grossly distorted the dogs’ true character.
Believing Jack Russells to be cuddly couch potatoes and good with children, the public flocked to them, often with tragic consequences for both dogs and people. Children were sometimes bitten, the family cat killed or other pets mauled. Soon, JR rescue organizations, dedicated to finding second homes for rejected dogs, had more than they could handle.
The public, in short, had fallen madly in love with Jack Russells, but wanted them as gentle pets, not feisty sporting dogs. And this popularity vastly accelerated the Terrier’s transformation into a modern show breed. In 1990, the Parson Jack Russell was recognized by Great Britain’s Kennel Club, and in 1997, its American counterpart was accepted by the AKC.
Following their own misreading of JR history, Parson Russell breeders set standards designed to produce taller and gentler dogs. None were allowed under 12 inches. Only smooth and broken coats were permitted (even though most of Russell’s had rough coats), And, since the parson’s own dogs were, they declared, “bold though cautious,” they decreed that submissiveness in the modern breed “is not a fault” while being “quarrelsome” is. “Overt aggression towards another dog” they deemed a disqualification.
Yet by stipulating taller Terriers, the PRTAA had ignored the advice of countless early JR people, including that of Russell’s friend and neighbor, Alys Serrell, who advised that “a leggy dog is of little or no use for underground work.” And its emphasis on less quarrelsome or aggressive dogs merely seemed to confirm what Pearce and other early Terrier people detested most—that show breeding not merely undermined a dog’s sporting ability, but its fighting spirit as well.
So, not surprisingly, although the Parson Russell’s stud book was closed less than 25 years ago, the dogs are already losing much of their once-glorious diversity. Many look mass produced—spindly dogs too tall for serious underground work and with monotonously similar coats and conformation. Certainly these “spiders,” as some critics call them, are less robust than Russell’s biographer “Otter” Davies’ description of Trump, whose “loins and conformation of the whole frame [were] indicative of hardihood and endurance.”
The transformation of the Parson Russell from mixed to pure breed parallels the history of all purebred dogs, and serves as a warning of the dire future that awaits them. For while many breeders take great care not to breed too closely or propagate inherited diseases, once the stud book is closed, even the most careful line breeding merely postpones the inevitable.
Already, veterinary pathologist George A. Padgett has found 532 diseases afflicting purebred dogs. Over two-thirds of Newfoundlands are born with a genetic defect, he says, as are 40.3 percent of Cairn Terriers, 29.8 percent of Bichon Frisé and 33.5 percent of Scotties. Others report that 30 percent of Dalmatians are born deaf. Borzois have been bred to have noses so long that some pups have difficulty suckling their mother’s teat. Many Norwich Terriers, Bulldogs and Boston Terriers can only be whelped by cesarean section. “A modern Bulldog,” according to Keith Steward Thomson, former president of the Academy of Natural Sciences, “more resembles a veterinary rehabilitation project than a proud symbol of athletic strength or national resolve.”
Aggravating this tragedy, says Padgett, is breeding of what he calls “matadors” (e.g., Blencathra Badger)—show-ring champions who “produce large numbers, perhaps hundreds or even thousands, of offspring.” Equally destructive is the belief shared by many breeders that any dog who wins in the show ring is “breedable”—an idea that, he says, is “just plain dumb. No. It’s not dumb, it’s stupid!”
Mixed Breeds Are the Future
When a beloved dog, whatever its breed, dies, we seek to find another just like him. So we go to a breeder and buy a replica. By doing so we convince ourselves that our departed dog continues to live in the soul of the new one. We think we have purchased his immortality. But we haven’t.
Purebreds represent neither dogs’ past nor their future. As geneticist Richard Dawkins tells us, genes are nearly “immortal.” So those of purebreds are no older than those of mongrels. A dog’s true connection with the past lies in his character and abilities, not his genes. For millennia, dogs were defined by the jobs they did, and crossbred to ensure they would continue to perform them well. When the rural people who created these jobs disappear, dogs lose this past, and attempts to freeze their shapes in time through inbreeding do not preserve it. They merely rob dogs of a future.
Purebreds can be saved only by opening their stud books. Just as the meek shall inherit the Earth, so lowly mixed breeds, including perhaps the few remaining crossbred Jack Russells, represent the future of dogs.
This article is an adaptation from the author’s new book, We Give our Hearts to Dogs to Tear: Intimations of Their Mortality (Transaction Publishers), a memoir of the Chase family’s 32 years in Montana, which they shared with successive generations of Jack Russell Terriers. The book considers the mortality of, and connections between, the land and dogs: how suburbanization and declines in land stewardship threaten the former, and indiscriminate inbreeding by show dog breeders imperils the latter.
Culture: Science & History
Sniffing out the facts and exploring the relationship between our two species
No observer can help but remark upon the incredible variety of sizes, shapes, temperaments and behaviors of the dog—from the one-pound Chihuahua to the 200-pound Mastiff; the stubby-legged, placid Basset Hound to the long-legged, fleet Greyhound. Nowhere else in the animal kingdom does so much morphological diversity exist within a single species.
In large measure, the 400 or so breeds of dog extant today are products of human breeders, who, as Charles Darwin pointed out nearly 150 years ago, have selected consciously and unconsciously for specific physical and behavioral traits. But dogs are also the products of 40 million years of canid evolution through natural selection. The forces of evolution created the unique physiological and behavioral characteristics— the senses, physical abilities, social and individual behaviors and brains—that made the wolf the ideal progenitor of the dog. Those attributes resonate in human myths from around the world that ascribe to canids wild and domestic central roles in the creation of humans, guarding the dead or guiding them to the afterlife and serving as intermediaries between humans and nature.
Various legends of the dog as a fell beast and spreader of violence and disease are also widespread, reflecting a less exalted place in human affairs. But it is the diversity and malleability of canid characteristics that have made dogs indispensable allies of humans for more than 100,000 years—longer than any other domestic animal.
From an evolutionary perspective, the diversity found in the domestic dog echoes trends in wild canid evolution, albeit on a much different time scale. Rising from a common ancestor, new species of wild canids spread over millions of years into nearly every type of habitat on Earth. Today, 35 species of canids are found on every continent but Antarctica. However, centuries of persecution to protect domestic livestock and harvest furs and trophies, along with habitat destruction, have brought several of those species, including the African wild dog and the little Ethiopian wolf, close to extinction. Other species, like the gray wolf, have been extirpated from much of their historic range. Yet the dog, the coyote and some foxes continue to flourish. The signal difference is that dogs have evolved almost exclusively through artificial selection by humans while wild canids have evolved through natural selection.
The full details of canid evolution, including development of the dog, remain unclear because of the incomplete nature of the fossil record, but what we do know reveals how a remarkable group of predators evolved and what they have meant to the natural and built worlds. In an effort to capture this rich story, the Natural History Museum of Los Angeles County has created an interactive multimedia exhibition exploring canid evolution and the role of dogs in human societies. As scientific advisors of “DOGS: Wolf, Myth, Hero & Friend,” we will be working on a book to accompany the exhibition.
The exhibition and national tour is made possible by Pedigree® Food for Dogs and is supported by a generous grant from the National Science Foundation. The exhibition premieres at the Natural History Museum of Los Angeles County on October 13, 2002, and over the next five years is scheduled to travel to San Diego and San Bernardino, California; Seattle; Mesa, Arizona; Omaha; Washington, D.C; Milwaukee; Philadelphia; Cleveland; and Chicago, with more cities to be announced.
The evolutionary history of dogs begins some 40 million years ago in North America, when Hesperocyonines, looking like a cross between a fox and a weasel, emerged from the soup of carnivores. Hyena-like canids, the Borophagines, or “bone-eaters,” with bone-crushing jaws, followed and persisted until around 2.5 million years ago, when the last one vanished.
The ancestor of today’s canids arose in North America 8 to 12 million years ago and looked like a fox. Within a million years, that animal crossed the Bering land bridge into Europe and diverged into a number of new species, including the gray wolf, which later migrated back into North America. Some 3 million years ago the first ancestral dogs and cats reached South America by way of the Isthmus of Panama. Finding a paradise full of prey and free of competing predators, the canid invaders soon radiated into several new species, each adapted to South America’s unique habitats. Alone, the voracious, diminutive bushdog of today’s Amazon rainforest brings down pacas larger than itself. The maned wolf is often called the “fox-on-stilts” because of the disproportionately long legs that allow it to peer over the tall grass of the pampas. The hoary fox and the crab-eating fox also emerged at this time.
The 35 species of living canid include the gray wolf (the largest), the coyote, the jackal, the African wild dog, the Ethiopian wolf, the fox, the dhole and the raccoon dog. Although so closely related to the gray wolf as to be the same species, we continue to call the domestic dog, Canis familiaris, a separate species because it is nearly always reproductively isolated, is subject to artificial selection and only exists in the wild as a feral animal, like the dingoes of Australia.
Dog breeds, however, are not considered separate subspecies because without human interference they freely interbreed, within size constraints. Most breeds were created during the past 200 years, not nearly enough time to cause a significant genetic divergence. Artificial selection by humans only involves concentrating traits already present in the wolf/dog genome—morphological characteristics like size and coat color, and behavioral features like herding, hunting, retrieving or guarding. In addition, certain types of genetic exoticism—dwarfism, giantism, and neoteny, or the retention of juvenile features into adulthood—have been fixed through selective breeding.
What Makes Diversity Possible
Canids cover much of the dietary field, from the highly carnivorous wolf, dhole and African wild dog to the insectivorous bat-eared fox and the largely frugivorous raccoon dog of Japan. There are also generalist munchers, like foxes, coyotes and, of course, dogs. Yet even the wolf will eat grass and fruit, though perhaps not as much as dogs, and feed on prey ranging from moose to mice.
Canids can do that because, on the whole, their teeth have not evolved to perform specialized tasks, like crushing heavy bones (in the hyena) or grinding grasses and grains (in herbivores). Canids have in addition to the distinctive canines, carnassial teeth for shearing and molars for crushing—a sort of broad-based dentition that allows them to consume a wide variety of foods. In domestic dogs, tooth size is reduced, as are jaw strength and overall relative size, probably as a result of relaxed selection for these attributes relative to wild canids. Still the dog’s varied and sometimes eccentric culinary choices reflect the ability of canids to adapt to the available food.
The social nature of wolves provides the evolutionary template for dogs. Wolves are highly social and live in a complex society maintained by systems of communication, cooperation, and aggressive and submissive behaviors. They exist in small family units consisting of a single reproductive (dominant or alpha) mated pair and their adult offspring from consecutive years. Some packs may also contain non-relatives or “strangers.”
Generally only the alpha pair reproduce, while adult offspring assist in all aspects of pack life including hunting, provisioning and guarding of offspring, defending pack territories, and attending to the den. Such packs maintain territories and aggressively repel interlopers—so aggressively, in fact, that interpack aggression may be the largest cause of non-human-induced mortality among wolves.
These wolfish behaviors are a kind of pre-adaptation for human/dog relations. Dogs can be readily submissive to their owners, but show various degrees of aggression toward strangers or territorial interlopers. They form long-term bonds with humans, as they would often do in a pack or with mates, and show cooperative and altruistic behavior, sacrificing for humans just as they would for kin.
How Old Is Our Oldest Friend?
But there is new evidence that the archaeological record does not tell the full story of the dog’s origin. Research by one of us (Robert Wayne and colleagues) on mitochondrial DNA, inherited through the mother and involved in the cell’s energy system, indicates that genetically the dog split from the wolf perhaps over 100,000 years ago and today differs in genetic (DNA) composition from the wolf by no more than 1 percent. This finding suggests that behavioral features may have been key in the domestication process and indicates that for much of the history of anatomically modern humans, there have been dogs.
The Domestication Question
Mutual tolerance and respect, combined with the proto-dogs’ willingness to submit to human direction, could well have set up the dynamic relationship that has changed and flourished through many human cultures and adaptations. Certainly the similarities between the wolf’s pack structure and the extended families of early humans made it easy for proto-dogs to fit into human societies.
Proto-dogs may have remained unchanged in appearance for tens of thousands of years, perhaps until what we know as the domestic dog began to appear in the fossil record. We know that many European travelers described the dogs of the Inuit and many North American Indian tribes as indistinguishable from wolves. That might reflect not only a lack of selection for traits we identify with dogs but also the intermingling of dogs and wolves. In this view, the look of proto-dogs began to change in places where people started to establish more permanent settlements and change their ways of living at the end of the last Ice Age.
Dogs Extend Our Abilities
Dogs extend virtually all human senses. They detect odors at concentrations that are 1,000 to 100 million times lower than what humans can perceive, and they perform better than any machine. Today, dogs are used to detect explosives, guns, money, drugs, underground oil and water leaks, contraband agricultural products, termites, and almost as many objects as one can imagine. Dogs continue to find game and humans, including people trapped in rubble, and even to track endangered species.
Dogs see better at night, dusk and dawn than humans, and they can recognize moving objects at up to 540 meters (900 yards). Humans created gaze, or sight, hounds thousands of years ago to take advantage of the dog’s ability to see and run down large, fast prey, like gazelles and deer. Dogs hear over a much broader range of frequencies than humans, which enhances their value as watchdogs and as helpers for the hearing-impaired.
All canids exhibit both skeletal and physiological adaptations for running, and some species/breeds are better built for running than others. In the wild, canids run to catch prey and to avoid predators. For millennia, humans have taken advantage of the dog’s ability to run for hunting, hauling and sport racing.
Canids are also highly vocal, communicating through barks, bays, yodels, yelps, whines, growls and howls, with domestic dogs being the champion barkers. When it comes to howling, though, many of them come up short, and some dogs lack even a full range of barks. Humans do not always understand or appreciate these vocalizations in their house dogs, but these sounds are important in hunting and guard dogs, and dogs understand their meaning.
Looking at the work dogs perform and the companionship they provide, it is easy to romanticize their place in human society. Numerous myths and legends from many cultures attest to the importance of dogs and various wild canids—they are presented as creators of the world or of men, bringers of fire, healers, guardians or guides to the underworld, the inseparable companions of gods as well as men.
The Deadly Relationship
Dogs, too, have suffered persecution as spreaders of rabies and killers of livestock—in some areas dogs have long killed more livestock than wild predators, who are more frequently blamed. Millions of dogs are abandoned and abused each year or sacrificed in research. In some parts of the world, health officials continue to slaughter tens of thousands of stray dogs during rabies epidemics, despite the presence of a vaccine. Even without the fear of rabies, dog bites remain a major public health problem in the United States and other countries, serving as a constant reminder that for all of his virtues, the dog, like every canid, often acts with his teeth.
Dogs can also spread diseases like parvovirus and distemper to their wild cousins, a particular problem for endangered canids such as the Ethiopian wolf. Hybridization with domestic dogs is a problem for that imperiled wolf as well.
At the behest of their human companions dogs have served heroically in war; in fact, prior to the invention of firearms, they were a lethal part of any arsenal. But war dogs have also been turned to torture and brutality—against Native Americans during the Spanish conquest, for example, or runaway slaves or innocent civilians and protestors in many nations. Once popular sports, bull and bear baiting and dog fighting are now generally considered cruel spectacles, although they persist as illegal blood sports.
As scientific advisors of the exhibit by the Natural History Museum of Los Angeles County, we have attempted to present a full portrait of the rich history of human’s best friend and the rich, natural family of canids from which it came. We recognize that it is a story without end as scientists, veterinarians, historians, archaeologists and anthropologists continue to fill in the often significant missing details and as humans continue to shape dogs to new purposes through breeding and training. We have a responsibility to dogs and their wild cousins that we cannot ignore, for in ways nearly too numerous to count, they have helped us get where we are. They bring balance to our lives and to the natural world, and they provide an insight into the mechanisms of evolution itself.
Visit “Dogs: Wolf, Myth, Hero & Friend” online.
Culture: Science & History
A domestication that went both ways
That the dog is descended from the wolf—or more precisely, the wolf who stayed—is by now an accepted fact of evolution and history. But that fact is about all that is agreed to among the people who attempt to answer fundamental questions about the origins of the dog—specifically, the who, where, when, how and why of domestication.
Dates range from the dog’s earliest appearance in the archaeological record around 14,000 years ago to the earliest estimated time for its genetic sidestep from wolves around 135,000 years ago. Did the dog emerge in Central Europe, as the archaeological record suggests, or in East Asia, where the genetic evidence points? Were they tame wolves whose offspring over time became homebodies, or scavenging wolves whose love of human waste made them increasingly tame and submissive enough to insinuate themselves into human hearts? Or did humans learn to follow, herd and hunt big game from wolves and in so doing, enter into a complex dance of co-evolution?
Despite the adamancy of adherents to specific positions, the data are too incomplete, too subject to wildly different interpretations; some of the theories themselves too vague; and the physical evidence too sparse to say with certainty what happened. Nonetheless, some models—and not necessarily the most popular and current ones—more clearly fit what is known about dogs and wolves and humans than others. It is a field in high flux, due in no small measure to the full sequencing of the dog genome. But were I a bettor, I would wager that the winning view, the more-or-less historically correct one, shows that the dog is the result of the interaction of wolves and ancient humans rather than a self-invention by wolves or a “conquest” by humans.
Our views of the dog are integrally bound to the answers to these questions, and, for better or worse, those views help shape the way we approach our own and other dogs. It is difficult, for example, to treat as a valued companion a “social parasite” or, literally, a “shit-eater.” To argue that different breeds or types of dogs represent arrested stages of wolf development both physically and behaviorally is not only to confuse, biologically, description with prescription but also to overlook the dog’s unique behavioral adaptations to life with humans. Thus, according to some studies, the dog has developed barking, a little-used wolf talent, into a fairly sophisticated form of communication, but a person who finds barking the noise of a neotenic wolf is unlikely to hear what is being conveyed. “The dog is everywhere what society makes him,” Charles Dudley Warner wrote in Harper’s New Monthly Magazine in 1896. His words still hold true.
Since the dog is both a cultural and a biological creation, it is worth noting here that these opposing views of the dog’s origin echo the old theory that the sniveling, slinking pariah dogs and their like—“southern breeds”—derived from jackals, while “northern breeds”—Spitz-like dogs and Huskies—descended directly from the wolf. Darwin thought as much, so did the pioneering ethologist Konrad Lorenz until late in his life, when he accepted that the wolf was the sole progenitor of the dog. In the theories of Raymond Coppinger and others—and I think this transference is unconscious—the scavenging jackal becomes a camp-following, offal-eating, self-domesticating weenie of a tame wolf. In turn, those wolves become the ur-dog, still manifest in the pariahs of India and Asia, from which the dog we know is said to have emerged. It’s a tidy, convenient, unprovable story that has an element of truth—dogs are accomplished scavengers—but beyond that, it is the jackal theory with a tattered new coat. In dropping humans from the process, the scavenging, self-domesticating wolf theory ignores the archaeological record and other crucial facts that undercut it.
Fossils found at Zhoukoudian, China, have suggested to archaeologists such as Stanley Olsen, author of Origins of the Domestic Dog, that wolves and Homo erectus were at least working the same terrain as early as 500,000 years ago. The remains of wolves and Homo erectus dating to around 300,000 years ago have also been found in association with each other at Boxgrove in Kent, England, and from 150,000 years ago at Lauzerte in the south of France. It seems more likely that this omnivorous biped, with its tools and weapons, lived and hunted in proximity to that consummate social hunter, the wolf, through much of Eurasia, than that their bones simply fell into select caves together. Who scavenged from whom, we cannot say.
Wolves were far more numerous then than now, and they adapted to a wide range of habitats and prey. On the Eurasian steppes, wolves learned to follow herds of ungulates—in effect, to herd them. Meriwether Lewis observed the same behavior during his journey across North America in the opening years of the 19th century; he referred to wolves that watched over herds of bison on the Plains as the bisons’ “shepherds.” Of course, those “shepherds” liked it when human hunters attacked a herd because they killed many more animals than the wolves, and although the humans carried off the prime cuts, they left plenty behind.
Ethologists Wolfgang M. Schleidt and Michael D. Shalter refer to wolves as the first pastoralists in “Co-evolution of Humans and Canids,” their 2003 paper in the journal Cognition and Evolution. Early humans, they argue, learned to hunt and herd big game from those wolves; thus, the dog emerged from mutual cooperation between wolves and early humans, possibly including Neanderthal. There is no evidence yet of Neanderthal having tame wolves, much less dogs, but the larger point is that when modern humans arrived on the scene, they found wolves already tending their herds, and they immediately began to learn from them. That was long before humans began, in some parts of the world, to settle into more permanent villages, some 12,000 to 20,000 or 25,000 years ago.
Schleidt and Shalter based their model on wolf behavior and on genetic studies that have consistently shown that dogs and wolves diverged between 40,000 and 135,000 years ago. The first of those studies emerged from the lab of Robert K. Wayne, an evolutionary biologist at the University of California at Los Angeles who had already made headlines by showing definitively that the dog descended from the wolf alone. In a paper appearing in the June 13, 1997, issue of Science, Wayne and his collaborators said that dogs could have originated around 135,000 years ago in as many as four different places. They also argued that genetic exchanges between wolves and dogs continued—as they do to this day, albeit in an age during which dogs have become ubiquitous and wolves imperiled.
Since that paper appeared, the dog genome has been fully sequenced and provides a time frame for domestication of 9,000 generations, which the authors of a paper on the sequencing in the December 8, 2005, issue of Nature pegged at 27,000 years. But except for that, subsequent studies of mitochondrial DNA, which is most commonly used to date species divergence, have pointed to a time frame of 40,000 to 135,000, with 40,000 to 50,000 years ago looking like the consensus date.
Most of this work has been conducted in Wayne’s lab; in the Uppsala University lab of Carles Vilà, his former student and the lead researcher on the 1997 paper; and in the lab of Peter Savolainen of the Royal Institute of Technology, Stockholm, another collaborator on the original paper.
A signal problem with the early date is that it doesn’t appear to match the archaeological record. The dog is not only behaviorally but also morphologically different from the wolf, and such an animal first appears in the fossil record around 14,000 years ago in Bonn-Oberkassel, Germany. Archaeologists nearly universally peg the origin of the dog to that time.
Wayne, Vilà and their supporters have suggested from the start that behavioral change could predate morphological change, which would have occurred when humans began to create permanent settlements, thereby cutting—or at least reducing—their wolf-dogs’ contact with wild wolves. People might also have begun attempting to influence the appearance of their dogs at this point.
But those Germans get in the way again. Bonn-Oberkassel, site of the consensus first fossil dog, is not a permanent settlement.
Trying to square genetic and archaeological dates, Peter Savolainen resurveyed the mitochondrial DNA of dogs and wolves, recalibrated the molecular clock and proposed in a paper in Science, November 22, 2002, that the dog originated in East Asia 15,000 to 40,000 years ago. It was a good try, but now it appears that his “40,000 years ago” date was more accurate. Also, the earliest known dog appears in Germany, not East Asia, a region to which other genetic evidence points as well.
In many ways, the dispute over dates and places is just a precursor for the debate over how that happened. Archaeologists and evolutionary biologists who want the first dogs to look like dogs have tended to argue that the transition is a result of a biological phenomenon called “paedomorphosis.” That basically means that the animal’s physical development is delayed relative to its sexual maturation. It produces dogs with more domed heads; shorter, broader muzzles; and overall reduced size and slighter build than a wolf. Accelerated physical development relative to sexual maturation (hypermorphosis), on the other hand, produces dogs larger than the progenitor wolf.
When maturation is stopped early enough, the resulting animal is said to resemble a “neotenic,” or perpetually juvenilized, wolf. Coppinger and others have carried the argument further to argue that behaviorally, the dog resembles a neotenic wolf, with some breeds being more immature or less developed than others. There is general agreement that, beginning in the late 19th century when the dog began to move into the city as a pet, breeders sought to soften and humanize the appearance of some breeds to make them look like perpetual puppies. But beyond that, it is more correct to view the dog as an entity different from the wolf.
Currently, many researchers like to invoke an experiment in domestication launched in 1959 at the Institute of Cytology and Genetics in Novosibirsk, Siberia, by Dmitry Belyaev and continued after his death by Lyudmila Trut and her colleagues. Belyaev selectively bred foxes for “tameness” alone, defined as their level of friendliness toward people. He ended up with foxes that resembled dogs. A number of them had floppy ears, piebald coats, curly tails and a habit of submissively seeking attention from their human handlers with whines, whimpers and licks. (I wouldn’t want such a dog.)
Anthropologist Brian Hare tested the tame foxes in 2004 and found that they, like dogs, had the capacity to follow a human’s gaze, something wolves and wild foxes, not to mention chimpanzees, won’t do.
A number of researchers have embraced these tame foxes as a template for dog domestication. While they doubtless cast insight on the problem, I doubt that they will answer all questions. Arguments by analogy are suspect science and should be even more so in this case, since the selection criteria for these foxes were also against aggression—hardly the case for dogs—and foxes clearly are not wolves.
That said, the experiment does appear to confirm that selective breeding for behavior alone can also produce morphological changes similar to what the wolf experienced in becoming a dog.
Coppinger has invoked the fox experiment to support his theory that wolves that became dogs self-domesticated. As humans in some areas moved into permanent settlements, their refuse heaps became feeding grounds for wolves who were tame enough—or least-frightened enough—to feed near humans. Subsequent generations became more tame, and people began to allow them to wander their camps, eating feces, hunting rodents. From that group, people took some animals for food. Then, when the animals were thoroughly self-tamed, people began to train them to more wolfish behaviors, like hunting.
What he and others overlook in citing the fox experiment is that those animals were subjected to intense artificial selection by people. They also ignore the fact that the first dog appears in a seasonal camp, not a permanent settlement.
In their book, Dogs, Coppinger and his wife, Lorna, argue that these early protodogs would have resembled the ownerless dogs of Pemba Island, a remote part of the Zanzibar archipelago. As a model, Pemba suffers numerous problems, as does Coppinger’s theory. It is an Islamic island, and Islam has scarce place for dogs, believing them filthy, largely because they scavenge and eat excrement.
Beyond that, Pemba was a wealthy island in the 18th and 19th centuries due to its clove plantations, which were worked by African slaves and overseen by Arabs. The plantations have long since fallen into disrepair, on an island populated by the descendants of free slaves, where poverty is the rule. Attempting to read the past by looking at the present is a well recognized form of historical fallacy. It can’t be done, especially in a place where there is no strong cultural tradition.
Elsewhere in the developing world, free-ranging dogs are often more than scavengers or food. Some are fed; they protect territories or vendors’ carts. A few might be taken in, but, again, these dogs must be studied and understood in their current context and then placed in a broader historical context, if possible.
Moreover, Coppinger ignores the entire tradition of dogs and people in Europe, Japan and Korea—wherever dogs were employed from an apparently early date for a purpose, including companionship and ritual. Archaeologist Darcy F. Morey clearly demonstrated in the February 2006 issue of The Journal of Archaeological Science that people have been burying dogs and treating them with reverence and respect from the beginning, hardly the fate of scavengers.
People will argue, but I think the question of whether the dog is a juvenilized wolf is best answered with this observation: The dog follows human gaze, according to Hare, and is so attentive to people that it can imitate them, according to Vilmos Csányi, and it does so from an early age. No wolf of any age can replicate that basic behavior. It is far better to look at the dog as a differently developed wolf than as a developmentally retarded wolf.
Similarly, until shown otherwise, it seems more accurate to view domestication as a dynamic process involving wolves and people. At a time when the boundaries between human and wild were much more porous than now, people doubtless took in animals, especially young animals of all kinds, especially wolf pups, since in many places, they were hunting the same game and perhaps scavenging from each other.
As those pups matured, they returned to the wild to breed, with the naturally tamest among them denning close to the camp where they had been raised and, yes, could scavenge. Over the past year, researchers have shown that the area of the brain known as the amygdala is quite active when “fear of the other” begins to develop. In 2004, a team of researchers from Uppsala University, including Vilà, reported in the journal Molecular Brain Research on changes they had found in gene expression in the frontal lobe, hypothalamus and amygdala of wolves, coyotes and dogs. More than 40 years ago, J.P. Scott and John L. Fuller showed that the dog pup had a lengthened socialization period before fear of the other set in, compared with the wolf pup.
No one knows how fast the change happened, but in some places, tame wolves—dogs—resulted from this process. They provided territorial defense, helped with hunting (which they do well), scavenged, and were valued for companionship and utility. Some could be trained to carry packs. That early dog probably remained nearly indistinguishable from the wolf except in places where their gene pool became limited by virtue of some isolating event. The smaller gene pool forced inbreeding that, along with changing environmental conditions, somehow “destabilized” the genome.
Vilà and two colleagues suggested in an article published online on June 29, 2006, in Genome Research, that domestication relaxed “selective constraint” on the dog’s mitochondrial genome, and if that relaxation extended to the whole genome, as it appeared to, “it could have facilitated the generation of novel functional genetic diversity.”
European and North American breeders have taken full advantage of that or some other mechanism to create the most morphologically diverse mammal around. But other cultures did not follow that path.
There are other theories afloat in what is an exciting time for people who study dogs. But the one that succeeds will reflect the dynamic relationship between human and dog.
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