Good Dog: Behavior & Training
Similar brain abnormalities in both species
A new study has found that Doberman pinschers with canine compulsive disorder (CCD) have abnormalities in brain structure that are much like the ones in humans who have obsessive compulsive disorder (OCD). The study, conducted by eleven researchers, is called “Brain structural abnormalities in Doberman pinschers with canine compulsive disorder” and was published in the journal Progress in Neuro-Psychopharmacology and Biological Psychiatry.
The research suggests that more research about anxiety disorders in dogs may be a promising avenue for developing new ways to treat them in people. It also stands to reason that more research about anxiety in people may prove fruitful in finding new ways to alleviate suffering for dogs with similar problems.
Canines with CCD and humans with OCD typically perform repetitive behaviors. In humans, excessive hand-washing and endless checking that appliances are off or that doors are locked are common. In dogs, common behaviors are flank-sucking, blanket-sucking, licking and tail chasing. In both species, anxiety disorders can interfere with quality of life and daily routines, and can also cause injury as skin is chafed and rubbed raw by licking, washing, or sucking.
It’s no big surprise that the brains of affected individuals have similarities. After all, it has been known for a long time that members of both species exhibit related symptoms and respond to the same medications, and that there’s a genetic basis for these disorders in dogs as well as in humans. Still, the discovery that brain abnormalities are also alike adds to our understanding of the parallel nature of anxiety disorders in us and in our best friends.
News: Guest Posts
June 28 to 30—streaming live
SPARCS is a unique venture organized by Prescott Breeden and Patti Howard of The Pawsitive Packleader, Seattle Dog Training. From June 28-30, 2013, anyone in the world can see some of the leading canine science researchers in action—either in a conference hall in Redmond, WA, or streaming live to your living room.
SPARCS is short for the Society for the Promotion of Applied Research in Canine Science, which aptly summarizes the goals of the conference: (1) to promote research and education in canine science, and (2) to provide a platform for leading minds in canine science to present, discuss and debate modern behavior science.
Canine Science? Explain
If the phrase “Canine Science” gives you pause, I assure you it does not imply that dogs are meeting in the park to discuss the current issues of the day, such as:
- Owner Responses to Half Eaten Sandwiches: A Review
- Why Does the Cat Run Around at Night?: A Roundtable Discussion
- Where Are They Taking Our Poo?
Canine Science, generally speaking, is research devoted to the biology, ecology, behavior and cognition of dogs, wolves and related canids. It is a catch-all phrase that highlights the surge of research into canine minds and experiences. My article in The Bark, Dog Smart: Exploring the Canine Mind, describes this field in more detail. SPARCS brings together the following leading researchers to discuss their inquiry into the dog for a general audience:
Marc Bekoff is a long-time researcher and writer of more than 500 scientific and popular essays. In a book store? Check out one of his twenty-two books, including Minding Animals and the children’s book Animals at Play: Rules of the Game. He regularly updates a Psychology Today Blog, Animal Emotions: Do animals think and feel?
- Bekoff on dogs and their urine: Observations of scent-marking and discriminating self from others by a domestic dog (Canis familiaris): tales of displaced yellow snow.
- Bekoff on play: Social play and play-soliciting by infant canids.
Ray Coppinger has published over fifty papers on dog research. His favorite publication, however, is the book Fishing Dogs, a humorous and iconoclastic look at dogs, fishermen and professors. His book, Dogs: A Startling New Understanding of Canine Origin, Behavior & Evolution, is a classic text in the field.
- Coppinger on different behavioral sequences between dogs: Degree of behavioral neoteny differentiates canid polymorphs.
- Coppinger on improving assistance dog training programs: Observations on assistance dog training and use.
Michael W. Fox wears many hats. He is a veterinarian with a Ph.D. in medicine, and he also holds a degree in animal behavior (ethology). His career encompasses extensive research into dog behavior and development as well as holistic and integrative veterinary medicine. He encourages veterinary institutions to incorporate animal behavior and welfare science into their curricula.
- I covered Fox’s 1963 paper, Developmental Abnormalities of the Canine Skull in the Dog Spies post, Where Should Dogs Put Their Tongues?
- Fox on dog development during the first month of life: The postnatal development of neocortical neurons in the dog.
Alexandra Horowitz’s current research at the Dog Cognition Lab at Barnard College investigates animal communication and attention, dog olfaction, inter-species play behavior, theory of mind and anthropomorphisms.* She writes regularly for The New York Times, and her best-selling book, Inside of a Dog: What Dogs See, Smell, and Know, is essential.
- Horowitz on attention during dog-dog play: Attention to attention in domestic dog (Canis familiaris) dyadic play.
- Horowitz on the “guilty look” in dogs: Disambiguating the “guilty look”: Salient prompts to a familiar dog behaviour.
Kathryn Lord received her PhD in organismic and evolutionary biology, which of course means she studies wolf pups. Her research focuses on the evolution and development of dog and wolf behavior.
- Lord on sensory development of wolves and dogs: A Comparison of the Sensory Development of Wolves (Canis lupus lupus) and Dogs (Canis lupus familiaris).
- Lord on the meaning of dog barks: Barking and mobbing.
Adam Miklósi leads the Family Dog Project at the Department of Ethology at Eötvös
Loránd University in Budapest, where I had the pleasure of conducting my Masters research (covered on SciAm by Jason Goldman of The Thoughtful Animal). In the last 15 years, the Family Dog Project research group has published over 100 scientific papers and organized the inaugural Canine Science Forum in 2008. His book, Dog Behavior, Evolution and Cognition is required reading in canine ethology.
- Miklósi on the building blocks of meaningful social interactions: On the utilization of social animals as a model for social robotics.
- Miklósi on other species’ use of human communicative gestures: A comparative analysis of animals’ understanding of the human pointing gesture.
Monique Udell has worked with a variety of species such as wild cats, megachiropteran bats, coyotes, foxes, mice, non-human primates and a range of companion animals including dogs, cats, and ferrets. She has a special interest in how the cognition and behavior of domestic dogs and wolves can be altered by lifetime experience.
- Udell on dog sensitivity to human behaviors: What did domestication do to dogs? A new account of dogs’ sensitivity to human actions.
Before Clive Wynne found a way to combine a childhood fascination with dogs with his day job as a psychology professor, he studied the behavior of animals ranging from pigeons to dunnarts (a mouse-sized marsupial) at universities in Britain, Germany, the USA, and Australia. Now head of the Canine Cognition and Behavior Laboratory, he is full of tales of everything from the tame foxes of Siberia to the dogs of the Moscow subway.
- Wynne on anthropomorphism: What are animals? Why anthropomorphism is still not a scientific approach to behavior.
- Wynne on the relationship between companion dogs and children: The other side of the bond: Domestic dogs’ human-like behaviors.
So, What’s This Conference About?
The SPARCS conference investigates dogs from three angles: “Origins in the Wild,” “Social Behavior and Emotions” and finally “Cognition and Development.”
Origins in the wild
“It is widely accepted that dogs are descended from wolves, but that is about the only uncontroversial fact about the origins of dogs…. I have come to a new proposal for the origin of dogs.” Clive Wynne
“In my presentation I shall talk about the emotional lives of nonhuman animals (animals) – beastly passions – and how they very much care about how we treat them.” Marc Bekoff
“The modern wolf and the modern dog diverged into their present forms, sometime, somewhere, and somehow. We should discuss those when, where, and how questions.” Ray Coppinger
Social Behavior and Emotions
“I shall also talk about why play has evolved – what it is “good for” and why it is very important that we come to terms with the details of what animals do when they play.” Marc Bekoff
“So the basic question is: What makes a dog skillful for living in the anthropogenic [human] environment, and whether we can claim that there is a parallel between some of the behavioral skills of dogs and those of humans?” Ádám Miklósi
“Dogs are socially and emotionally promiscuous and, given the right conditions, can form attachments to members of many other species.” Clive Wynne
Cognition and Development
“How the dog’s brain and behavior develop is integral to our understanding of critical and sensitive periods in helping facilitate a strong social bond and in enhance learning/trainability, emotional stability and stress & disease resistance.” Michael W. Fox
“[W]e must be careful not to forget the true diversity of the domestic dog population, or assume that the sum is more representative than its parts. Indeed, it is at the fringes of the species where we often discover examples of amazing cognitive feats, or hidden canine capacities unveiled by unique environmental or experiential contexts.” Monique Udell
“First, I aim to highlight and examine the attributions we unthinkingly make to dogs. Second, I use findings about the biology and cognition of dogs to create a better picture of the dog’s experience: the umwelt, or point of view.” Alexandra Horowitz
What About My Living Room?
Because SPARCS aims to make continuing education accessible, the conference will be broadcast live and free of charge: “As long as you have a computer, a tablet, or a smartphone, everyone will be able to watch our broadcast from anywhere in the world.”**
SPARCS plans to be a yearly conference, so keep it on your radar!
Ticket, Live Stream and Schedule
on Social Media
SPARCS on Facebook
SPARCS on Twitter
All photos courtesy of SPARCS
** SPARCS adds, “Donations are absolutely optional however graciously appreciated. If you watched our event online and enjoyed it, consider donating to SPARCS.”
Dog Smart: Exploring the Canine Mind at The Bark
Talking dogs: Welcome to the 3rd Canine Science Forum at Dog Spies
Inside the 3rd Canine Science Forum at Dog Spies
This story was originally published by Scientific American. Reprinted with permission.
About the Author: Julie Hecht is a canine behavioral researcher and science writer in New York City. She wriites a behavior column for The Bark. She would really like to meet your dog. Follow on Twitter @DogSpies.
Culture: Science & History
Village dogs’ genetic code may hold clues to canine evolution and health
Like classic twin studies that investigate the interplay of nature and nurture, comparing the genome of village dogs to modern dogs may help disentangle the long-term evolutionary effects of genetic and environmental influences.
Mastiff to Min-Pin, Corgi to street cur: all dogs share the same set of roughly 20,000 genes. What makes one dog different from another—or, in the case of purebreds, almost the same— is how the genes are expressed and restricted from being expressed, and how they communicate with one another. Therefore, it may be safe to say that each of the world’s 800 to 900 million dogs is a distinct combination of different versions of the same genes. Or maybe not. At least, that’s what some scientists suspect, and they think they’ll find answers in the DNA of the ubiquitous, free-ranging canine outcasts that populate developing countries throughout the world.
While village dogs were being socially shunned, modern dogs—a subpopulation that likely split off from village dogs thousands of years ago—were serving society. So tightly woven into the fabric of our lives that we rarely think of them as human-engineered, dogs have been refined for increasingly specialized tasks such as hunting, transportation, protection, warfare, ornament and companionship. As a result of rigorous artificial selection over a long period of time, many of their ancestral gene variants are suppressed. Some have disappeared altogether, creating a fragile homozygous genome that has little diversity.
In contrast, village dogs are barely tolerated by society. Although considered a domestic species, they are the products of thousands of years of natural selection. Consequently, their heterozygous genomes are robust and extremely diverse. In addition, it’s possible that long after modern dogs branched off from the family tree, some village dog populations may have developed new gene variants that protect their immune systems.
Evolutionary biologist Adam Boyko, assistant professor in the Department of Biomedical Sciences at the Cornell University College of Veterinary Medicine, is confident that comparing and contrasting the two branches of the domestic canine family tree will provide answers to some of the mysteries that continue to surround the evolution of the domestic dog: When and where were dogs domesticated? What were the global migration paths of humans and dogs? What genetic changes occurred when wolves became dogs? Which genes are responsible for extreme size, shape and behavior differences? What are the underlying causes of genetic diseases? And how do parasites have an impact on canine well-being?
As a postdoctoral student at Cornell, Boyko worked under the tutelage of Carlos Bustamante, now professor of genetics at the Stanford School of Medicine. Curious about how the underappreciated and even less-studied village dog genome might reframe our current understanding of canine evolution and domestication, Boyko and Bustamante persuaded Ryan and Cori Boyko (Boyko’s brother and sister-in-law, who were then both graduate students in anthropology at the University of California, Davis) to add a few side trips to their otherwise romantic African honeymoon. Their instructions were to catch semi-feral, uncooperative village dogs and draw blood samples, then ship the samples back to the lab for analysis. Information from the preliminary DNA samples indicate that the researchers are on the right track. I asked Dr. Boyko about his research, and if it has future application to invigorating the health of our companion dogs.
Jane Brackman: How will mapping the genome of the village dog help us understand the mechanisms of traits in modern dog breeds?
Adam Boyko: Geneticists have spent a lot of time looking at purebred dogs. When something is selected for, either by natural or artificial selection in a population, geneticists can tell because of the patterns that are left in the genomes of individuals in those populations. In humans, for example, we can clearly see that lactase persistence, the ability to digest milk into adulthood, was selected for in some populations.
When we look for these patterns in purebred dogs, we find that things like ear f loppiness and tail curliness are driving these patterns, or short legs or small/big size. Basically, we find the effects of artificial selection by humans for breed standards. If we did a similar scan for selection in village dogs, perhaps some of those same genes would show patterns of selection, but I think we’d also see a new class of genes showing patterns due to natural selection.
For example, maybe there was a lot of selection in early dogs for genes in certain metabolic pathways because there was such an extreme dietary shift from wolves to dogs. Or maybe new parasites and pathogens caused selection at genes influencing the immune system. Or maybe we’ll see selection around genes that influence behavior and temperament.
Basically, there are all sorts of theories about how dogs became domesticated and what makes a dog a dog. When we look at purebred dogs, the main thing we are able to see is what makes certain dog breeds look and behave one way versus another. Maybe by looking at village dogs, which are much less influenced by the strong and recent artificial selection taking place in breed dogs, we’ll be able to see patterns of selection that occurred earlier in dog history.
JB: Might your findings have application for the future? For example, if you were to come across genes influencing the immune system, would breeders be able to use that information to revitalize the pedigreed-dog immune system?
AB: It is certainly true that my research may find a new MHC-type immunity gene [the major histocompatibility complex mediates the immune system’s white blood cells] that has been lost in many purebred dogs and which could reinvigorate their immune diversity. Or perhaps it will find variants associated with diet, and make us start considering a dog’s genetic makeup when making dietary recommendations. But I’m really not comfortable speculating, since I’m likely to be quite wrong in these predictions.
For example, I would have never guessed that deliberately infecting patients with intestinal parasites [Helminthic therapy] would cure ulcerative colitis, but that seems to be the case, and signatures of selection in the human genome help explain why.
But having said that, I think looking at the genomes of village dogs will be extremely useful. For example, we could get a better picture of the kinds of traits that were selected for in natural dog populations, including disease resistance, which might give us useful insights into diseases we diagnose in our pet dogs.
Conversely, as veterinarians and geneticists find more mutations that cause disease or unique traits in dogs, we can look at the genomes of diverse village dogs to see when and where these mutations arose, and whether they are also found in any other village or purebred dog populations.
It’s a really exciting time to be a canine geneticist, as we have all these new genetic tools at our disposal and many, many purebred and free-ranging populations that have yet to be characterized genetically.
JB: Some populations of village dogs, such as those you’re studying, have been isolated for many thousands of years, evolving under pressures that the stem parents of modern breeds were never exposed to. Is it possible that these dogs have “new” gene variants that don’t exist in the genome of modern breeds?
AB: It’s certainly possible, and it’s something I’m very interested in. For example, my lab is looking at free-ranging dogs in the highlands of Peru to see if they have any genetic adaptations for high altitude. Perhaps more importantly, some village-dog populations might harbor disease-resistant variants for parasites or pathogens that are prevalent in their area, but these variants might not have made it into modern purebred dogs, since those breeds were mostly founded elsewhere.
JB: How urgent is it that we learn more about these ancient dog genomes?
AB: We know how quickly pre-Columbian Native American breeds were lost when Europeans brought dogs with them to the New World, and we see that it will happen like that very soon in other remote parts of the world. So we’re working as fast as we can to get the data before the dogs are gone.
JB: What’s going on in your lab now?
AB: We’re collecting DNA samples and the genetic information we need so we can start piecing together what’s going on in these interesting but largely neglected free-ranging dog populations. We are seeking insights into dog population history to discover patterns of selection around certain genes that can then become the basis of further study. Our work is very hypothesis-driven. We have certain hypotheses about how dogs evolved, and we try to collect the right samples to test these hypotheses.
As geneticists learn more about how genetic variation controls complex traits in purebred dogs, we find it’s quite different than what we see in humans. Why? There are at least two competing hypotheses, and by gathering data from free-ranging dogs, we can start testing them to figure it out. Some of this gets into technical discussion about genetic architecture, recombination, epistasis and pleiotropy and such, so I’ve avoided getting too academic. But I also don’t want to be dismissive of it since those technical, hypothesis-driven aspects of the project are the bread and butter of my lab in terms of student training.
JB: In longitudinal studies such as the Morris Animal Foundation’s Golden Retriever Lifetime Study, researchers gather information from participants’ DNA and then match what they find to traits the test dogs may display over a lifetime. Will you have an opportunity to see how, for example, an immunesystem mutation affects a village dog’s health as it ages?
AB: Our project is a huge undertaking, and there’s a ton of data we’d love to gather on each dog but just simply aren’t able to since, at this point, we’re focused on sampling as many dogs from as many populations as possible to maximize the amount of diversity we can analyze. I really don’t want to overstate what we’re able to do in one visit to check out a dog and draw blood, which is limited to looking for genetic signatures in the genome of these dogs showing signs of selection and/or local adaptation.
But, since we have a fairly good idea of what genes do in modern dogs, at least in a rough sense, if we see a genetic signature in village dogs for positive selection around a gene we know is involved in immune function (for example), that’s a big discovery.
JB: At the risk of oversimplifying, say you’re looking at a region that you know to be linked to a negative trait and you see that the switch is turned off in the village dog DNA and turned on in modern dog DNA—would you feel that you’d found a “smoking gun”?
AB: It’s possible. Then, of course, as you allude, we would want to go back, look at dogs carrying that mutation versus other dogs, and see if there are different health outcomes. Perhaps [dogs with the mutation] are more resistant to intestinal parasites or perhaps they are more prone to autoimmune disease or something. Until we find the mutations, it’s a bit speculative to make predications about what exactly the findings will mean to owners. This is certainly “basic research” in the purest sense.
JB: In people, size is determined by hundreds of genes, each with a small effect. In purebred dogs, body size can be regulated by a single gene. Is this unique to dogs?
AB: It depends. There are other traits in other species controlled by a couple of loci [location of a gene on a chromosome]. I would argue that yes, it’s pretty unique. Whether or not dogs are special in that there is something about their genome that predisposes them to this type of diversity, or perhaps because humans worked so hard at creating them, we don’t know. This debate is still raging in the literature. It is definitely the case that genes have many, many effects. Rather than being a blueprint in which each gene is responsible for just one part of building the whole organism, the genome is more complicated, with each gene taking on different roles at different times or in different tissues.
JB: Do multiple-trait relationships also show up in village dogs?
AB: I think this would also occur in village dogs if the mutations were in those populations. The difference is that selective breeding has actively promoted these large-effect, diversifying mutations in dog breeds, making them relatively more common. Natural selection usually selects against such large-effect mutations in natural populations. You won’t see a short-legged wolf because it couldn’t hunt.
In fact, most of these large-effect mutations probably first arose in village dogs. The difference is that these mutations aren’t usually beneficial to village dogs, but the ones that aren’t too detrimental might persist at low frequency long enough for humans to start trying to promote breeding of that trait. Take achondrodysplasia [a type of dwarfism]. It almost certainly arose in village dogs, but to a free-ranging dog, super-short legs and all that comes with them probably aren’t much of a selective advantage. But once folks started looking for dogs to turn their spits, they found these super-short dogs to be useful, and eventually that genetic variant made its way into a whole host of modern breeds.
For the specific achondrodysplasia mutation, I don’t know if that is the exact story, but I do think this is likely to be the case for many large-effect mutations. Depending on how early in dog evolutionary history the mutation arose, it could be found in most regional village dog populations, or it could be restricted to certain populations that are close to where it first arose. Lots of research still left to be done!
JB: As a lifelong dog lover, you must find it difficult to see the deplorable conditions in which some of these dogs live.
AB: There’s so much disease in these high-density populations. As these communities become more urbanized, dogs are living like rats and pigeons. Getting DNA on these populations is not enough of a reason to allow the animals to exist like this. Life on an urban street is rough existence.
JB: If you adopt a village-dog puppy and raise it in a typical Western environment, what kind of dog will you have?
AB: Adopting the dogs is not part of our project, but we know people who have done this. They can be great dogs. They don’t have some of the aggression issues you might see in some of our dogs, because they are culled for aggression, or for eating a chicken. There are some things that aren’t tolerated. So you might say that people in the villages impose a form of selection. The dogs are smart and resourceful. They seem to adapt.
Good Dog: Behavior & Training
Benefits of lower protein and higher fat
It’s not news to anyone that the food that we feed our dogs matters. The right food may translate to better health, proper weight management, longer life, a shinier coat, and better performance in a range of sports and activities. New research suggests that the diet of working detection dogs can even have an impact on their ability to smell.
Joseph Wakshlag at Cornell and his colleagues at Auburn University found that dogs who were fed more fat and less protein than typical diets contain were better able to detect certain scents such as TNT, ammonia nitrate and smokeless powder. Over a year-and-a-half, they rotated dogs through three diets and compared their detection abilities when they were on each diet. The three diets were: 1) a high quality performance diet, 2) regular adult dog food and 3) regular adult dog food combined with corn oil. The ability to detect scents was highest when the dogs ate the diet of regular dog food combined with corn oil. That diet had less protein but the same amount of fat as the high performance diet. The high performance and regular diets had equal amounts of protein, but the high performance diet had more fat.
Digesting protein causes a rise in a dog’s body temperature, as does exertion in the form of physical activity. The panting that is essential for lowering body temperature reduces a dog’s ability to smell well. In order to do their detection work as effectively as possible, dogs must cool down so that they are not panting. A diet higher in fat and lower in protein seems to allow dogs to cool down faster and therefore smell better.
What constitutes a high performance diet may depend on the sort of performance that is desired. Dogs who work by running or pulling hard may need more protein to succeed at their job than dogs who need to be able to maximize the effectiveness of their olfactory abilities.
Good Dog: Behavior & Training
Its association with lifespan and cause of death
In a new study called Reproductive Capability is Associated with Lifespan and Cause of Death in Companion Dogs, researchers report on the links of reproductive status (intact or spayed/neutered) with both lifespan and cause of death. Previous studies have suggested that sterilization increases the risk of certain cancers. However, if spaying and neutering actually does increase life span, then any cancers that are more common in older dogs may only appear to be more common in sterilized dogs because sterilized dogs live longer.
The overall conclusions of this new study are that there is a link between lifespan, cause of death and reproductive status. Sterilization was associated with longer lifespan. The mean age of death for intact dogs was 7.9 years and for sterilized dogs was 9.4 years. Sterilization increased life expectancy 13.8% in male and 26.3% in females.
In this study, researchers found differences in the cause of death between the reproductively capable group and the sterilized group. Compared to reproductively capable ones, dogs who were spayed and neutered were more likely to die of cancer and immune-related diseases, but less likely to die from infectious diseases, trauma, vascular disease and degenerative diseases. These differences in causes of death were consistent when the data were compared between dogs of the same age.
Data are from 40,139 dogs in a veterinary teaching hospital who died from 1984 to 2004. Juvenile dogs, dogs with a congenital issue that caused death, and dogs whose reproductive status, cause of death, or age were unknown were eliminated from the over 80,000 dogs originally considered for inclusion in the study. Reproductive capability was defined in this study as intact versus spayed or neutered, and does not mean the sterilized dogs had not reproduced. It’s unknown if they had reproduced prior to being sterilized. There were no data on how many times intact dogs had reproduced, only that they were still reproductively capable.
Though the results of this study are intriguing, it is important to recognize the limitations in the data and therefore in the conclusions. Though the groups—intact or sterile—are assumed to differ in no other way, that may not be the case. It is possible that the members in the sterilized group have received more regular or better medical care throughout their lives, for example. The sterilized dogs may come from different sources such as rescue groups or shelters rather than from pet stores or breeders. In other words, differences in life span or cause of death may not relate to reproductive status, but to one of these other factors. This study shows links of reproductive status with lifespan and cause of death, but we cannot assume that reproductive status is the cause of these differences. They may be correlated for some unknown reason.
Some other concerns I have about the data are that the dogs had all been referred to a veterinary teaching hospital for medical reasons, which means that the dogs in the study may be largely dogs with serious health issues rather than typical dogs. This means that conclusions based on this study may not be applicable to dogs in general.
I’m glad that studies are expanding on the question of lifespan and reproduction by looking at causes of death instead of just reproductive capability. I think this study is a great start at exploring questions that are of interest to all of us who love dogs, but I do think we need to exercise caution in order to make sure that we are distinguishing between studies that show correlations between various factors and those that demonstrate a causal relationship between those factors.
Culture: Science & History
"Though in their deep heart’s core, there is a commonality of origin, spirit, emotional intelligence and empathetic sensibility, the wild wolf looks through us, while the dog looks to us. "
Of all the myriad members of the animal kingdom, the domesticated dog (Canis lupus familiaris) is closest to us. With individual exceptions in other species, this canine species is the most understanding, if not also the most observant, of human behavior—of our actions and intentions. This is why dogs are so responsive to us, even mirroring or mimicking our behavior. And it is why dogs are so trainable.
Fear in unsocialized and abused dogs interferes with their attentiveness to and interpretation of human behavior and intentions. This is one reason wild species like the coyote and wolf, even when born and raised in captivity, are difficult to train. The wolf “Tiny,” whom I bottle-raised and intensely socialized during her formative early days, never really lost her fear and distrust of strangers.
Tiny did not start mirroring human behavior until she was close to nine years old. At this point, she began to mimic the human-to-human greeting grin, revealing her front teeth as she curled her lips into a snarly smile. In my experience, dogs who can do this do so at a much earlier age, even as early as four to six months.
In comparing socialized (human-bonded) wolves and dogs in terms of how they have related to me as well as to my family members, friends and strangers, I would say that the main difference between the two species is the fear factor. Differences in trainability hinge on this; as I theorize in my new book (Dog Body, Dog Mind), domestication has altered the tuning of the dog’s adrenal and autonomic nervous systems. This tuning (which dampens adrenal fright, flight and fight reactions and possibly alters brain serotonin levels), is accomplished through selective breeding for docility, and by gentle handling during the critical period for socialization.
According to the earlier research of my mentors—Drs. John Paul Scott and John L. Fuller of the Jackson Laboratory in Bar Harbor, Maine—pups with no human contact during this critical socialization period (which ends around 12 to 16 weeks of age) are wild and unapproachable.
When we peel off the wolf’s innate fearfulness and put it on the dog, we turn the dog into a feral facsimile of a wolf. But a human-socialized wolf without fear could be an extremely dangerous animal, even attacking a human perceived as a pack rival. This happened to me in the 1970s during the filming of the NBC documentary, “The Wolf Men.” An alpha male wolf, along with his female cagemate who was in heat, had been released into a large wooded compound belonging to my friend, the late wildlife illustrator and conservationist Dick Grossenheider. Earlier that memorable morning, the she-wolf had greeted and solicited me, a total stranger, when I had visited the two wolves in their enclosure. (I am not saying that a male dog would never react to me in a similar way under comparable circumstances; I was once urinated on by the alpha male lead sled dog of a well-known racing pack in a similar situation.)
Canine Evolution and Human Needs
We see many things in our dogs’ eyes, the windows of their souls. They are also mirrors of the human soul, since every pair of dog’s eyes reflects—for better and for worse—how well that dog has been treated by our own kind. Dogs read our eyes and are attentive ethologists of human behavior, action, emotion and intuition. A change in tone of voice can make a dog tremble in fear or dance and yap for joy. Such ability to read human behavior, intentions and emotions was naturally selected for as dogs domesticated themselves and adapted to life with Homo sapiens, the “killer ape.”
Civilizing the Killer Ape
These half-human killer apes were never to be fully trusted, however, since when they were very hungry, or warring between themselves, they would often engage in cannibalism, as today, people still kill and eat dogs for sustenance and “good medicine.” (See James George Frazer’s The Golden Bough.).
Just as not every dog is fully domesticated, in that some can still turn feral, and others turn on their masters, so the wolf has failed to fully domesticate and civilize the killer ape. We still wage war with our own kind, and ignore the biological wisdom and prescience of such injunctions as do no harm, resist evil and treat others as we would have them treat us. All good dogs know this, and show it in their eyes and behavior. (But they have not forgotten how and where to bite!)
The secure, well-loved and understood dog is more often an extrovert than an ambivert wary of strangers. Secure, well-loved and understood wolves, in contrast (with few exceptions, some of whom become more easy-going around new people and in new places as they grow older, as did Tiny in her early teens), are more often ambiverts or introverts. They are fearful when meeting unfamiliar people. Differences in individual, breed and species autonomic tuning (as mentioned earlier) also account for differences in disease resistance, temperament and learning ability.
The Canid Conscience
Good dogs can see and respond to our own deep heart’s core of love and devotion because it is from this center of our own being that we embrace and celebrate theirs. That is what Franz Kafka in his essay, Investigation of a Dog, meant, I believe, when he wrote: “All knowledge, the totality of all questions and all awareness, is contained in the dog.” And this is why the ancient Egyptians believed that dogs were our guide in the afterlife—they were such good guides and loyal companions in real life. Embodying finer qualities of feeling and sensibility than the relatively irresponsible and emotionally challenged average human, dogs are worthy of being looked up to with awe and gratitude. We should help others of our own kind feel and know that in the deep heart’s core of all good dogs and wild wolves lies the source of an abiding affection that we, in moments of grace and communion, may share.
Since this core is as evident in a wolf as it is in a Toy Poodle, it is clear that neither domestication nor wildness has altered their true natures. In the heart of every dog is the spirit of the wolf that embodies the finer qualities of human nature that we call love and devotion.
News: Guest Posts
I had watched the dog origin wars as a chronicler of the dog-human relationship for several decades when in 2009 I was approached a young editor The Overlook Press about writing a book on the origins of the dog. I readily agreed, and the result was How the Dog Became the Dog.
Pondering the conflicting dates, places, and theories associated with the emergence of the dog, I concluded that as soon as our forebears met wolves on the trail they formed an alliance of kindred spirits, and the process began. Their basic social unit was a family with ma and pa at the head and young ones of varying competency. They worked and hunted cooperatively. They were consummately social but capable of prolonged solo journeys.
It made sense that the Middle East, if not North Africa, was where this all started because that would have been the region of first contact. But because of their natural affinity, wolves and humans got together wherever they met. Some of the resultant “dogwolves”—my phrase for doglike wolves or wolves that act like dogs—created lineages that survived a while then fizzled out; others endured.
I identified several hotspots for early dogs across Eurasia and a group of humans that at least according to genetic evidence might have made its way through the cold of the last Ice Age from the Persian Gulf oasis, then a fertile land, to the Altai Mountains of Central Asia, a region that also hosts the headwaters of the Amur River, still famous for its wildlife. This group’s dogwolves mixed and matched with others along the way, especially the big mountain dogs of the Caucasus. This group of hunters and foragers gathered in the Altai around 40,000 years ago and from there ultimately took the New World.* They also went with their dogs, I calculated, south and east into China, Korea, and Japan and west again with their giant dogs, now mastiffs.
I based that conclusion in part on the types of dogs found in the New World. It made more sense that the possibility for the phenotype was present even if the phenotype itself was not manifest than that it was introduced later.
It was with some interest, then, that I read in PLoS One for July 28, 2011, about a 33,000 year old ‘incipient” dog from the Altai Mountains—that is, an early attempt at a dog that went nowhere. The finding was immediately challenged, and the fossil dismissed as a wolf, even if a strange one. So a new team of researchers redid the work in Robert K. Wayne’s evolutionary biology lab at UCLA and on March 7, 2013, published an article in PLoS One confirming that the 33,000 year-old-fossil is that of a primitive dog.
Writing for their colleagues from Russia, Spain, and the U.S., Anna S. Druzhkova of the Siberian Branch of the Russian Academy of Sciences and Olaf Thalmann of Turku University, Finland, state that when compared with other canids, the Altai dog, as it is known, shows closest affinities with New World dogs and modern dog breeds, ranging from Newfoundlands to Chinese Cresteds and including cocker spaniels, Tibetan mastiffs, and Siberian huskies.
Equally interesting from my perspective, the Altai dog does not appear to have been related closely to wolves in its immediate vicinity or to modern wolves. It came to the Altai from elsewhere, probably with people.
The researchers emphasize that there is uncertainty in their findings because they are based on a single region of mitochondrial DNA. But from my standpoint, the work provides one bit of evidence that’s I’ve not been barking up the wrong tree—and that seems worth noting.
*Ted Goebel et al., “The Late Pleistocene Dispersal of Modern Humans to the Americas,” Science, March 14, 2008. Connie J. Kolman et al., “Mitochondrial DNA Analysis of Mongolian Populations and Implications for the Origin of New World Founders,” Genetics, April 1996.
Good Dog: Behavior & Training
More than just noise
A friend suggested that one of the reasons we love dogs so much is that they can’t talk back. But I wonder whether that’s true. Sure, a dog won’t tell you, “You really shouldn’t have that second cookie,” but does that mean dogs are not talking back?
Dogs are anything but mute, and while we usually focus on wagging tails and beguiling eyes, vocalizations—among them, barks and growls—provide us with another window into dogs’ everyday experiences.
Social species are known to be much noisier than animals who lead solitary lives. Snow leopards roam the mountains of central Asia in near silence, but groups of monkeys do a lot of highvolume chattering. So, given that dogs and their wild progenitor, the wolf, are über-social, it’s no surprise that both produce a wide range of vocalizations: they bark, whine, whimper, howl, huff, growl, yelp and yip (among other nuanced sounds). From the earliest moments of their lives, dogs and their canid relatives produce tonal yelps and whines, and atonal barks and grunts appear in the fi rst few weeks of life in conjunction with the onset of social behavior.
There’s a big difference between the bark of an adult dog and that of an adult wolf, however. Dogs seem to play every instrument in the orchestra, hitting the highs of the flute and the lows of the tuba, sometimes with the duration of a Wagnerian opera. Plus, there seems to be no context in which a dog won’t bark: They bark when alone and with other dogs. Some bark before, during and even after a ball is thrown. A car goes by or the doorbell rings and barking ensues. In contrast, wolves bark less frequently and in fewer contexts, primarily for warning or defense.
Meanings Behind the Message
That being said, research that has been conducted on the subject is incredibly insightful. Take growls, which, it has been shown, dogs use to accurately judge another dog’s size. How in the world do we know that? Tamás Faragó, PhD, and his colleagues at the Family Dog Project at Eötvös Loránd University in Budapest (familydogproject.elte.hu) presented dogs with two images of the same dog: one was true to size and another was 30 percent larger or smaller. Dogs then listened to a pre-recorded growl, and most dogs looked at the image of the full-size dog rather than the altered image.
Growls appear to be meaningful in other ways as well. In another study, Faragó and his colleagues used some clever trickery to explore how dogs respond to growls recorded in different situations. In an apparently empty room, a dog was allowed to approach a bone. Unbeknownst to the dog, there was a speaker hidden behind the bone, and as the dog approached, the sound of a “play growl,” a “stranger-approaching” growl or a “food-guarding” growl was transmitted through it. Dogs were likely to take the bone when hearing the “stranger-approaching” or “play” growl, but the food-guarding “my bone” growl deterred them. Even though the foodguarding and stranger-approaching growls sound quite similar (at least, to our ears), they prompted different behavior.
Many studies investigating vocalizations are based on prerecorded samples, but it is important to remember that vocalizations and visual signals usually go hand-in-hand. In the strangerapproaching context, dogs growled with closed mouths, whereas in fooddefense situations, they showed their teeth and pulled back their lips.
While we tend to take notice when we hear a growl, we often dismiss barking as meaningless noise, as though it is simply an item on a dog’s daily checklist: “Take a walk, have breakfast, bark.” Before the turn of the century, that was the prevailing view among researchers and theorists. At most, barking was thought to result from social facilitation— one dog barking prompts other dogs to bark—or maybe attentionseeking, or even rivalry or defense.
Only recently have researchers begun to investigate whether barks produced in different contexts vary in their acoustic parameters (such as tone and pitch). Scientists theorized that if— like growls—barks displayed consistent differences, they might have a more specific communicative function, perhaps even be associated with a dog’s internal motivational or emotional state. For example, some barks might convey aggression while others might convey friendliness.
In one early study, Sophia Yin, DVM, MS, recorded a variety of breeds barking in response to different situations: a stranger ringing the doorbell (“disturbance barks”), separated from an owner (“isolation barks”) and play. Yin found that the barks did indeed have different acoustic properties. Disturbance barks were harsher and lower in pitch with little amplitude modulation, while isolation and play barks were pitched higher and had greater tonal and higher frequency and a wider range of amplitude modulation. More recent studies confirm that dog barks follow particular patterns. For example, a dog barking at a stranger sounds very different from a dog barking before going on a walk. But do these vocalizations carry meaning? They do for dogs. When dogs in one study listened to barks recorded in a new context or from a new dog, they gave more attention to the unfamiliar bark. This suggests that dogs can detect that some barks are different from others, though scientists are still exploring ways to determine how exactly they perceive and process that information. Humans, too, can decipher barks. Whether or not they’re experienced with dogs, people are quite good at classifying barks into their appropriate contexts and attributing them to perceived emotional states. After listening to randomly played recordings, people describe isolation barks as full of despair, while barks from a play session are said to be happy. Our ability to do this starts early; by age 10, children are able to assign different-sounding barks to the correct context. Today, we can distinguish the acoustic properties of certain barks so accurately that we’re able to program computers to categorize them (which confirms that computers will one day take over the earth; personally, I hope Ryan Gosling will be there to save us).
Recognizing the Patterns
A recent publication by Kathryn Lord, PhD, offers an additional take on why dogs bark. She and colleague Ray Coppinger, PhD, investigated the contexts in which other species use barklike sounds: “When other species emit their version of a bark, they are usually in some sort of conf licting situation. For example, an animal is at a nest or den and observes some sort of threat. Customarily, the animal would run, but because of its situation, it can’t, so it barks. We think [that] when dogs bark, they are making these sounds in association with an alert or an internal motivational state of conflict.”
In a sense, Lord and Coppinger argue that “conflicted” should be dogs’ middle name. They suggest that dogs bark in so many different situations because they often find themselves conflicted: they are in the house and want to go out, they are out and want to come in. And it may be that, through the process of domestication itself, dogs have become more prone to put themselves in these sorts of situations. In comparison with wolves, dogs have a substantially decreased f light distance; something can easily get too close before the dog feels conf licted about how to respond.
Udell suggests that barking doesn’t have to be whittled down to one simple explanation. “If you look at communication and vocalizations in a wide range of species, it usually isn’t about one thing. Chickadees have ‘alert’ calls, but they also have songs, and the songs themselves can mean different things in different contexts. I think the same could hold true for dogs.”
But genes aren’t everything. As Susan Friedman, PhD, a pioneer in the application of applied behavior analysis to captive and companion animals and a psychology professor at Utah State University, explains, “While Shih Tzus as a group tend to display less barking than Miniature Poodles, that doesn’t mean barking in Miniature Poodles is impervious to change. And I’ve certainly known individual Miniature Poodles who are quiet and individual Shih Tzus who are barky, both based on their current situations. The individual always bests any generalization.”
Dr. Yin’s study of dog barks concurs. Even within breeds, she found variations in who barked and when. Rudy and Siggy, 11-year-old German Shorthaired Pointers, both barked in the disturbance context, but when alone, Rudy did not bark and Siggy had lots to say.
The effects of the social environment on dog behavior can be important because sometimes, dogs just go with the flow. On The Bark’s Facebook page, Bev Morey of Kansas commented, “After attending day care each afternoon, my Weimaraner now barks at anything and everything. So annoying.”
“So annoying” is one of the challenges of barking. While all vocalizations, including barking, are generally seen as normal elements of dog behavior, barking is one of dogs’ less-appreciated attributes. According to Laura Monaco Torelli, CPDT-KA, KPA CTP, director of training at Animal Behavior Training Concepts in Chicago, “Barking can be especially challenging for those in urban settings, as they live in close quarters with neighbors.” Owners of barking dogs might receive dirty looks or formal complaints from neighbors, and enough complaints can lead to eviction.
Though dogs bark for any reason under the sun, barking is a construct of context, genes and environment, and so is flexible. For example, feral dogs are much less noisy than their counterparts who play with toys, sleep in beds and go to obedience class.
Friedman explains. “For dogs, barking is a functional behavior, meaning it is maintained, increased or decreased due to consequences. Once this is [understood], it opens the door to changing the duration, intensity and frequency of the behavior by changing the consequences.” In other words, dogs can learn to be quieter.
However, perfect quiet is probably unrealistic. Owners can’t always control the stimuli that prompt barking, especially if they’re not home 24/7. Moreover, barking that has been solidified and maintained over time through intermittent reinforcement has a lot of staying power. “It seems that owners unintentionally reinforce the barks produced when a dog is around food or toys, and these become the begging barks of that dog,” says Faragó.
Monaco Torelli agrees. “If a dog learns that the noise in the hallway goes away when he barks, barking becomes an effective behavior. Barking is followed by the consequence of the noise in the hallway stopping.”
Owners should focus not on eliminating barking altogether, but on reducing it to levels they find appropriate and livable. When she meets with clients to discuss their dogs’ barking issues, Monaco Torelli asks questions such as, “How many barks is okay? What’s excessive to you?” This, she says, gives the trainer a good starting point from which to develop a plan to teach the client how to reshape a dog’s barking behavior. Trainers and owners discuss acceptable barking, and then implement techniques to achieve desired levels in each context.
Friedman shares the way she manages her own dog’s barking: “We live in the country, and when we let the dogs out, they bark at the deer for a number of seconds. Then we say, ‘That’s enough, thank you,’ and they are quiet and we praise them.” She adds, “It’s a [mistake] to think that barking is the problem. The real problem is that dogs don’t stop barking when we ask.”
So-called “quick fixes” can make barking worse, particularly if the underlying reason for the behavior isn’t addressed. “Putting an anti-bark collar on a fearful dog is unlikely to decrease barking if the consequence [shock or spray] increases the dog’s fear. If the fear increases, barking could as well,” explains Marylandbased Mary Huntsberry, MA, ACAAB.
Strategies for Change
Barking can be managed and modified, so if you want to influence your dog’s vocal style, it helps to start early and be observant. Teaching dogs the boundaries of acceptable vocalizations from an early age will pay off for everyone; when dogs are young, barking might be cute, but as they age, the cute factor tends to wear off. If the behavior is already in place, there are ways to alter it, Huntsberry observes. “It helps to do a functional analysis. During an extensive interview, I identify what happens immediately before (antecedent) and after (consequence) the unwanted behavior so I can identify the trigger and what maintains it.”
Monaco Torelli focuses her attention on the dog-human relationship. “When owners are frustrated by their dog’s behavior, we show them some immediate training goals and success points so they see that their dog can do what they want them to be doing, instead of what they don’t want them to do. This helps them rebuild their bond with their dog.”
The takeaway message is that barking is a nuanced and flexible behavior, and relationships can grow by paying attention to what your dog’s vocalizations mean. And if you’re on a post-holiday diet and want to train your dog to bark incessantly whenever you make a move for another slice of cake, well, that’s just good teamwork.
News: Guest Posts
Dogs and wolves share a similar genetic profile. So why are their behaviors so different?
The reasons aren’t clearly understood. In a recent paper in the journal Ethology , evolutionary biologist Kathryn Lord's doctoral research (University of Massachusetts, Amherst) suggests differences in later behaviors might be related to the pups' earliest sensory experiences during the critical period of socialization, the brief period when a puppy's exposure to novel things results in long-term familiarity.
Lord's research demonstrated that dog and wolf pups acquire their senses at the same time:
· Hearing: Onset 19 days, reliable by 28 days
· Seeing: Onset 26 days, reliable by 42 days
· Smelling: Reliable by 14 days (onset likely earlier)
· Dog pups wait until 28 days to explore their environment when all senses are operational.
· Wolf pups begin exploring the world at 14 days, relying solely on scent, when they are still blind and deaf.
Although wolves are tolerant of humans and things they were introduced to during the critical period, they don't generalize that familiarity to other people or novel things when they mature. Dogs on the other hand, can generalize, and if properly socialized are not spooked by novel sounds and sights.
Why do mature dogs and wolves behave so differently? Lord's conclusion is that at the gene level, the difference may be when the gene is switched on, not the gene itself.
What could that mean? Research has shown that the brain is capable or rewiring itself in dramatic ways. Early loss of a sense affects brain development. For instance, even though the developing auditory cortex of a profoundly deaf infant is not exposed to sound stimuli, it doesn't atrophy due to lack of use. Rather it adapts and takes on processing tasks of other senses including sight and touch. Perhaps wolves see the world in smell, and dogs see it a lot more like we do.
Click here to read the paper, A Comparison of the Sensory Development of Wolves (Canis lupus lupus) and Dogs (Canis lupus familiaris), by Kathryn Lord, Ethology, February, 2013.
News: Guest Posts
“Where goeth the food, so goeth the dog.” (old proverb)
The earliest archeological evidence dates dogs to about 14,000 years ago. Remains of small dogs in Israel go back 12,000 years. When people settled down in agricultural communities, they began to tinker with the natural environment, bringing about modification, intentionally or accidentally, in plants and animals. Of course dogs joined the party. They always do.
Not everyone agrees about why, where, when or how dogs evolved. But we all believe this: Whether dog domestication was accidental or intentional, abrupt of slow, happened 10,000 years ago or 80,000, domestic dogs descended from wolves and evolved with people. Perhaps it’s no coincidence then that we ask the same questions about dogs that we do of ourselves: How are we unique? Where do we come from? And when did we get here?
On Wednesday, January 23, canine geneticists announced they have identified key mutations in three genetic regions that allowed the wolf, a traditional carnivore to thrive on a carbohydrate diet. This adaptation was surely useful for opportunistic animals that were scavenging waste near ancient farming communities.
How they did it
Geneticists Erik Axelsson and his team at Sweden’s Uppsala University looked at DNA from gray wolves and domestic dogs, searching for small differences that might have shown up early in evolution as wolves transitioned to dogs. They zeroed in on specific mutations that dogs have and wolves don’t. In all, researchers found 36 genomic regions that reveal differences. Nineteen of those have to do with brain function, eight are related to the nervous system, and the rest are linked to starch digestion and fat metabolism, three of which carry instructions for making a protein that’s necessary for the digestion of starch. One is an enzyme that turns starch into sugar maltose. Another is an enzyme that turns maltose into glucose. And the third makes a protein that moves glucose from the gut into the bloodstream.
What does it mean?
If you think it answers the question as to why, where, and when dogs were domesticated, you’d be misinformed. It’s really more interesting than that.
1. Dogs eat more starch than wolves. The mutation explains why. Keep in mind that just because you have a mutation that lets you digest grain, it doesn’t mean, when given the opportunity, you wouldn’t rather have pork chops than cheerios. Just ask my dog, or my spouse for that matter. Wolves, dogs or proto-dogs (depending on your position) could have had the mutation long before humans planted grains. The study doesn’t suggest a time line.
2. Because all the breeds in the study have the mutation, the mutation occurred before these breeds radiated out from their direct ancestor. However, don’t assume that our modern breeds are representative of any dogs older than 500 years. There is a ginormous gap, at least 8 thousand years, between the ancient agrarian gang of dumpster diver dogs and the not-so-old proto dog that begat our modern breeds. Scientists don’t know if the missing link dog is extinct, and if she isn’t, they don’t know what living dogs would represent her. There’s plenty more work to be done.
3. The birth of agriculture impacted canids. But it did the same to humans, birds, insects, pigs, cows, and goats to name a few.
4. The study is a vindication for all the veterinarians who are treating dogs with kidney ailments as a consequence of the strange trend toward very expensive low-carb, raw meat diets. There’s a reason dog food is only 20- 30 % protein and 40 to 50% carbohydrates.
What others are saying
“Dogs are not just ‘tame wolves’ but have clearly adapted in a host of different ways to a very novel niche over a relatively short evolutionary timescale," said Adam Boyko, an expert on canine genetics and assistant professor of biomedical science at the Cornell University College of Veterinary Medicine and director of the Village Dog Diversity Project. “I think a lot of focus on dog domestication in the past centered on behavior and tameness. Clearly, they were important for domestication, but this paper also demonstrates genetic changes involved in diet adaptation.”
“The bigger question about the paper, said behavioral ecologist Ray Coppinger, is whether it sheds any light on the evolution of the dog -- whether they were domesticated "purposefully" by humans, or were they a result of humans creating a new niche which several species (including some Canis species) moved in and adapted to.” He added, “The researchers have done a great job showing that dogs and wolves genetically differ in their potential ability to digest starch. But it’s a fallacy to assume that the genes of the modern dogs included in the study are descended from original dogs. Thus the paper, sheds little light on the original dog, and does nothing to answer the question of artificial verses natural selection as the prime cause.”
What’s important about the study is not that it indicates when or where dogs originated. Rather, it’s a new tool that will help us understand how dogs and wolves are different. The research is groundbreaking, but it represents analysis of only 10 of the 36 genomic regions that the team identified. That means more exciting news is just around the corner.
Scholarly study takes on issues that are controversial. The dog origin debate continues to be particularly provocative. As for me, I just want to know who to thank.
Mark Derr, author of When the Dog Became the Dog has a very interesting post on this subject as well.
The genomic signature of dog domestication reveals adaptation to a starch-rich diet, Journal Nature, published on-line, January 23, 2013.
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