For thousands of years, dogs have worked with us, eaten with us, lived with us. Do they also think like us, wonders Kate Douglas

I HAVE a confession to make. I'm not a great dog lover. I simply can't trust a designer wolf. You may see man's best friend, but I see a wild animal that has inveigled its way into our homes and hearts. Sure, it can look cute. But I've always suspected that this beast might leap at my throat without a second thought. After all, dogs just don't understand that such behaviour is socially unacceptable. Or do they?

It turns out that far from being an interloper and socially inept, the dog is the product of tens of thousands of years of evolution in a very particular environment--our homes.

In recent years, evidence has emerged that dogs and humans have been living together for much longer than anyone ever expected. Genetic evidence suggests that we began to domesticate dogs while we were still hunter-gatherers, living in caves and mastering the first grunts of language (see "New tricks and old dogs"). Researchers are just starting to reveal how this strange partnership has shaped the way canines think and behave. "The dog's natural environment is the human family or other human social settings," says Vilmos Csányi from Eötvös Loránd University in Budapest.

Because humans and dogs evolved together he believes that we share certain patterns of thought that allow us to live together. "Dogs are interested in the emotional and intentional content of the human mind and they are able to learn and to maintain the rules of human social settings," says Csányi. So while others look to apes to shed light on social cognition, his team is pioneering the study of dogs.

One of the first things they did was to investigate the bond between humans and their pooches, to see how like a family member they really are. Dogs and their owners are clearly emotionally attached, and selective breeding has favoured infantile canine features. But, soppiness aside, does the relationship between the two species really resemble the bond between a human parent and child? To find out, József Topál, Ádam Miklósi and other researchers from Csányi's lab gave dogs the "strange situation test", originally devised to study the special bond or attachment that exists between an infant and its mother or primary carer.

A securely attached baby behaves in a characteristic way in a strange situation. Provided the mother is nearby, the infant shows little fear and is happy to explore a new environment. When she leaves, the infant becomes distressed but will usually settle with a stranger. The preference for the mother is clear, however, when she returns and the baby is eager to greet her.

Topál and Miklósi tested how 51 dogs responded to a similar strange situation. The dogs were keen to play and explore in an unfamiliar room, as long as their owner was there. When the owner left, the dogs didn't play so much and showed other signs of anxiety such as barking and waiting by the door. Even if they eventually settled, all well-attached dogs greeted their returning owners enthusiastically. "It seems that dogs and infants behave very similarly," says Miklósi, "and we think this is a result of evolutionary domestication."

Csányi says there are two stages to forming this relationship. First, comes a form of imprinting. If 6 to 12-week-old puppies come into contact with people, their innate capacity to bond leads them to accept humans as a member of their own species. Thereafter a dog can develop an attachment to any person who shows it affection.

The researchers believe that the attachment to people might explain why dogs sometimes appear stupid. Back in 1980, Harry Frank from the University of Michigan-Flint, described how a wolf that could not be trained to sit on command learned to manipulate a complicated door catch simply by watching another wolf open it. But trained dogs couldn't master the catch even after years of seeing the door open and close. Frank concluded that through domestication dogs become obedient and trainable while losing some cognitive abilities such as problem solving. They have a decreased capacity for insight because throughout their evolution human intervention has detached them from the consequences of their actions.

Many people believe that any domestic animal is not as intelligent as its wild relative. Dogs certainly have smaller brains for their body size than wolves, particularly in the areas associated with vision and olfaction. But as Miklósi points out, domestication is not necessarily to blame. One likely ancestor of dogs, the small Asiatic wolf, had a smaller brain than other wolves. What's more, dogs don't seem to have lost other mental abilities that would have helped their ancestors hunt in packs. They understand object permanence--that things don't just disappear even when they can no longer see them. "Dogs are maybe at a similar level in this ability as apes," says Miklósi. And they are capable of making mental maps to allow them to find new routes through familiar territory.

Topál and Miklósi suspected that the poor problem-solving ability of canines did not stem from a loss of mental abilities during their evolution, but from the way an individual dog's behaviour is shaped by its relationship with its owners and by training. The stronger the attachment between a dog and its owner, the researchers suggested, the more likely the pet was to behave in a socially dependent way, relinquishing its powers of independent thought and action.

To test the idea they asked 28 owners to fill in a questionnaire showing the extent of their anthropomorphic attitudes to their dog. Questions included, "How often do you allow the dog into your bed?", "Do you celebrate your dog's birthday?" and "To what extent does your dog identify with your emotions?" The dogs were then given a problem to solve. They had to work out that they could get a food reward by pulling on the handles of plastic dishes that protruded from underneath a wire fence.

Sure enough, the more intimate the bond between dog and owner, the worse the animal at solving the problem. But the differences disappeared as soon as the owners encouraged their dogs to get the food. "Dogs with an intimate bond did not perform worse but showed 'dependent' behaviour," says Miklósi. "It is not that they don't understand the problem."

Csányi and his team can back up this claim with further evidence from their studies of interactions between blind people and guide dogs. "In this case, we find the best problem-solving dogs are those that are strongly attached to their blind masters," says Csányi. Here the bond allows a dog to cooperate with a human to negotiate difficult situations. So, although guide dogs are trained to take control, the researchers found that once an animal develops a bond with its master, it hands over the decision making only to step in when the need arises.

Until now only humans were supposed to be capable of this kind of sophisticated cooperation, where the initiative is constantly shifting between two parties. Other animals only work together where they share interests and objectives, such as those hunting in packs, or defending young offspring.

Obeying the rules

In Csányi's view, domestication has in fact increased the dog's cognitive abilities, not reduced them as Frank believes. By selecting individuals that form strong attachments and are tractable, we have produced an animal that is genetically predisposed to learn and obey rules.

While this is central to the guide dog's abilities, it also means all dogs can fit into their particular social environment. Even without formal training, dogs become socialised simply by being with people. They have a talent for working out the underlying rules. "They easily extract them from games and from observing other dogs or humans," says Csányi.

Marc Bekoff from the University of Colorado has studied how dogs, wolves and coyotes play. "All animals learn certain codes of conduct about their own species' morality through play," he says. "I think dogs learn codes of conduct from humans through dog/human play." They learn the ground rules for acceptable behaviour, such as how hard they can bite without harming. And, like any animal, when dogs play, they hone the behaviours they will need elsewhere.

There is little research into the evolutionary effects of such interactions between dogs and humans, but Bekoff suspects that they have enriched the mental life of dogs. A study in his lab reveals that playful interactions between puppies are much more varied than those between young wolves or coyotes. He thinks dogs have evolved more varied forms of behaviour because of the sophisticated games people play with their pets and the selection for dogs that are good at such games. "It would feed over into other areas," says Bekoff. "In general ways it would make the dog more cognitive."

One area where human contact has certainly enhanced the mental capacity of dogs is communication. Miklósi and his colleagues showed that dogs can learn to respond to subtle human gestures. The pets could retrieve hidden food items when prompted by their owner pointing, bowing, nodding, turning their head and even just glancing towards the hiding place. It may sound simple, but no other animal--not even chimps--performs so well.

The researchers believe that dogs really do understand what gestural cues mean. Rhesus monkeys can find a hidden object that a human is pointing to--but only if the distance between the reward and the end of the finger is less than 20 centimetres. They don't seem to understand about pointing, but instead learn that an outstretched finger may signal that there is food nearby.

In Miklósi's study the distance between gesture and reward did not affect a dog's success. Also, because the cue was given before the dogs were allowed to search for food, there was no way they could simply follow the movement of the gesture. Instead, Miklósi suggest, dogs seem to be drawing a mental line between the finger and the reward. "We think this is the first step to argue that dogs understand that we are communicating something to them."

Last year, researchers at Emory University in Atlanta confirmed the findings, and repeated the experiments using dogs to send gestural cues to other dogs. Brian Hare and Michael Tomasello found that while a six-month-old dog could not understand the human gestures, it could respond to cues from another dog. This pattern was reversed in four-year-old dogs. They argue that perhaps dogs have an innate ability to read gaze cues from each other which they learn to extend to people, while, for some reason, losing that capacity with their own species. "Dogs are genetically selected for their ability to tune in to humans," says Tomasello, who is now at the Max Planck Institute in Leipzig.

Miklósi wanted to find out if dogs could send signals to people as well as receive them. He found that when the pets knew where a reward was hidden, they would make a noise to attract their owners and alternate their gaze between the human and the hiding place. Miklósi interprets this behaviour as "showing". "Dogs are able to do the same as human infants and apes," he says. "What is behind this could be a kind of conditioning or a higher mental process." Miklósi believes it is the latter. He argues that if gaze alternation was simply a learned response the behaviour would not be universal. Also, autistic children--who lack a social sense--do not behave in this way.

Tomasello takes a more sceptical view. "Gaze alternation can mean different things and I don't think it means dogs are pointing," he says. "I think they are looking back to check and see whether you are coming." He has found that goats also show this behaviour. "I think gaze alternation is a general mammalian ability, but the dogs are really tuned in," he says.

Symbols and signals

Now Csányi's group is looking at dogs' grasp of language. On average, they found that mature pets understand 40 expressions, mostly signalling actions. The range was between 7 and 80. "Their understanding is different from ours," says Csányi. "We use words as symbols, they use words as signals mainly." So, for example, dogs can extract simple information such as whether they will be going for a walk and who will be taking them. It's not clear how they do it, but the ability can't be explained by simple conditioning because these words are embedded in long sentences, and hearing the word is not immediately followed by going for a walk.

The remarkable social skills of dogs are understandable given that they are adapted to the same environment as we are. "The root of human evolution was crowding," says Csányi. "We do not know exactly why, but early humans started to lump together, which created a complex behavioural problem to be solved." He argues that communication, social bonding, following rules and cooperation have evolved in people and dogs so that both species can cope with this unusual setting. In addition, humans have the ultimate social glue, empathy--we can see into one another's minds. To say that dogs possess similar insight is highly controversial, yet Csányi and others claim that they do.

Most researchers accept that only animals that can recognise themselves in a mirror are self-aware, allowing them to empathise, sympathise and attribute intent and emotions in others. Dogs do not pass the test. And imagine removing porcupine quills from your dog's nose. Ouch! Yet another dog watching this operation would be oblivious to the suffering, according to Gordon Gallup from the State University of New York at Albany, who invented the mirror test. He argues that because dogs have no sense of self, they cannot use their experience of pain to attribute painful experiences to others.

But Csányi suggests that dogs can perceive when a person or another dog is in danger and empathise with the emotional state of people who are sad or ill. Bekoff agrees. In his forthcoming book on animal emotions, he recounts the story of a dog who saved the life of his canine companion by awaking their owner to let him know that the second dog was ill. Bekoff also tells a tale about his own dog, Jethro, who adopted an orphaned rabbit and, years later, rescued an injured bird. "I think Jethro is a truly compassionate soul," writes Bekoff. "He could easily have gulped each down with little effort. But you don't do that to friends, do you?"

Jeffrey Masson, author of Dogs never lie about love, has no doubt that dogs empathise with humans. "If they're not self-aware, how come they can appear so guilty?" he asks. Csányi even goes so far as to compare canine attachment with human love--empathy incarnate. Masson believes that dogs could teach us a thing or two about love and, indeed, may already have done so. Dogs have been part of our evolutionary environment, just as we have been part of theirs. "There may be mutual influences," he says.

Further reading:

"Attachment behavior in dogs" by József Topál, Adam Miklósi and others, Journal of Comparative Psychology, vol 112, p 219 (1998); "Dog-human relationship affects problem solving behavior in the dog" by József Topál and others, Anthrozoos, vol 10, p 214 (1997); " Domestic dogs use human and conspecific social cues to locate hidden food" by Brian Hare and Michael Tomasello, Journal of Comparative Psychology, vol 113, p 173 (1999)

New tricks and old dogs

Canine remains at human burial sites led researchers to suspect that dogs became domesticated around the time that our nomadic hunter-gatherer ancestors settled down to grow crops, around 14 000 years ago, long before we acquired goats, cattle and sheep. But in 1997, Carles Vilá and researchers in Robert Wayne's lab at the University of California at Los Angeles blew this idea wide open.

They compared mitochondrial DNA from 67 breeds of dogs with that from wolves, coyotes and jackals. The studies revealed at least four separate lines of descent from dogs back to wolves, showing that there were at least four successful attempts to domesticate them. The real surprise, though, was the high level of genetic variation between different breeds. "The mitochondrial DNA data suggest very clearly that the diversity found in dogs might have an origin much older than 14 000 years," says Vilá. Knowing the rate at which these DNA sequences change, he estimated that the split with wolves--and hence domestication--occurred around 135 000 years ago.

If this is right, domestication started at around the time that our own species evolved, and perhaps not long after our ancestors acquired language. Pet ownership could well pre-date such cultural mainstays as art and the practice of burying the dead. But even Vilá, now at Uppsala University in Sweden, accepts that the date is controversial. Wayne hopes new research will pin it down. "We are examining ancient breeds, such as the Xolo, ancient remains from the Middle East and South America of the earliest dogs and nuclear genetic markers," he says.

From New Scientist magazine, 26 February 2000.