Domestication and Tameness: What Do We Really Know?

In early July 2014, the journal Genetics published a long theoretical article speculating on the biological mechanism behind the suite of behavioral, physiological, and morphological changes that occur in domesticated mammals but not in their wild forebears. These changes include floppy ears, shorter muzzles, smaller teeth, reduced brain size, curly tails, “docility,” and neotenous or juvenile behavior, according to the authors.

Together these characteristics constitute what the authors call the Domestication Syndrome, a name borrowed from plant geneticists, and are a result of changing cellular development from the neural crest. The neural crest is a group of multipotent stem cells that migrate through the body and differentiate into cells having to do with skin pigmentation, cranial cavity shape and size, and facial structure, as well as the sensory, sympathetic, and parasympathetic nervous systems. What the neural crest cell ultimately becomes is dependent largely on its context.

In their aptly titled paper, “The ‘Domestication Syndrome’ in Mammals: A Unified Explanation Based on Neural Crest Behavior and Genetics” by Adam S. Wilkins, whose multiple appointments include one at Humboldt University’s Institute of Theoretical Biology, Richard Wrangham at Harvard University, and W. Tecumseh Fitch at the University of Vienna, argue that multiple genetic mutations affect the expression of neural crest cells for various parts of the body to varying degrees, largely by reducing the number of cells produced.

The researchers also work to cast their theory in Darwinian terms, arguing that Darwin first identified and sought to explain the changes that occurred under domestication but, because he was unaware of genes, he could not have—and, indeed, did not—identify the cause. The authors say that they are completing his work.

This is a mechanistic view of an as yet unexplained phenomenon. It has a coherence and simplicity that appeal to many science journalists, but it also has several significant problems, primary among them an attempt to make selection for “docility,” which they define here as “tameness,” the trigger for the entire Domestication Syndrome. It is that, they say, citing Darwin and Dmitry Belyaev, a Russian geneticist who conducted experiments with Siberian silver foxes from a fur farm designed to elucidate the genes behind domestication.

Belyaev and his colleagues claimed that by breeding solely for “tameness,” they produced doglike foxes with piebald coats and a nearly pathological craving for human attention. These foxes served as a model for the way wolves became domestic dogs, Belyaev and his followers argued. I have offered extensive critiques of this work elsewhere, as have other people, and each criticism elicited, like now, a slightly different restatement of the experiment, its methodology and conclusion. (See also my blog post on this subject.)

Following Belyaev, Professors Wilkins, Wrangham, and Fitch would make breeding for tameness, which they say alters the hypothalamic-pituitary-adrenal system [HPA axis}, the trigger for the Domestication Syndrome, the unfurling of reduced numbers of cells from the neural crest, altered by genetic mutation, at its various destinations.

“In a nutshell, we suggest that initial selection for tameness leads to reduction of neural crest derived tissues of behavioral relevance via multiple preexisting genetic variants that affect neural crest cell numbers at the final sites, and that this neural crest hypoproduction produces, as an unselected by product, the morphological changes in pigmentation, jaws, teeth, ears, etc. exhibited in DS,” they write. Domestication becomes genetically predetermined.

But is selection for tameness alone, the path of domestication, even for dog? Related to that is the more fundamental question of what is meant by “docility” and ‘tameness’ and how one can hope to define the behavior of early dogs based on the behavior of those today?

Beylaev and his followers almost certainly produced foxes with reduced flight response, which they called tameness, and increased response, which led the cornered animal to flee and then fight when cornered—a response the researchers call aggression. Fear aggression is but one form of aggression.

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There is no evidence dogs were created through selection for tameness alone—neither self-selection nor human directed selection. Nor were they made free of aggression by design or accident. Among the world’s approximately one-billion dogs are a large number capable of attacking, killing, and consuming other human and non-human animals. [See for example Free-Ranging Dogs & Wildlife Conservation (2014). They might still look like domestic dogs, but they are wild--feral--and sometimes dangerous.

Could it be possible that the researchers are, in fact, looking at more recent developments in what we might call the continuing domestication of the dog?

English and European dog fanciers began wanting more tractable dogs in the mid-19^th century when they started to bring their canine companions into cities and demand well trained gundogs and retrievers. At that time, they also wanted more human- and juvenile- looking dogs. Free-ranging and randomly breeding village dogs, especially in the developing world, were considered untrained and useful only for scavenging.

“Everywhere the dog is what man has made him,” wrote the essayist and long-time editor Charles Dudley Moore in the January 1896 edition of Harper’s New Monthly Magazine. In America, he went on, the dog is “often tamed and registered, sometimes collared, occasionally muzzled, and now and then pounded. But as a general rule, the dog is too free and has not learned his place.” Dogs were taught their place with choke chains, chain link fences, leash laws, and death if they were caught running freely. They were made to look civilized through intensive breeding.

Today, ironically enough, a popular kind of dog is the pitbull and its crosses. Becoming common enough to form their own landrace, these dogs are capable of assaulting and killing people among whom they live without warning. They rouse fear of dogs in many people.

There also is no real evidence that early domesticated animals, from donkeys to water buffalo, Asian elephants to llamas were initially selectively bred for docility or tameness. Indeed, there appears to have been continual outcrossing to wild stock for most domesticated animals for sometimes considerable periods after “domestication.”

The researchers also argue that contrary to popular belief domestic animals do not revert to the wild type after they go feral. While they might not revert completely in terms of appearance, feral populations can be the opposite of docile or tame. Critical socialization periods, lengthened during domestication, are often shortened in feral animals.

An equally serious problem is raised by the researchers almost in passing: their theory does not account for curly tails, among the signature manifestations of domestication in many species. There are other problems to watch for but what better place to end for now than with the tightly curled tail of a pig?