For centuries, conventional wisdom says that an animal's coat color and its temperament may go together. For example, individuals with lots of depigmented, white fur -- paint horses, white cats, depigmented pointers -- are sometimes found to be nervous. The evidence suggests that this wisdom is not always an old wives' tale. Coat color and temperament are sometimes connected, because there are links between hormone chemistry, neural development, and pigment production. The relationship between temperament and coat color may have played an important role in the domestication of different species, including the Norway rat.
Temperament is an individual's way of responding to the world. Shy, bold, cautious, irritable, docile, reactive, and passive are all examples of temperament. An individual's temperament tends to be consistent between situations and over an individual's lifetime.
One of the most striking differences between wild animals and domestic animals is the difference in their temperaments.
Wild animals tend to be highly reactive to their environment. When excited they tend to react strongly, even violently. Wild animals in captivity respond stressfully to things like unexpected movement, sounds, transportation, and proximity to humans. A wild fox brought into captivity cringes and shrinks away from an approaching human hand, and if pressed closely it may lash out and bite. Adult wild red foxes brought into captivity have even broken off their canine teeth in an attempt to escape, and one wild fox has been reported to have torn at the wooden door of his cage in a frenzy until he dropped dead from exhaustion (Keeler et al. 1970).
Domestic animals, in contrast, are more passive toward their environment. They are not stressed by unexpected movement, sounds, or the proximity to humans. Domestic animals tend to be docile and placid when compared to their wild counterparts.
Wild animals are so stressed and so reactive to the captive environment that they have trouble thriving and breeding in captivity, and are difficult for humans to approach and handle. For these reasons, one of the key features of domestication is a temperament shift from the reactive wild temperament to the docile domestic temperament. A docile, unreactive animal is less stressed by its environment, easier to handle, and more productive than a reactive, intractable one.
This change from wild to domestic temperament has many, many facets. Among them are:
Selection from proximity to humans: Part of the temperament shift may happen before the wild animals even enter captivity. Some wild animals live in close proximity to humans, benefitting from the waste, shelter, and predator deterrence inadvertently provided by humans. The individual wild animals that react less to the humans may derive a greater benefit from them. This reduction in reactivity may make these animals easier to domesticate at a later date. For example, domestic dogs may be descended not from wild wolf cubs brought into captivity, but from wolves that fed on village trash heaps and became less reactive to humans over many generations (Coppinger and Coppinger 2001).
Natural selection in captivity: Once the wild animals are captive, the most stressed, reactive animals may die or fail to breed. These animals leave no descendants. The less stressed, less reactive animals have a higher chance of surviving and breeding in captivity. Hence, through the process of natural selection, the subsequent generations contain a higher percentage of docile individuals than the original captive group.
Artificial selection for docility: Humans play a large role in the temperament shift by choosing to breed only the calmest, most docile animals.
Taming of individuals: Within the lifespan of the individual, young animals socialized to humans are less stressed by human presence (e.g. Galef 1970). Physiologically, the adrenal glands of rats handled when young are less responsive to stress (Levine 1968, Levine et al. 1967). Selection and taming interact. Over the generations, the animals' tamability increases, its potential level of tameness. Whether an animal's potential degree of tameness is reached depends on its experience with humans (see Price 2002 for a whole book on the subject).
Note, however, that "reduced reactivity to the environment" and "taming" are not the same thing. It is possible to tame young wild animals by handling them frequently. Such handling greatly reduces their aggression toward humans, but it has little effect on timidity in novel situations and other behaviors typical of wild rats (in rats, Galef 1970). Wild animals accustomed to the presence of humans may remain highly reactive to new stimuli in their environment like loud noises, sudden movement, and novel objects (Grandin et al. 1995). Therefore, a tame wild animal may be quite different from a tame domestic one.
Coat color is a small but fascinating part of the story of domestication and behavior. Links between coat color and temperament have been found in species as diverse as cats, dogs, foxes, mink, rats, deermice, and fallow deer (e.g. Hemmer 1990, Keeler and and Moore 1961, Trut 1999, Trapezov 1997).
For example, light colored fallow deer become tamer than those with wild-type coloration (Hemmer 1990). Black cats tend to be more placid than wild-type agoutis, which may be why black cats are found more commonly in cities while agoutis are more common on farms (Todd 1977).
Color and temperament are linked in foxes, too. Foxes of different colors display different levels of fearfulness toward humans. One way to measure fearfulness is the distance a wild animal keeps between itself and a human (the flight distance). In a vivid account, Keeler et al. (1964, 1965, 1970) describes walking into an large fenced-in range containing many foxes, and seeing different color foxes at different distances. The red foxes were the shyest and stayed much more than 200 yards away from the human, usually out of sight. The silver-colored foxes were a little bolder and were spotted about 200 yards away. Pearl-colored foxes maintained a distance of about 150 yards, while amber-colored foxes actually approached humans, coming as close as 15 feet, and sometimes as near as 12 inches. The author's overall impression was of a color gradient of fearfulness. Flight distance wasn't the only behavior linked to color in foxes: the amber foxes were also less active than silver foxes, they ran more slowly, and were less aggresive toward other foxes when feeding (Keeler et al. 1968).
So, in many species, there is a relationship between coat colors and behavior. How is that possible?
This strange link between coat color and temperament stems from a relationship between pigment production, hormones, and neurochemistry. It is not the case that coat color causes a difference in temperament, but rather that certain physiological processes underlie facets of both coat color and behavior. In particular, the hormones and neurotransmitters involved in the stress response and other behaviors are closely integrated with pigment production.
For example, the neurotransmitter dopamine and the hormones noradrenaline and adrenaline, which are involved in the stress response, have the same biochemical precursor as the melanin pigments (Anonymous 1971, Ferry and Zimmerman 1964). In addition, dopamine directly influences pigment production by binding to the pigment-producing cells (Burchill et al. 1986). Dopamine indirectly influences pigment production by inhibiting pituitary melanotropin, also known as melanocyte stimulating hormone (MSH), which is responsible for stimulating pigment cells to produce pigment (Tilders and Smelik 1978).
Therefore, by breeding only the most docile animals in a group, humans select for physiological changes in the animal's hormonal and neurochemical systems, changes that impact morphology and physiology -- including fur color. A change in fur color during domestication may therefore be an incidental byproduct of selection for tameness.
Here are two examples of the links between a particular coat color and temperament:
Pigment cells are found in the skin and at the base of hairs, where they produce pigment that colors the fur. But pigment cells and pigments aren't just found in the skin, they're also found in the brain, including brain regions related to mood and stress.
During development, pigment calls start out at the back (in an area called the neural crest) and migrate to the rest of the body (Gilbert 1994). Anything that affects the distribution of pigment cells in the body affects not only the hair color, but mood and stress as well. The hooded gene of the Norway rat (Wendt-Wagener 1961) and the star gene of silver foxes (Praslova 1993) are examples of genes that delay the migration of pigment cells from the back to the rest of the body.
Cell migration isn't the only connection between depigmentation and the stress response. The pigment melanin also shares a metabolic pathway with stress hormones like adrenaline (called catecholamines): they from the same precursor, tyrosine (Nagatsu et al. 1964).
So it is no coincidence that many domestic animal species have depigmented patches of fur: think of border collies with their white ruff and white feet. Think of blazed horses with white socks, black and white holstein dairy cows, white-faced hereford cattle. Domestic animals with piebald coats are extremely common. This depigmentation may not be an accident, but may be a byproduct of selection for tameness.
Belyaev's silver foxes: The most famous example of a connection between depigmentation and docility is Belyaev's foxes (Belyaev and Trut 1975, Belyaev 1978, Trut 1999). Belyaev brought wild silver foxes into captivity and bred them specifically for tame behavior. Experimenters tested the animals' temperaments by reaching into the cages of young foxes and trying to touch them, stroke them, and give them food. Foxes were also placed in a large enclosure with a human. The most docile foxes were retained for breeding, foxes that reacted with more fear and aggression were not bred.
The experiment lasted for over forty years and tested more than ten thousand foxes. The results were striking. Through this process of breeding exclusively for tameness, Belyaev obtained foxes that eagerly approached humans and licked their hands and faces. These foxes even tried to attract human attention by whining and wagging their tails.
But these behavioral differences weren't the only changes that Belyaev obtained in his tame foxes. These foxes also differed morphologically and physiologically from their wild counterparts. The tame foxes had floppy ears, curly tails, and domed skulls. The females went into heat twice a year (like domestic dogs) instead of once a year (like wild foxes). And instead of having a solid silvery black coat, many had patches of depigmented, white fur. The percentage of foxes with white patches went up from 0.71% to 12.4% of the population, an increase of 1646% over forty years (Trut 1999).
What happened? By selecting for tamability, Belyaev selected for physiological changes in the systems that govern the body's hormones and neurochemicals. Those changes had far-reaching effects on the animals' behavior and development, and ultimately on their morphology and physiology.
Trut's rats: Belyaev's fox breeding experiments were repeated in wild Norway rats (Trut 1997), with same result. After 15 years of selection for tameness (over 30 generations of rats) in a captive colony, the percentage of piebald rats (berkshire and hooded) increased rapidly until about 73% had white bellies. The white belly-patches of these rats were large, sometimes spreading to the sides. About half of the piebald rats had white socks too. Over time, solid-colored rats disappeared almost entirely from the population.
In a control population of wild rats bred for 15 years and not selected for tameness, a few piebald rats appeared but they never comprised more than 10% of the population. The white patches of these unselected piebald rats remained very small (a small white spot on the belly or chest) and none of the rats had white socks.
Therefore, in this experiment, selection of Norway rats for tameness correlated with their depigmentation. The population selected for tameness had a much higher percentage of depigmented animals than a similar group that was not selected for tameness.
Note that while moderate depigmentation tends to correlate with calmness, extreme depigmentation can correlate with neurological problems (Grandin 1998), as well as vision and hearing impairments. Here's more information on mutations in pigment cell migration.
Agouti is a common wild type color that consists of alternating bands of light and dark pigment on the hairs. Agouti animals have a little molecule that switches pigment production between light and dark pigments on a single hair as it grows, creating bands. Nonagouti animals lack this little molecule, so their hair is completely dark. Nonagouti animals tend to be solid black.
This little molecule, called the "agouti protein," is also found in the brain, where it blocks neurochemicals known to have potent effects on behavior and physiology. Agouti animals have different neural profiles of neurotransmitters involved in stress (catecholamines) and larger adrenal glands (which produce stress hormones) than nonagouti animals.
A relationship between nonagouti (black) coloration and docility has been shown in foxes, rats, and deermice. In foxes, Keeler found that the most fearful foxes were the wild-type reds, which carry the dominant agouti allele. The less fearful silvers, pearls, and ambers were all homozygous for nonagouti (Keeler 1970). The size of the adrenal glands of these different-colored foxes correlated with their fearfulness (Keeler et al. 1968).
In rats, Keeler (1942) and Cottle and Price (1987) compared the behavior of black and agouti rats that were descended from recent wild ancestors. The rats used by Keeler (1942) were third-generation descendants of a cross between a wild agouti male and domestic albino females. Cottle and Price's rats were the sixth generation descendants of wild rats who were heterozygous for agouti and nonagouti. All the rats within a study therefore had a similar genetic background and had been raised in similar conditions.
Both studies found that the black rats were more docile than the agoutis. More agouti rats than black rats bit, attacked and squealed during handling tests, and the agoutis' responses were more intense than those of black rats. Black rats were more catchable, strokeable, and handleable than agouti rats.
The same results were obtained in agouti and black deermice that had been bred in the laboratory for over 20 generations (Hayssen 1997). In handling tests, more agouti deermice bit and attacked the experimenter than black deermice. Black deermice were also easier to catch, stroke and handle than agouti deermice.
The link between coat color and temperament stems from a relationship between pigment production, hormone chemistry, and neurochemistry. Selecting for behavior can change hormonal status as well as the timeline of development.
This biological relationship between temperament and coat color may therefore be one of the historical reasons that black and piebald colorations are so much more common in domestic animals than in their wild counterparts.
• New York Times article: Nice rats, nasty rats, maybe it's all in the genes.