4.3 Phenotypic changes that appeared without being selected
As well as these behavioural changes, many of the selected foxes had unusual white markings (Figures 13c and d). The first colour change that the Russian investigators noted in their foxes was a white ‘star’ on the forehead similar to that of other domesticated mammals (Figure 14a), which enlarged in later generations to form a blaze (Figure 13c and d). Both these patterns are very common in domesticated horses (Figures 14a and b) and cattle (Figure 14d), but absent from their wild ancestors (Figure 5c and d). Many of the tamest foxes were piebald or skewbald (as in other species, Figures 3a, c and d, 7, 14c and d), had floppy ears (similar to those of the animals in Figures 2, 3b and d, 8a, c and d, 12a, c and f) and longer, silkier fur (as in certain dogs, Figures 8c and 12f). After more than 40 years of selective breeding, the coat patterns of some of the foxes (Figure 13d) were remarkably like those of collie dogs (Figure 8b). None of these features of the coat or ears were deliberately selected for; they were the accidental consequences of selection for tameness and tameness alone.
More detailed study of some of the early fox fetuses revealed that the pigment-forming cells migrate to the skin two days later in the tame foxes than in unselected wild-types, and a much higher proportion of the cells die.
Would this mechanism produce a piebald coat?
Yes. Patches of fetal skin that were successfully invaded by pigment-forming cells would produce dark hair, while those with few or no pigment-forming cells would produce lighter hair, or white hair.
Dermal cells that form pigments are derived in the developing embryo from an important and diverse group of embryonic cells called the neural crest. If these cells fail to migrate to an area of skin, do not mature properly or die in the fetus, that area of skin and all the dermal structures derived from it, such as hair and feathers, lack the correct pigment in the adult.
In an attempt to identify the molecular and cellular bases for these changes under domestication, the breeders also measured some anatomical features of the brains and assayed corticosteroid hormones from blood samples. (Techniques for measuring these hormones and knowledge of their structural and functional diversity have improved greatly since this research began in the 1960s. The family of signal molecules includes glucocorticoids (e.g. cortisol), corticotropins and several more.) Levels of these hormones rise within seconds of acute episodes of pain or fear and the background levels are also higher in animals (and people) that are subject to chronic stress or anxiety. After 12 generations of artificial selection, the average levels of these hormones were down at half those of the control population, and to only a quarter by the 30th generation.
What are the problems for interpreting these observations on a population of wild animals kept under confined conditions in captivity?
Hormone levels could be unnaturally high in unselected foxes because of the husbandry conditions. The selection regime could be just favouring those foxes that maintain normal levels of hormones in spite of the conditions. However, all wild animals, particularly predators, experience stress as an integral part of finding food, competing for mates and avoiding danger.
The average total mass of the brain was about 25 per cent less in tamer foxes than in controls. Sex differences in the size and shape of the skull were also reduced, with males becoming feminised. In spite of the smaller size of their brains, rigorous psychological tests showed that ‘domesticated’ fox cubs were better than wild foxes, and as good as dog puppies, at responding appropriately to social cues from people, such as investigating an object that the handler points at. A byproduct of reduction of fearfulness and stress by selective breeding for tameness seems to be improvement in such ‘social intelligence’, though the mechanisms remain to be explored.
The time course of postnatal development also changed. Tamer cubs opened their eyes and showed clear responses to loud sounds an average of two days earlier than the controls. The appearance of obvious fear was delayed: posture and facial expression indicating fear were first detected at an average age of nine weeks in selected foxes, compared to six weeks in the controls.
Other behavioural traits, including barking like domestic dogs, were also noted in far greater frequency in the selected population of foxes. The similarities in behaviour and appearance between dogs and domesticated red foxes are even more impressive in view of the conclusion from the phylogenetic analysis (Lindblad-Toh et al., 2005, see Section 3.1) that these species’ last common ancestor lived at least 10 My ago.
Intense selection for tameness has altered brain chemistry and anatomy and the time course of development, though gene expression seems to be almost unchanged. Researchers at Uppsala University in Sweden compared mRNA expression in three regions of the brains of farmed and wild foxes: of nearly 30 000 genes studied, the expression of only about 40 (0.1 per cent) was altered by selection for tameness (Lindberg et al., 2005).
Can major phenotypic difference accompanied by only minimal genetic change appear naturally?
Yes. An example is plumage colour in bananaquits that arose from a point mutation that alters a single base pair. There are probably many more.
Factors that mediate fear control the action of certain other genes that determine the maturation of other behavioural and anatomical characters. One interpretation is that behaviours such as whining, barking and tail wagging are ‘released’ when fear is reduced. This explanation is indeed inadequate, and not all the changes observed in the selected populations of foxes could be easily explained on this hypothesis. In the first few pages of On the Origin of Species… Darwin noted that ‘colour and constitutional peculiarities go together’, citing the example that ‘Cats with blue eyes are invariably deaf.’ 19th-century knowledge of development, physiology and genetics could not explain these associations, leaving Darwin to describe them as ‘quite whimsical’; understanding these relationships, now termed epigenetics, is one of the triumphs of 21st-century biology.
Other anatomical changes recorded in the tamer foxes also seen in other domesticated mammals were drooping ears (Figures 3b and d and 12a, b, c and f), shorter, upturned tails, shorter snouts (Figure 12d), and differences in the proportions of the head, especially the relative length of the upper and lower jaws (Figure 3b). The range of dog breeds shows that these anatomical characters can occur in many different combinations. The fox experiment suggests how this variation, which humans have developed and exaggerated under artificial selection, may have originated.