The Mechanism of Winter Whitening

In the Far North

At landscape scale, there is a general relationship between cold winters and snow cover—the further north the latitude or the higher the elevation is, the greater the chances are that a regular covering of snow every winter can be expected. Likewise, there is also a general connection between whitening in the landscape and in weasels. In cold climates the autumn temperatures plunge quickly, and all northern weasels always turn entirely white.

The processes setting off the autumn molt, initiated by the shortening days, are the same everywhere, but the processes controlling the growth of the new hair are different in weasels living in mild compared with cold climates. The follicles can produce brown hair only if they contain melanin, which they cannot have unless the melanocytes (small cellular factories in the skin) have first been told to make it by MSH (melanocyte-stimulating hormone). In warm-climate weasels, the MSH is produced on cue by the pituitary, the follicles respond to it, and the new winter hair grows out brown. But in cold-climate weasels, an inhibitor either prevents the pituitary from producing MSH, or prevents the follicles from responding to it. The effect is to turn off the supply of MSH and of melanin, and the new hair grows out white (Rust & Meyer 1969) (Figure 3.5).

On the other hand, the winter climate alone does not provide a complete explanation of the control of winter whitening. Early evidence for why it does not came from transplant experiments across the transition zone between all-

Melanin Mechanism

Figure 3.5 The annual molt cycle and winter whitening in North American longtails. In northern populations, the production of melanin in autumn is inhibited, so the winter fur grows white. In southern populations, the inhibition of MSH is switched off, so melanin is produced and the winter hairs grow brown. The rest of the cycle is the same in all populations. (Redrawn from Feder 1990.)

Figure 3.5 The annual molt cycle and winter whitening in North American longtails. In northern populations, the production of melanin in autumn is inhibited, so the winter fur grows white. In southern populations, the inhibition of MSH is switched off, so melanin is produced and the winter hairs grow brown. The rest of the cycle is the same in all populations. (Redrawn from Feder 1990.)

white and all-brown winter fashions. If temperature or some other purely environmental condition were the sole controlling agent, then weasels born on one side of the dividing zone and transferred to the other side should change to white or not according to the custom in their new home, but they do not.

In the summers of 1936 and 1937, a male and two female long-tailed weasels, captured on the warm, snow-free coast of California, were transported east along the latitude lines to Lake Tahoe, high up in the cold and snowy Sierra Nevada; in the other direction, a female from Lake Tahoe and a male from Salt Lake City, Utah, were moved from snowy environments to the mild Mediterranean climate of Berkeley, California (Hall 1951). All the animals were kept in outdoor cages with wire mesh sides open to the elements; all were exposed to about the same day length as at home; all molted at the usual time—but into the "wrong" winter coat. Those from east of the line turned white even in California where all weasels wear brown in winter; and those from west of the line stayed brown even in the mountains, where all the residents turn white. Two wild-caught longtails from northern climes kept in heated quarters at a constant temperature of 18°C to 24°C still turned snowy white in October-November and back to brown in March-April (Noback 1935; R.A. Powell, unpubl.). In all these cases, the animals remained at about their usual latitude.

So heredity, as well as winter climate, must be involved in the control of winter whitening. The weasel populations of a local locality must be adapted to the expected conditions of their homeland. Where it is always very snowy or always very mild it is easy to predict whether a white coat will be needed or not; there is no need for any individual to make a decision. This proposition was confirmed by Feder (1990) in a series of elegant experiments on eight captive stoats kept on short-day photoperiod at the University of Fairbanks, Alaska. Two stoats from Alaska and two from Oregon were kept warm (18°C to 20°C), and two from each place were kept cold (below zero). All four Alaskan stoats molted to white, and all four Oregon stoats molted to brown, regardless of temperature.

At one stage it seemed that a second argument for some degree of genetic control could be deduced from the fact that, in all temperate countries where not all individuals turn white automatically, those that do are significantly more often females. Hutchinson and Parker (1978) pointed out that a correlation between sex and tendency to turn white would necessarily follow if the gene controlling winter whitening is sex linked—that is, dominant in one sex and recessive in the other. The advantage of this arrangement would be that it is an efficient way of maintaining a genetic polymorphism, a constant readiness to meet sudden changes in the characters favored by natural selection in present conditions. With respect to winter whitening, those animals that stay brown in a mild winter are best adapted, whereas those that turn white in the occasional exceptionally long snowy winter are the lucky ones. A stable, sex-linked genetic polymorphism ensures that the population always includes a few individuals with every combination, every winter, so some will always benefit whatever happens.

The problem with this idea is that the mechanism controlling the molt cycle involves prolactin, which also plays a very important part in the reproductive cycle of females. It would take a very careful, critical experiment to disentangle the different roles played by prolactin in the control of winter whitening and reproduction in the two sexes, and that has not, so far, been done.

In the Transition Zones

Not all weasel populations are so predictable in their winter dress as are those of Alaska and Oregon. As Figure 3.4 shows, there seems to be a "zone of indecision" where winter climates are quite unpredictable and where it might be an advantage to have some sort of temperature switch, enabling a given animal to decide one way or the other—to turn white this year or not. Within this zone, white or brown animals may be found in different proportions apparently varying with location and temperature.

In the transition zone, the results of translocation experiments appear unpredictable. For example, in 1953 Rothschild and Lane (1957) caught a young stoat in the Swiss Alps and brought it home to England, about 5° of latitude further north. In September, the transplanted animal turned pure white, despite the mild autumn and the established custom of locally resident stoats to stay brown. In contrast, Roger and Consie Powell brought two stoats already in their white winter coats to North Carolina from Minnesota in winter (10° of latitude further south). After a summer in brown, they did not turn white in the following winter, and neither did the female's offspring, born in North Carolina.

The idea that individuals might have a "choice" of whether to turn white or not is a completely different proposition from the idea of genetic adaptation to expected climate at the population level. It implies there could be provision for some level of response to weather, rather than climate, and at the level of the individual rather than the population. How could this happen?

One early study that seemed to suggest a possible mechanism was that of Gaiduk (1977). Gaiduk calculated that in Belorussia, where he worked, the fur of the hindquarters and lower flanks of stoats would grow white if the temperature at the time was 2°C, but it had to be below -1°C before the head and back would turn white. Even though all stoats in Belorussia normally turn white every year, Gaiduk's results implied that there could be a minimum critical temperature below which new fur grows only white, which is different for different parts of the body. In milder regions the critical temperatures required for whitening could be different, probably higher, and the autumn weather more variable, so that the threshold might be exceeded for one part of the body but not for another. If true, this arrangement could amount to a "switch" that could control the supply of melanin with short-term changes in the weather. For a given individual animal, the switch could be "off" while the new fur grew on the tail and sides, but by the time the new dorsal fur was growing, it could be "on" again.

The result would be that the animal would appear to be "pied" (Figure 3.6), and in places where the weather conditions in autumn are very variable, one might observe a mixture of white, brown, and pied individuals in different proportions each winter. These animals would look as if they were caught in the middle of molting. An alternative explanation could be that they were wearing a full-grown winter coat in which the switch had turned off the supply of melanin before the cycle of hair growth was complete. If so, the proportion of pied stoats should be correlated with local and annual variation in winter temperature.

The trouble is that Gaiduk's intriguing conclusion includes a hidden assumption, that low temperatures predict the snow cover against which white coats

Figure 3.6 Pied stoats appear to have been caught halfway through molting, but are more likely to be heterozygous for the alleles that control whitening of the winter fur.

would be an advantage, which is not always true. Moreover, it was based on simple observations, not on manipulative experiments. Where such experiments have been done, using captive animals from populations that always reliably turned white or stayed brown, temperature did not control whether stoats turned white or not (Feder 1990).

We suggest another explanation. If winter whitening is controlled by a poly-genetic system, then all individuals must have the genes that determine the response of the follicles to MSH in autumn. The difference between well-adapted populations in the far north and far south is that, in each, only the genes for either white or brown in winter would be expressed. The "transition zones" could represent, not places where individuals can exercise an option, but places where different proportions of individuals have different genetic origins, including hybrids. The "transition zones" could mark the places where postglacial recoloni-zation of the northern lands (Chapter 1) has brought populations of winter-brown weasels from snow-free southern refugia into contact with populations of winter-white weasels from snowy northern refugia. The contact zone is narrow and well defined where least and common weasels meet in Scandinavia and where stoats of different origins meet in northwestern North America, but is wider and more diffuse in other temperate populations of stoats living in variable climates.

If this hypothesis is correct, then there is no need to postulate a temperature "switch." Extensive hybridization between these different stocks, plus natural selection acting on the results to produce locally adapted resident populations, would be sufficient to produce the patterns we see. For example, it would be reasonable to suppose that more of the stoats that have lived in cool northeast Scotland since soon after the ice ages might have retained their adaptation to colder periods in the past, including expression of genes for winter whitening, than stoats in the milder climate of England. Indeed, in northeast Scotland at 57°N, over 90% of stoats of both sexes seen by Hewson and Watson (1979) in each January from 1969 to 1974 had changed color, of which most were in full ermine.

By contrast, most English stoats stay brown. An inquiry conducted by questionnaire in 1931-32 in Yorkshire (54°N) found that, of2,930 stoats killed, only 21 were in full ermine (all females) and another 175 (85 females, 90 males) were pied. Ninety percent of the informants had never seen a fully white stoat, and 40% had never seen a pied one (Flintoff 1933, 1935).

Likewise, very few stoats collected over 4 years by King and Moody (1982) in Fiordland, in the cool far south of New Zealand, during the months between the end of the autumn molt and the beginning of the spring molt (June to November), were white. In one area at 44°S to 45°S, only 71% of the 34 females collected and 47% of the 62 males collected had any white hairs at all. Of 124 females and 305 males collected from the whole country during those months, only eight were in almost full ermine, and even they still had a few brown hairs remaining around the eyes. Most were pied, at best, and many had only a few white hairs just in front of the black tail tip.

King and Moody (1982) compared the proportions of white or pied stoats collected in 14 samples taken in the southern winter and spring months of June to November with the local weather records. The results were consistent with the idea of local adaptation linked to temperature. The variation among samples in the proportion of pied stoats was significantly correlated, both with the mean daily minimum temperature in July (the coldest month) and with the number of days of ground frost per year. Further, white and pied stoats were more common at higher elevations and more southerly latitudes, although, even there, the vast majority of stoats stayed entirely or mostly brown.

Stoats from the cool end of Britain (the far north) turned white more consistently than those from the cool end of New Zealand (the far south) even though they were not exposed to a much colder or snowier climate than the New Zealand ones sampled in these studies. In both areas, the minimum temperature for the coldest month is usually within 5°C either way from zero, and in both, snow seldom lies more than 10 to 20 days in any winter. In this and other respects, the New Zealand stoats are more like English than Scottish ones. New Zealand stoats are probably descended from English (non-whitening) stock, and they have lived in New Zealand for only about 120 generations. In those that have spread into the coolest parts of their new homeland, natural selection might still be in the process of retrieving their lost or latent genes for whitening. These observations make sense if heredity, rather than temperature, controls what color of winter coat is worn by individuals.

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