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Authors: Chris Smith,Dr Christorpher Smith

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The answer, it turns out, is only skin deep and is made possible by a series of specialised pigment-loaded cells, called chromatophores, which are wired to the animal's brain and are also sensitive to hormones circulating in the bloodstream. These chromatophores behave like
the pixels of a TV screen. They are arranged in layers beneath the chameleon's transparent outer skin. Those in the uppermost layers are referred to as xanthophores and erythrophores, and contain respectively yellow and red pigments including carotenoids, which are the molecules that make carrots look orange.

Deeper down in the skin is a layer of iridophores. These contain a colourless crystalline compound called guanine that reflects blue light. Then, deeper still, is a layer of cells called melanophores. These contain melanin, the same substance that gives humans a suntan. By varying how active they are, the chameleon can trigger the melanophores to soak up more or less light to make itself look lighter or darker. The pigments within the chromatophores are stockpiled as a collection of granules in the cells. When the chameleon wants to change colour, signals from the nervous system, together with chemicals in the blood, activate individual chromatophores and cause the granules to disperse across the cell and change its colour, rather like giving it a coat of paint.

By activating different combinations of chromatophores at the same time, different
colours can be produced. This works in the same way that mixing red and yellow produces orange. So to make itself appear green, a chameleon switches on the yellow in its xanthophores and the blue in its iridophores: blue plus yellow makes green. Or, to make itself appear darker, the animal can activate its melanophores, which allow melanin to spread across the cell and soak up light, turning the chameleon brown. While chameleons may not be masters of disguise, they are certainly makeover masters, at least when it comes to skin redecoration.

In 2009, the world celebrated the 150th anniversary of one of the most famous books ever published, Charles Darwin's
On the Origin of Species
. Darwin's insight, stimulated by the five years he spent as the naturalist aboard HMS
Beagle
, was to recognise the workings of the process of natural selection, the cornerstone upon which the theory of evolution is founded.

During natural selection the favourable characteristics of an organism, such as those which enable it to succeed in a particular environment, become more common in successive generations. This is because a successful organism is much more likely to breed and multiply than a less successful one, so any unfavourable traits are progressively weeded out, while good traits are concentrated within the population. This is the origin of the term ‘survival of the fittest', which was coined in the 1860s by the British economist Herbert Spencer after he read Darwin's book.

Now, though, a new study on wild Scottish deer carried out by Edinburgh University researcher Loeske Kruuk and her colleagues
17
suggests that the concept of ‘survival of the fittest' is something of a myth, or an oversimplification at best. Why? Because scientists had previously overlooked the fact that amongst most animals there are two sexes, and what works well genetically for one sex won't necessarily wash with the other. The researchers made the discovery after several years spent studying the red deer population on the Isle of Rum. During their analysis, the team tested the paternity of the deer using genetic fingerprinting techniques to work out who was related to whom, and then logged how many offspring each animal produced and how many young were then born to those offspring.

What the researchers had expected to see, based on the concept of ‘survival of the fittest', was that the successful males should have successful daughters as well as successful sons. But when the results from both generations were compared, astonishingly, a very different pattern emerged. Far from being a genetic paragon of
fitness, the daughters of the successful males who had fathered large numbers of young (both male and female), tended to be relatively unsuccessful themselves in the deer-dating stakes. On average, these females produced fewer calves overall. The sons of the successful males, on the other hoof, were unaffected.

This, say the scientists, is because the genes that single out a successful stag include those for large stature, impressive antlers and the ability to roar the loudest, none of which are of much use to a female. ‘What we've found is that the genes that make a successful male do not always make a successful female,' says Kruuk. ‘So the idea that some genes are better than others is just too simplistic. Instead it depends on the sex of the individual animal carrying the genes.'

Is the same true for successful females? Do they have wet blankets for sons? ‘It's slightly more complicated when you look at it that way round,' says Kruuk, ‘because females contribute not only their genes to their offspring's later performance, they also provide maternal care. So a good quality female, although she may be passing on genes which are detrimental in a son, will also provide very high-quality maternal care. These
two effects seem to balance one another out.'

Does this leave ‘survival of the fittest' for dead, or even stuck in a ‘rut'? Perhaps not, because the effect seen in the deer has an unexpected spin-off: it contributes to genetic variation, which makes the population fitter as a whole, since a larger gene pool means a better ability to cope with life's challenges further down the track.

Scientists believe that the majority of living things on earth, whether mould, mice or men, use a body (circadian) clock to synchronise their activity to the local environment. In humans, that means we go to sleep when it gets dark and wake up when the sun rises. For nocturnal animals the reverse is true, and many seasonally breeding species track the changing relative lengths of the day and night so they know when in the year to mate. But one thing researchers hadn't bargained for is what happens to animals that live where the sun don't shine – at least for long periods – like the Arctic?

Here, for about six months of the year, the world is plunged into near-continual darkness; for the other six months, the sun never sets. Between the two is an ‘equinox' period when days are about the right length, but any animal that attempted to set its clock by the sun in this environment would be in for a chaotic lifestyle, even by the standards of a city commuter. But there are animals that flourish in these conditions, reindeer among them, so what's happening to
the body clock in these species? Scientists had suggested that animals like reindeer have evolved merely to ignore their clocks (a trait that seems to be shared with teenagers and students), but this turns out to be a myth that's just timed out.

The idea first came to light when researcher Karl-Arne Stokkan
18
began studying wild reindeer living in his native Norway and on Svalbard, a cluster of islands in the Arctic Ocean, further to the north. Together with colleagues, he equipped groups of the animals with movement-sensitive collars called ‘Actiwatches', so he could distinguish when they were moving, and hence awake, from when they were stationary and therefore probably asleep. The results showed that, unlike humans (new parents excluded), reindeer don't sleep through a night but instead have irregular cycles of activity and rest, during which they periodically take a nap. This erratic pattern is maintained regardless of whether it's permanently light or permanently dark, which led the researchers to conclude that the reindeer are more slaves to their stomachs than their body clocks.

According to Stokkan, being ruminants, the animals' activity is driven by their digestive systems, so they feed whenever the weather permits. Also, by dozing only when they feel tired, there's less chance of missing out on a meal, which is a serious consideration when you live in a land where, rather like a school canteen, high-quality calories can be hard to come by.

The big mystery, though, is how the animals are ignoring their body clocks like this. Originally the researchers thought that, by some behavioural trick, they were able to put the clock mechanism into idle when it suited them. But now circadian scientist Andrew Louden from Manchester University
19
thinks that, for this species at least, the hands have fallen off their biochemical clocks altogether. He and his colleagues took blood samples from reindeer as they were being exposed to artificial short cycles of light and darkness, each lasting two and a half hours. What they saw was that every time the lights went out the levels of one clock-linked chemical, called melatonin, shot up. Normally, melatonin won't change like this if the body clock believes that it's the wrong
time of day. So the fact that the levels altered in this way suggests that, unlike people doing a boring job, reindeer aren't clock watchers.

To prove the point, the Manchester scientists grew reindeer cells in the culture dish and added DNA from a jellyfish to make the cells glow whenever two of the genes known to power the mammalian body clock became active. Compared with mouse cells, where the genes turned on and off sequentially – like clockwork, you could say – the reindeer cells, unlike Rudolph's nose, refused to light up. This suggests that, for these animals, the body clock has evolved not to tick anymore.

So do they live in a world devoid of a concept of time, destined to be eternally immune to jet lag? The answer is, in terms of day-to-day time, probably yes, but scientists are now discovering that these animals have a far more intriguing hold on long-term timekeeping. According to Louden, ‘If you asked a reindeer the time of day – assuming it could speak of course – it probably wouldn't have a clue. But if you asked it the date – in other words, the time of year – they'd probably be able to tell you with extremely high accuracy.' And that's because Louden and his colleagues have found that reindeer seem to have substituted
a yearly ‘circannual' clock for a daily one. They don't understand in detail how it works, but it seems to involve activating certain patterns of genes in a specialised region of the brain's hypothalamus, which has evolved specifically for this purpose in these animals. This is what enables them to get their migration and mating timetables spot on.

Most importantly, this research answers one of the enduring questions of our time – how reindeer know it's Christmas, and how they cope with staying up all night to keep Santa on schedule …

FACT BOX

Body clock

In mammals (other than reindeer) the body clock is based in a specialist region of the brain's hypothalamus called the suprachiasmatic nucleus. This is a small rice-grain-sized cluster of about 20,000 interconnected nerve cells resembling a miniature pine cone. It sits directly above the optic chiasm, the route
through which visual information from the eyes is relayed to the brain. A nerve branch from the chiasm feeds information about light exposure from the retina into the clock cells to keep them ticking to time and to reset the system when the clock gets confused by jet lag.

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