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SOME ideas just won鈥檛 go away. They may seem dotty, yet all the evidence
suggests they are right. Even so, those who dare to have their name associated
with such ideas risk being branded as cranks or intellectual misfits.

One such notion is metachromism. According to this theory, many of the
colours of monkeys and other mammals are not for camouflage, communication or to
help the animals survive in any way. Instead, they are simply the consequence of
a predictable sequence of colour changes through evolutionary time. No wonder
most biologists object. This is pure biochemical determinism, and flies in the
face of Darwinian ideas about adaptation.

Metachromism would probably have faded into obscurity had it been proposed by
some minor figure. But it wasn鈥檛. It was the brainchild of a renowned
mammalogist, Philip Hershkovitz of the Chicago Field Museum. When he died in
1997, at the age of 87, one obituarist described him as the last person who knew
everything about neotropical mammals. His papers and books on the evolutionary
history and taxonomy of South American monkeys and marmosets remain the basis
for much of the currently accepted classification of the continent鈥檚 primates.
Yet the theory of metachromism, which was central to his analysis, was deemed so
wacky that most researchers have politely ignored it. Now evidence is emerging
that the old master may have been right all along.

Most mammalian hair colours are due to the pigment melanin. It comes in two
basic types: eumelanin and phaeomelanin. Hairs containing eumelanin look black
or brown, depending on the concentration of pigment granules, while those with
phaeomelanin can be various shades of red or yellow.

According to Hershkovitz, the most primitive coloration for mammalian hair is
the agouti pattern, where individual hairs have alternating bands of eumelanin
and phaeomelanin within their hollow cores. He suggested that the hairs on some
part of the body鈥攖he base of the tail, say鈥攎ight then become
saturated with just one type of melanin, and that once this occurs, a
鈥渕etachromic progression鈥� begins. Over many generations, the amount of melanin
in each hair diminishes, giving a distinctive sequence of colour changes. For
areas saturated with eumelanin, the progression is from black to brown to drab
to grey. For phaeomelanin, the sequence is red to orange to yellow to cream.
Both pathways end in white, when the hairs contain no pigment.

Path of no return

This process, which Hershkovitz called bleaching, is a one-way street. Once
the ability to produce a colour is lost, it cannot be regained. Hershkovitz
based his family trees of modern Amazonian monkeys and marmosets on this
progression. An ancestral species would always be the one further back up the
metachromic sequence, so an all-agouti species would, he considered, be
ancestral to one with black, red or white patches of fur.

鈥淗ershkovitz鈥檚 theory smacks strongly of `orthogenesis鈥�, an idea popular
around the turn of this century and ultimately rejected in the 1920s,鈥� says
Allan Larson from Washington University. Orthogenesis was an alternative to
Darwinian natural selection, which found favour in the US and Germany,
especially among palaeontologists and developmental biologists. The idea was
that organisms were propelled along a predetermined evolutionary pathway by an
unexplained, near-mystical internal force.

The paradox is that, although Hershkovitz鈥檚 thinking seemed anachronistic,
his findings appear to stand the test of time. For example, in 1997, Susan Cropp
Jacobs decided to test Hershkovitz鈥檚 classification of marmosets in the genus
Saguinus, a group central to his theory. 鈥淭hese little primates show an
amazing variety of coat colours,鈥� says Jacobs, who is now at the University of
Chicago. Working with Larson and James Cheverud, she isolated and analysed
mitochondrial DNA from 13 species and subspecies of Saguinus and drew
up a family tree based on the differences. She then compared it with one based
on coat colours and the metachromic theory. The match was almost perfect. 鈥淚
couldn鈥檛 believe it,鈥� she says. 鈥淚 was so sure we were going to scuttle
尘别迟补肠丑谤辞尘颈蝉尘.鈥�

Other independent studies have also found that metachromism seems to work.
Researchers at Duke University have successfully applied metachromic analysis to
the several groups of lemurs. The theory can also reveal evolutionary
relationships in squirrels, tree kangaroos and cuscus marsupials. And Lars
Werdelin of the Swedish Museum of Natural History has proposed a similar process
for the evolution of coat colour in big cats.

Even so, Jacobs is not a convert. 鈥淚 still don鈥檛 believe it is a valid
mechanism,鈥� she says. 鈥淢etachromism is, I think, the outcome of some other
effect we have yet to recognise.鈥� Cheverud agrees that metachromism as
Hershkovitz proposed just doesn鈥檛 seem tenable. 鈥淭here is certainly a phenomenon
requiring an explanation, but I doubt that metachromism provides it,鈥� he
says.

But one researcher is convinced that, with a little modification,
metachromism has a place in mainstream biology. Douglas Brandon-Jones of the
Natural History Museum in London also set out to prove the idea wrong, but after
spending more than 20 years studying Asian colobine monkeys he has changed his
mind. 鈥淔ar from proving Hershkovitz wrong, I鈥檝e found that they fitted the
concept amazingly well.鈥�

Like Hershkovitz, Brandon-Jones believes that colour changes don鈥檛
necessarily evolve to increase an animal鈥檚 chances of survival. He, too, has
identified a bleaching process, although he believes that agouti is a rather
complex pigmentation. Brandon-Jones鈥檚 chromatic progressions runs from black,
through grey to brown and in some cases onward through red, orange and yellow to
white.

His version of metachromism is also less deterministic than the original.
鈥淗ershkovitz looked at metachromism in a rather finite, inflexible manner,鈥� he
says, 鈥渨hile I regard it as a very dynamic short-term process. And I don鈥檛
believe it is resolutely leading all mammals to a irreversibly white-furred
蹿耻迟耻谤别.鈥�

Islands of change

Brandon-Jones鈥檚 idea is based on the Pleistocene refuge hypothesis of
rainforest speciation, which suggests that during times when the climate was
cool and dry, rainforests contracted, leaving islands in which isolated
populations of wide-ranging species were stranded. These separate groups
then evolved into today鈥檚 species鈥攐r so the theory goes. But according to
Brandon-Jones, speciation occurred not during glacial isolation, but afterwards,
as animals dispersed as the climate grew wetter. He proposes that dispersal,
colour change and speciation are inextricably linked.

鈥淎s the forest expands, some of the primate population act as nuclei for the
subsequent interglacial diaspora,鈥� says Brandon-Jones. 鈥淓ach is then surrounded
by a new set of derived subspecies. Eventually, these may form full species.鈥� He
noticed that a sequence of colour changes seems to radiate out from these
nuclei, like ripples in a pond. 鈥淲hen you look at distributions of species and
subspecies and match them and their colour patterns to glacial refugia, the
process of colour change looks a lot like chromatography, with differing colours
migrating different distances.鈥�

But what triggers the changes in colour? Brandon-Jones believes the process
is, in some way, a consequence of migration from one place to another. 鈥淚t takes
time for a forest to be suitable to these leaf-eating monkeys,鈥� he says.
鈥淥nce it is, I believe colonisation would be rapid indeed, and here鈥檚 where
metachromism comes in. A consequence of the population movement is an abrupt
change in colour of the newly established population relative to its parent
population.鈥� This fits with his findings that colour change seems to occur in
pulses over time, correlated with phases of forest regeneration.

Brandon-Jones also believes that during interglacials, some reversal of the
process might occur, eliminating most of the brown, red and white populations.
鈥淚n the long term,鈥� he says, 鈥渕etachromism might be cyclical.鈥�

Metachromic theory has allowed Brandon-Jones to tease apart some very complex
taxonomic problems. One key discovery was that the Southeast Asian leaf monkeys,
Presbytis, and their relatives the brow-ridged langurs,
Trachypithecus, are both undergoing the bleaching process described by
Hershkovitz. What鈥檚 more, the pattern can be seen again and again around various
areas where forests are known to have hung on during the last glaciation. 鈥淚t
was these isolated repeating patterns that caused much of the previous
confusion,鈥� says Brandon-Jones. But these were just the sort of ripples in a
pond that his theory predicted.

The analysis has allowed him to trace the history of Presbytis back
190 000 years, and in so doing, turn old notions on their head. 鈥淚 found that
the species ancestral to all others was the black sureli, which lives on the
Mentawais鈥攆our tiny islands off Sumatra.鈥� Brandon-Jones is convinced that
the black sureli鈥攖raditionally regarded as an isolated oddity鈥攐nce
spread from these islands to Java, Borneo and the Malay Peninsula. It then
evolved into three of today鈥檚 Presbytis species. Each has subspecies,
and these show remarkable parallelism in their coat colour patterns.
鈥淢etachromism provides the best explanation for their distribution,鈥� he
says.

Brandon-Jones鈥檚 studies are giving metachromism a new air of respectability.
He has published his findings in the Biological Journal of the Linnean
Society and other prestigious journals. His revised plan for the
interrelationships of Southeast Asian leaf monkeys has been used in parts of the
mammalogists鈥� bible Walker鈥檚 Mammals of the World. And his ideas
underpin the species arrangement in Conservation International鈥檚 next field
guide to Asian primates. 鈥淚t really does seem like he鈥檚 onto something,鈥� says
Stephen Nash of Conservation International, who is illustrating the guide and
who knew Hershkovitz. But even enthusiasts such as Nash admit that the theory is
incomplete. 鈥淚t鈥檚 the absence of a verifiable mechanism that seems to be
something of a sticking point,鈥� he says.

A partial explanation for metachromic colour progressions may come from
studies of colour inheritance in animals as diverse as cows, fruit flies,
chinchillas and koi. At Washington University, Cheverud has made a literature
survey of mutations in colour-coding genes. 鈥淭here were recorded instances that
went against the run of Hershkovitz鈥檚 proposal,鈥� he says. In cows, for example,
a mutation of a single base pair of the melanocortin-1-receptor gene, will
result in red parents having black offspring. 鈥淏ut, such situations were less
common than those that agreed,鈥� says Cheverud. 鈥淚t seems mutations are more
likely to result in bleaching.鈥�

So what lies behind this predictable sequence of colour changes? 鈥淢ouse coat
colour involves over 40 genes, and it is likely that this is also true for other
mammals,鈥� says Nick Mundy of the University of Oxford. With this in mind,
Cheverud suggests it could simply be that there are more genes that cause one
kind of chromatic shift than another. 鈥淚nteractions among genes could also cause
this. It鈥檚 very complex,鈥� he says. 鈥淔or example, colour changes can result from
mutations in genes controlling the size and number of melanin granules as well
as their type. It鈥檚 a field that needs a lot more work. But there does seem to
be a directionality to bleaching.鈥�

Convincing the sceptics

Larson agrees. 鈥淏ased on the biochemistry of how the pigmentation is
produced, it is perhaps more likely that certain kinds of mutation will knock
out certain pigments and produce variation that looks like Hershkovitz鈥檚
bleaching process,鈥� he says. He accepts that coat-colour variation may not be
produced at random.

Even so, many researchers remain unconvinced. 鈥淚 just can鈥檛 see it,鈥� says
Caroline Ross, a primatologist at the Roehampton Institute in London. 鈥淚f
metachromism is so immutable, how come the world isn鈥檛 knee-deep in white-coated
mammals?鈥� It is an objection that Brandon-Jones encounters often.

鈥淗ershkovitz was, in many ways, his own worst enemy,鈥� he says. 鈥淗is
insistence that all animals are progressing relentlessly to an albinistic future
was probably enough to put most people off 尘别迟补肠丑谤辞尘颈蝉尘.鈥� But, he points out,
even Hershkovitz admitted that in some types of animal, selective pressures for
colours that enhance survival would take precedence over the non-adaptive
metachromic progression. One of his favourite examples of this was a North
American mouse, Peromyscus. The coat colour of some populations
precisely matches the soil colour where they live.

Brandon-Jones鈥檚 version of the theory is more flexible. True, it may have
lost some of its predictive power, with the assertion that monkeys can revert
back to colours that occur earlier in the sequence. But in some ways, the new
metachromism is even bolder than the original idea. Not content to stop at
monkeys, Brandon-Jones believes that many other animals also have metachromic
progressions, with distinct colour sequences with no adaptive advantage
appearing over time. 鈥淚鈥檝e opened things up a bit,鈥� he says. 鈥淚t鈥檚 time to pass
the baton on to the geneticists.鈥�