麻豆传媒

A FEMALE barn swallow patrols the skies, searching for a mate. She鈥檚 picky
and isn鈥檛 going to settle for just any male. Suddenly, she notices a brilliant
flash of colour鈥攁 proudly parading suitor. She is instantly drawn to him.
With that stunning red throat pouch, she just can鈥檛 resist him.

It seems that the brashest, most brightly coloured males always get the
girls. A flashy yellow wing tip or radiant red tail feathers are sure to attract
attention. And it鈥檚 not just birds who dress to impress. Throughout the animal
kingdom, there are males who show off through their wardrobe.

There can be no doubt that colours are status symbols, but what exactly do
they symbolise? And why do females fall for them? After all, a patch of red is
not going to help a male cope with life鈥檚 essentials, such as catching food. On
the contrary, bright colours attract predators as well as partners, making them
a disadvantage in the battle for survival.

This conundrum has been bothering evolutionary biologists since Darwin鈥檚
time. Now they are beginning to lift the lid on this enigma. The key, it seems,
is understanding the high price of putting on such colourful displays.

It鈥檚 130 years since Darwin coined the term sexual selection to describe the
central role that sex plays in evolution. Sexual selection works in one of two
ways. Either males compete with one another for potential mates, with the winner
taking the spoils, or females take the initiative and choose their partner.
Where males compete directly, it is usually easy to see how sexual signals work.
Large antlers on a stag, for example, not only warn rivals that he is no Bambi;
they can also be used as weapons. But the dandy yellow suits worn by canaries or
yellowhammers aren鈥檛 as handy in a scrap.

Over the past century or so, it has become increasingly clear that most bird
species鈥攁nd many other animals, including fish, reptiles and
mammals鈥攗se the second strategy. Those that do are among the most
strikingly coloured animals alive. But biologists have struggled to understand
exactly how bright colours signal a male鈥檚 worth. Explanations haven鈥檛 got much
further than the Darwinian notion that impressively adorned males must be the
fittest of their kind, capable of investing more energy in their sexual signals
than their rivals.

Such fumblings are underpinned by some important theory, though. For a start,
a signal between individuals usually contains reliable information about the
sender. Otherwise, like the boy who cried wolf, it will soon be ignored and
become meaningless. For a signal to be reliable, or honest, it is essential that
it cannot be faked by scrawny males.

Amotz Zahavi of Tel Aviv University realised that an honest signal must be
costly to produce and called this the handicap principle. In other words, the
cost of producing a signal will be too high for low-quality males鈥攋ust as
forking out for a flashy sports car will hit the pocket of someone with a low
income much harder than that of a millionaire鈥攅nsuring that only the best
males can invest in bright signals.

But just what do we mean when we talk of low-quality or high-quality males?
In 1982, evolutionary biologists William Hamilton and Marlene Zuk proposed a new
handicap hypothesis that forged a link between the quality of individuals and
their sexual signals. They argued that disease resistance is crucial in the
evolution of sexually selected characteristics. In essence, only males with
genes for, say, parasite resistance would be in prime condition and thus able to
express the best sexual signals. The flip side of the theory is that sick males
will look drab in comparison with healthier rivals. 鈥淚 think Hamilton and Zuk
deserve a lot of credit for having started this,鈥� says Anders M酶ller of the
Pierre and Marie Curie University in Paris.

Hamilton and Zuk鈥檚 idea sparked a rush to find evidence to back the theory.
鈥淚t鈥檚 a damn difficult idea to test,鈥� says Ian Owens of the University of
Queensland in Brisbane, Australia. And what followed was a mishmash of equivocal
results. Early evidence showing a relationship between levels of parasites in
the blood and plumage brightness turned out to be biased, because the assessment
of colour intensity was subjective and did not take into account the fact that
birds and humans have very different colour vision. Once colour scoring was
standardised, the correlation seemed to disappear. More recently, conflicting
evidence has come from studies of birds, fishes and lizards that looked at the
levels of blood parasites or more general measures of immune function, such as
the concentration of white blood cells, or the size of the spleen or other
immune organs.

To find a way through the confusion, M酶ller and his colleagues Philippe
Christie and Elena Lux used a statistical technique known as meta-analysis to
merge the results of around 50 studies. These yielded 69 separate comparisons of
relationships between the expression of secondary sexual characters such as
colour and either parasite load or immune response. Last year, they reported
that parasite load is not strongly linked to the expression of sexual signals.
But immune function is.

鈥淢ost of the early tests of the Hamilton-Zuk hypothesis based on parasite
data are pure misunderstandings, because they do not address the question of
resistance to debilitating parasites,鈥� says M酶ller. Animals are often affected
by a range of parasites. But because most of the experiments focused on single
parasites, it is likely that they were looking at relatively harmless organisms,
M酶ller says. 鈥淲hat Hamilton and Zuk were really talking about is resistance, and
using parasite abundance as a measure is an extremely indirect way of addressing
the question. Rather than looking at parasites we should look at immune defence
尘别肠丑补苍颈蝉尘蝉.鈥�

But how could immunity be linked to sexual signals such as colour? One idea,
proposed in the early 1990s by Ivar Folstad of the University of Troms酶 in
Norway and his colleague Andrew Karter, suggested that the key was testosterone.
In many vertebrates, the hormone is essential for the full expression of male
sexual characteristics, but it also suppresses the immune system. Folstad and
Karter described testosterone as a double-edged sword. Their immunocompetence
handicap theory predicted that only males with the best immune systems could
afford to have their immunity hindered by the development of extravagant
ornaments. The idea gained some support, but it is difficult to prove, and was
soon eclipsed by a more promising line of inquiry.

In the 1990s, interest was growing in a large family of natural pigments
known as carotenoids. Animals can produce colours in several ways, such as using
structures like butterfly wing scales to reflect various wavelengths of light,
or by exploiting combinations of melanin pigments. But carotenoids form an
important part of the colourful signals used by many animals. The pigments,
which can be stored in a variety of tissues, are made mainly by plants and
algae, and are acquired either directly from them or by eating insects. Most
carotenoids are either red, orange or yellow, but purples, greens and blues can
be produced by binding proteins to the pigments.

Studies of house finches, guppies and stickleback fish have shown that
females prefer males with a brighter, carotenoid-based colouration. But for
carotenoid-based signals to be an honest reflection of a male鈥檚 status, they
must be costly. Last year, Owens and his colleague Val茅rie Olson
described three ways in which this cost might be incurred. Carotenoids, they
said, would be costly if they are either risky, rare or required. They dubbed
these the three Rs.

Carotenoids would be risky if they have detrimental effects on the body.
鈥淭his [suggestion] is based largely on a few cases in the medical literature
where carotenoid supplementation led to a higher than expected rate of cancer,鈥�
says Owens. Many researchers have looked for such an effect in fish and poultry,
yet there is no evidence to back such claims except in humans, says M酶ller.
Olson agrees that 鈥渞isky carotenoids鈥� cannot explain wonderfully coloured sexual
ornaments.

The conventional view is that carotenoids are costly because they are rare.
Healthier males can forage for more of the pigments than their inferior
counterparts. To some extent, this is true. 鈥淭he question,鈥� says Owens, 鈥渋s
whether this is the full story, and even whether it is the most important part
of the story.鈥�

Indeed, evidence is piling up in favour of the third mechanism鈥攖hat
carotenoids are required, in particular by the immune system and in the
detoxification processes that neutralise free radicals. In rodents and other
mammals, researchers have found that the pigments help stimulate the
proliferation of the T and B-lymphocytes that fight invading pathogens.
Carotenoids are also involved in the production of cytokines and interleukins,
essential molecules in the inflammatory response to injury. What鈥檚 more,
carotenoids are antioxidants that help mop up free radicals before they damage
DNA, lipids and proteins.

More than skin-deep

These pigments look like the missing link in Hamilton and Zuk鈥檚 original
handicap theory. They explain how the colourful calling cards of males reflect
their status: males can either use scarce carotenoids for immune defence and
detoxification, or for attracting females. Males that are more susceptible to
disease and parasites will have to use their carotenoids to boost their immune
systems, says M酶ller, whereas males that are genetically resistant will use
fewer carotenoids for fighting disease鈥攁nd advertise this by using the
pigments for flashy displays instead.

Until recently, this idea was simply speculation. 鈥淎t the moment there is a
big, big difference between the evidence and the theory,鈥� says Owens. 鈥淲e need
to know whether organisms really can shift the allocation of their carotenoids
between their immune system and their ornament.鈥� M酶ller set out to answer this
question, and some of his early findings happened almost by accident during
research at Chernobyl.

Working with Italian colleagues, including Nicola Saino of the University of
Milan, M酶ller investigated the health of male barn swallows that have been
forced to live with debilitating background radiation since 1986. 鈥淚 was trying
to measure mutation rates because of the unnaturally high levels of
radioactivity,鈥� he says. But blood samples revealed something more. The types of
white blood cells indicated, as expected, that the birds were under stress, yet
their immune response was down. Chernobyl swallows were also uniformly pale in
colour鈥攅ven males with long tail feathers, a sexual signal normally
accompanied by bright colouration. M酶ller believes that the high background
radiation forces the birds to neglect their disease-fighting capabilities and
shift carotenoids from sexual signalling to countering their unnaturally high
levels of free radicals.

Research on chickens also supports the idea that carotenoids can be co-opted
to fight disease. Infection by a single blood parasite can reduce an
individual鈥檚 carotenoid levels by as much as 80 per cent in a week. 鈥淭he
turnover can be dramatic in association with disease,鈥� says M酶ller.

In a recent study, M酶ller, Saino and their colleagues again looked at barn
swallows, this time in a normal environment outside Milan. These small, graceful
birds have several types of sexual signals to attract females, including their
long tail feathers and bright red throat patch. The birds with the longest tails
also have the brightest patches. M酶ller and his colleagues found that males with
dull signals had higher levels of immunoglobins, indicating they were more
frequently infected by pathogens. They also had lower levels of carotenoids in
their blood than brightly coloured rivals, who didn鈥檛 need to use up the
pigments in fighting disease. 鈥淚 love the idea of individuals facing a trade-off
between using carotenoids to make sexual ornaments or using them for their
immune systems,鈥� says Owens. 鈥淚t鈥檚 a beautifully elegant explanation for a lot
of puzzling facts.鈥�

However, much work remains to be done to find out how important the
phenomenon is, and exactly how the payoffs between carotenoid-based sexual
signalling and immune function pan out. M酶ller has some ideas about how the work
might proceed. 鈥淥ne could genetically engineer individuals to change their
production of immune substances, or explicitly change the amount of free
radicals that have to be neutralised by the detoxification system,鈥� he says.

But such manipulations will be no substitute for studies of animals in the
wild. That is why M酶ller is planning to return to Chernobyl, where the washed
out male barn swallows cannot help advertising their plight, and the females
can鈥檛 afford to be so picky about the colour of their mate.

CAROTENOIDS are not just involved in sexual selection, it seems. They may
also explain why baby birds open their mouths to reveal brightly coloured gapes
and why egg yolks are yellow.

In the past few years, there have been at least three studies showing that
parent birds respond more strongly to offspring with intensely red gapes. But
nobody knew why. Now Anders M酶ller from the Pierre and Marie Curie University in
Paris, Nicola Saino from the University of Milan and their colleagues may have
found an answer.

They suspected that a bright red gape is a way for chicks to advertise their
health to parents. If so, when a chick encounters a new pathogen, the carotenoid
pigments in the mouth should be redirected to the immune system, and the colour
will fade. To test this idea, M酶ller and his colleagues injected baby barn
swallows with sheep cells. Sure enough, their gapes became paler. What鈥檚 more,
giving them extra carotenoids reversed the effect. So, by preferentially feeding
chicks with the brightest gapes, the parents are investing in the offspring that
are most likely to survive.

Carotenoids are also the reason for the colour of egg yolks in birds,
reptiles and many fish. Egg producers exploit this by feeding birds carotenoid
supplements to intensify the colour of eggs, because customers prefer more
brightly coloured yolks. But no one knew why animals enrich their eggs with
these pigments.

Now Jon Blount and David Houston of Glasgow University, together with M酶ller,
believe they have found an answer, which they will publish next month. Rapidly
growing organisms, such as embryos, produce lots of free radicals because of the
high rates of metabolism during growth, and recent research has confirmed the
antioxidant properties of carotenoids can help protect developing embryos, they
say. Blount believes that incorporating carotenoids into the egg gives chicks a
head start in life. And a high-quality female can pass on more of the vital
pigments to her offspring.