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All the leaves are brown — anyone know why?

by Rowan Hooper

In Japan, the beauty of leaves in autumn is revered with almost religious fervor. Part of the autumn weather forecast is devoted to showing the “leaf front” as the color change in trees moves across the country. Millions of tourists travel to marvel at the display.

But how many people ask themselves why trees put on such a spectacular display? Probably not many.

It took a man of uncommon intellect to ask the question no one else had thought of — William Hamilton, the Oxford evolutionary biologist who died last year. Hamilton was arguably the most important biologist since Darwin, and his work forms the basis for much of modern evolutionary biology. But his ideas about autumn colors remained just rumors in the zoological community until earlier this year, when they were posthumously published. Co-author Sam Brown, now of the University of Montpellier, France, had been working on the paper when Hamilton died.

Hamilton’s reasoning looks deceptively simple in retrospect. He asked himself, what is all that autumn color for? It’s certainly not just for us to marvel at — it must have some function.

If animals use signals to convey information to other animals, then why not plants? Peacocks, for example, grow large, elaborate tails that are energetically expensive, both to develop and to carry around. Why? Because peahens can look at the tail and use the information to help them choose which male to mate with. Only healthy males are able to “afford” to grow expensive tails.

The theory that explains the evolution of such costly signals in these terms is known as the handicap theory. Handicap, because the animal apparently burdens itself with a heavy cost. If a signal is cheap to make, any crummy male could make it. Only expensive traits are reliable indicators of quality, because only “well-off” animals can make them. The theory, however, had not been applied to plants until Hamilton started thinking about autumn colors.

As the days shorten, trees start recycling the green chlorophyll in their leaves, slowing down growth systems in preparation for winter. But at the same time, the leaves actively synthesize new pigments. The red-purple anthocyanin pigments, for example, are made in huge amounts, even though they are not involved in photosynthesis. And there are some fluorescent compounds that are only found in autumn leaves. Trees don’t choose mates like peacocks, so why do they “invest” so much on signals? Who are they signaling to?

Writing in the journal Proceedings of the Royal Society (Biological Science), Hamilton and Brown draw an analogy with gazelles. When a cheetah is spotted, gazelles perform a costly “stotting” display — pogoing up and down in full view of the predator. What the gazelle is saying to the cheetah, in effect, is “Go and pick on someone else — I’m so fit and agile, I can perform these elaborate displays.”

Trees have predators, too, and they signal in a similar way. The bright autumn colors are the trees’ way of saying to its insect pests: “I’m strong enough to resist you. You might as well go feed on another tree.”

To test their hypothesis, Hamilton and Brown looked at 262 tree species and scored them according to the degree of color-change they underwent in autumn. Then they looked at the number of different aphid species that were associated with each tree species. Many insects attack trees, but aphid damage is particularly intense. According to one unrelated study, saplings sometimes weigh less at the end of the year than they did at the beginning — because of the damage caused by aphids.

The researchers found that tree species that were host to the most species of aphids were the ones that had the brightest autumnal colors. In other words, tree species that over evolutionary time have had the most to lose from insects, advertise their resistance the strongest. Returning to the gazelle analogy, if cheetahs didn’t exist to hunt them, gazelles wouldn’t have “needed” to evolve their stotting display. Maples, (kaede and momiji in Japanese), which are renowned for having some of the most spectacular autumn displays, are also some of the most heavily aphid-infected trees. The next test of this will be to see if brighter-colored individuals within a species have fewer aphids.

Hamilton was well-known for his approach to biological questions. Many of his ideas were so outlandish and out of sync with the times that they were ignored for years. His work on social insects, for example — ants, wasps and bees — now forms the basis for much evolutionary theory. Richard Dawkins credits Hamilton for waking him up to a gene-centered view of life. His ground-breaking book, “The Selfish Gene,” was inspired by Hamilton’s work.

“I knocked on Hamilton’s door as a Master’s student in Oxford in 1995,” said Brown in an e-mail interview. “He suggested I look at why some trees vividly change color in autumn. He put forward this crazy idea that this may be a signaling adaptation.”

Such was Hamilton’s approach: pursuing crazy ideas. Brown doesn’t know how this crazy idea will be received, or if it will stand the test of time. “It is still too early to tell,” he said. “The scientific community [is] too slow. My hope is that people are planning experiments to test the theory. But [working with Hamilton] was certainly a very inspiring time for me. His approach has had a lasting impression on the way I work.”

And that will be Hamilton’s legacy: He changed our understanding of the world, at a deep level. From social insects to selfish genes, and now autumn leaves.