From the Vault: Hamilton's Fall

ByCarl Zimmer
July 12, 2010
7 min read

[An old post I’m fond of]

Just before the winter solstice brings autumn to an end, here’s a chance to blog about the great evolutionary biologist–and student of fall foliage–William Hamilton. Hamilton, who died in 2000, has never reached the household-name status of other evolutionary biologists such as E.O. Wilson or Richard Dawkins or Stephen Jay Gould. But he deserves a place of privilege, for all his profoundly influential ideas. He found an explanation for altruistic behavior in many insect species by expanding biology’s notion of fitness to include the genes an individual shares with its relatives. He offered one of the best-supported theories for the origin of sex–as a way for a species to keep ahead of its parasites in their evolutionary arms race. And he proposed that sexual displays–such as peacock tails and rooster combs–are signals that males send to females to reveal their ability to fight off parasites and otherwise live well.

It wasn’t just the ideas he came up with that made Hamilton extraordinary–it was the way he came up with them. They just seemed to pop into his head, obvious and simple, and he proceeded to write them down in clipped, humble prose, tossing in a few equations to give a sense of their underlying beauty. And then he was off to the next idea, or a trip to the Amazon. Hamilton wasn’t much interested in promoting his ideas to the world at large, to become a talking head or a writer of best-selling science books (in part because he was extremely shy and humble). That’s probably one reason why Hamilton is sliding into obscurity even as his ideas live on.

In the current issue of Biology Letters, there’s an example of Hamilton’s enduring legacy. One of the last papers Hamilton wrote before he died (after an ill-fated trip to Central Africa to investigate a controversial theory about the origin of HIV), appeared in 2001 in the Proceedings of the Royal Society of London. He and co-author Samuel Brown asked why it is that leaves change color in the fall. There are many possible explanations. Perhaps leaves just look that way as they inevitably die, for example. Hamilton, however, believed there was an adaptation involved. He and Brown proposed that a brilliant leaf was, like a peacock’s tail, a signal. A peacock’s tail takes a huge investment of energy, energy that could otherwise be diverted to fighting off parasites or surviving other stresses. A strong male can afford to use up this energy, which makes the tail an honest ad for its parasite-fighting genes. In the case of leaves, trees are not sending signals to other trees–they are sending signals to tree-eating insects.

Trees, after all, are as besieged by insects as birds or other animals are by internal parasites. They fight their enemies a sophisticated arsenal of chemical agents, sticky traps, and other weapons of mass arthropod destruction. Hamilton and Brown proposed that trees that have a strong constitution warn off insects by changing colors in the fall. In a sense, they say, “I can shut down my photosynthesis early in the fall, pump a lot of red or yellow pigments into my leaves, and still have enough energy left to annihilate your babies when they hatch in the spring.. So just move along.”

Warning colors are a well-established fact in biology. Poisonous butterflies and snakes deter predators with them, and other species try to horn in on the protection by mimicking their appearance. But the notion that trees were warning off insects was quite new–just the sort of brilliant notion Hamilton might have while taking a stroll one autumn day. (Note: In forumlating his hypothesis, Hamilton depended heavily on a theory called the Handicap Principle formulated by Amotz Zahavi in the 1970s.)

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For evidence that autumn leaves are signals, Hamilton pointed to some interesting patterns. Aphids, for example, lay their eggs on trees in the fall; when the eggs hatch, the larva devour leaves voraciously. Hamilton and Brown found that aphids are less common on trees that have bright red or yellow leaves. And species with bright leaves tend to be burdened with more species of aphids specialized for feeding on them than trees with drab leaves.

Hamilton left this jewel of an idea behind after his death for other scientists to investigate. It’s a challenge to test, because there are so many links in the theoretical chain. “Vigor,” for example, is a tricky thing to measure in trees; you could, for example, shower a tree with aphids, close it up in a gigantic net, and see how well it defends itself against them. That’s a huge amount of work, however, that yields you one data point. And you’d still have to find a way to eliminate other factors, such as weather, the age of the tree, and so on.

But recently scientists have found a reliable clue to vigor in the shape of a tree’s leaves. Vigorous trees produce very symmetrical leaves, while weaker trees produces misshapen ones. Symmetry signifies much the same thing in swallow tails and gazelle horns and human faces. When a complex organ like a leaf or a feather forms, any environmental stress can throw off its development from perfect symmetry. In stronger indviduals, the develoment of the organ is better shielded from these insults.

In September 2001 a team of Norwegian biologists took advantage of the symmetry of vigorous leaves and went gathering leaves of birch trees. They collected them from 100 birch trees all told. Half of the trees were shimmering yellow, and the other half were still green. As Hamilton would have predicted, they found that the yellow leaves were consistently more symmetrical than the green ones. The researchers had gathered half their yellow and green leaves from a healthy stand of trees, and the other half from the middle of an outbreak of birch-feeding moth larvae. On average, the trees in the healthy stand had more symmetrical leaves than the moth-infested ones, once again just as Hamilton would have predicted. Finally, the biologists looked at how trees with different colors fared the following spring. They found that trees with strong colors suffered less damage from insects compared to trees with weak colors.

These results are powerful support for Hamilton, although they don’t tell the whole story. How much do aphids depend on the sight of leaves when they choose a tree, for example, as opposed to their smell? Still, it’s a disconcerting idea that’s gaining strength: a beautiful fall landscape is a giant shout of “Back off.” When you see a tree at its most autumnally glorious, be sure to remember Hamilton.

Update 9/27/04: Here is the sequel: some scientists think that fall colors mean something else.

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