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Scientists Square Off on Evolutionary Value of Helping Relatives
The New York Times, August 30, 2010

Why are worker ants sterile? Why do birds sometimes help their parents raise more chicks, instead of having chicks of their own? Why do bacteria explode with toxins to kill rival colonies? In 1964, the British biologist William Hamilton published a landmark paper to answer these kinds of questions. Sometimes, he argued, helping your relatives can spread your genes faster than having children of your own.

For the past 46 years, biologists have used Dr. Hamilton’s theory to make sense of how animal societies evolve. They’ve even applied it to the evolution of our own species. But in the latest issue of the journal Nature, a team of prominent evolutionary biologists at Harvard try to demolish the theory.

The scientists argue that studies on animals since Dr. Hamilton’s day have failed to support it. The scientists write that a close look at the underlying math reveals that Dr. Hamilton’s theory is superfluous. “It’s precisely like an ancient epicycle in the solar system,” said Martin Nowak, a co-author of the paper with Edward O. Wilson and Corina Tarnita. “The world is much simpler without it.”

Other biologists are sharply divided about the paper. Some praise it for challenging a concept that has outlived its usefulness. But others dismiss it as fundamentally wrong.

"Things are just bouncing around right now like a box full of Ping-Pong balls,” said James Hunt, a biologist at North Carolina State University.

Dr. Hamilton, who died in 2000, saw his theory as following logically from what biologists already knew about natural selection. Some individuals have more offspring than others, thanks to the particular versions of genes they carry. But Dr. Hamilton argued that in order to judge the reproductive success of an individual, scientists had to look at the genes it shared with its relatives.

We inherit half of our genetic material from each parent, which means that siblings have, on average, 50 percent of the same versions of genes. We share a lower percentage with first cousins, second cousins and so on. If we give enough help to relatives so they can survive and have children, then they can pass on more copies of our own genes. Dr. Hamilton called this new way of tallying reproductive success inclusive fitness.

Each organism faces a trade-off between putting effort into raising its own offspring or helping its relatives. If the benefits of helping a relative outweigh the costs, Dr. Hamilton argued, altruism can evolve.

Dr. Hamilton believed that one of the things his theory could explain was the presence of sterile females among ants, wasps, and some other social insects. These species have peculiar genetics that cause females to be more closely related to their sisters than to their brothers, or even to their own offspring. In these situations, a female ant may be able to spread more genes by helping to raise her queen mother’s eggs than trying to lay eggs of her own.

But as the years passed, Dr. Wilson’s enthusiasm for the theory waned. “It was getting tattered,” he said. Many species with sterile females, for example, do not have the strange genetics of ants and wasps. And many species with the right genetics have not produced sterile females.

After reading a 2008 article in which Dr. Wilson aired his misgivings, Dr. Nowak got in touch with him. Dr. Nowak and Dr. Tarnita were studying the mathematical underpinnings of evolution. They wanted to carry out a mathematical analysis of natural selection in general and inclusive fitness in particular. Dr. Wilson joined them.

The scientists developed equations that described two different behaviors in a population. One strategy might be selfish and the other altruistic -- leaving their nest after they hatch versus staying to help rear young, for example. The scientists then calculated the conditions in which one strategy or the other takes over the whole population.

The researchers found that inclusive fitness theory worked only under special conditions. All the effects that the animals had on each other had to take place on a one-to-one basis. In the real world, individuals may benefit from many other individuals as a group.

Standard natural selection, the scientists argue, explains everything inclusive fitness theory was supposed to, without these special conditions.

Dr. Nowak and his colleagues argue that their analysis should free scientists to think of other ways that altruism and other kinds of social behavior might evolve.

Thinking about why a worker would sacrifice her own offspring turns out be the wrong perspective on the question, they argue. Instead, they say, we should put ourselves in the queen’s perspective. They offer a mathematical model suggesting how natural selection could produce offspring that stay at a queen’s nest. If she produces daughters that stay in the nest, she can spend more time laying eggs, rather than hunting for food to feed her young.

“I think they’ve done a very thorough job,” said Michael Doebeli of the University of British Columbia. He has also grown skeptical about the importance many colleagues have put on inclusive fitness in recent years.

“The people who swear by this method somehow think there’s something magic about it that explains everything,” he said.

Dr. Hunt, who studies social wasps, does not find Dr. Hamilton’s ideas useful because it is nearly impossible to calculate the costs and benefits of helping relatives.

“I have never felt that inclusive fitness has contributed to an understanding of what’s going on,” he said. The Harvard team, Dr. Hunt said, is “basically on target.”

A number of scientists strongly disagree, though. “This paper, far from showing shortcomings in inclusive fitness theory, shows the shortcomings of the authors,” said Frances Ratnieks of the University of Sussex.

Dr. Ratnieks argues that the Harvard researchers cannot rule out kinship as a driving force in social evolution because their model is flawed. It does not include how closely related animals are.

It would be as if a team of researchers carried out a study on the effects of diet and exercise on health. Their subjects get different amounts of exercise but stay on the same diet. In the end, the experiment might show that exercise makes people more healthy. But it would not make any sense to also conclude that diet plays no role.

“If you don’t vary something you cannot say how important it is,” said Dr. Ratnieks.

Andy Gardner, an evolutionary biologist at Oxford, said bluntly, “This is a really terrible article.” One problem Dr. Gardner points to is the Harvard team’s claim that the past 40 years of research on inclusive fitness has yielded nothing but “hypothetical explanations.”

“This claim is just patently wrong,” Dr. Gardner said. He points to the question of how many sons and daughters mothers produce among the many insights inclusive fitness has brought.

In most species, the balance is 50-50. But there are exceptions. In some ant species, for example, the ratio is around three daughters for every son. That is because the sterile female workers invest more into female larvae than males. Inclusive fitness theory predicts just this situation, since the workers are more closely related to their sisters than to their brothers.

Dr. Gardner and a number of other biologists have co-authored a reply that they will be sending to Nature to challenge the new paper.

Dr. Hunt hopes to move the debate toward a resolution with a meeting he is to run in October at the National Evolutionary Synthesis Center in Durham, N.C. He will be bringing together scientists who build models of all the potential factors that drive the evolution of societies, from their kinship to their ecology. Ultimately, the scientists hope to build a model that can take into account all of these factors at once. “They’re all stoked, and I am too,” Dr. Hunt said.

Copyright 2010 The New York Times Company. Reprinted with permission.
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