Top 100 Stories of 2010 No. 3: E.O. Wilson's Theory of Altruism Shakes Up Understanding of Evolution
In 1975 Harvard biologist E. O. Wilson published Sociobiology, perhaps the most powerful refinement of evolutionary theory since On the Origin of Species. Darwins theory of natural selection postulated a brutal world in which individuals vied for dominance. Wilson promoted a new perspective: Social behaviors were often genetically programmed into species to help them survive, he said, with altruism
self-destructive behavior performed for the benefit of othersbred into their bones.
In the context of Darwinian selection, such selflessness hardly made sense. If you sacrificed your life for another and extinguished your genes, wouldnt the engine of evolution simply pass you by? Wilson resolved the paradox by drawing on the theory of kin selection. According to this way of thinking, altruistic individuals could emerge victorious because the genes that they share with kin would be passed on. Since the whole clan is included in the genetic victory of a few, the phenomenon of beneficial altruism came to be known as inclusive fitness. By the 1990s it had become a core concept of biology, sociology, even pop psychology.
So the scientific world quaked last August when Wilson renounced the theory that he had made famous. He and two Harvard colleagues, Martin Nowak and Corina Tarnita, reported in Nature that the mathematical construct on which inclusive fitness was based crumbles under closer scrutiny. The new work indicates that self-sacrifice to protect a relations genes does not drive evolution. In human terms, family is not so important after all; altruism emerges to protect social groups whether they are kin or not. When people compete against each other they are selfish, but when group selection becomes important, then the altruism characteristic of human societies kicks in, Wilson says. We may be the only species intelligent enough to strike a balance between individual and group-level selection, but we are far from perfect at it. The conflict between the different levels may produce the great dramas of our species: the alliances, the love affairs, and the wars.
When you published Sociobiology in 1975, you faced enormous resistance, especially to the implication that human nature was genetically based. Now your colleagues are defending one of key tenets in your bookkin selectionwhile you try to dismantle it. What do you make of the shifting attitudes in your field?
Interesting, isnt it? But Im not so sure I pivoted that much on kin selection in Sociobiology. If you look at the opening pages, I had a diagram showing how a future science of sociobiology would be built. Kin selection was a nice little part of it in 1975, but Sociobiology went way beyond that. It goes into demography: how groups are formed, how they compete, how communication evolves. Together with ecology and population genetics, it all formed a framework to help explain the origin of social behavior.
Yet a generation of sociobiologists built their research around the idea of kin selection. How did that happen?
They were enchanted by kin selection because it appeared to have a basis in mathematics. It seemed solid and it looked good. It was glamorous.
Your new paper states that the mathematical underpinning of kin selection, called the Hamilton inequality, does not work. Why not?
When analyzed to the bottom of its assumptionswhen we ask under what conditions it could holdit applies only to a very narrow set of parameters that dont actually exist on Earth. Inclusive fitness turns out to be a phantom measure that cannot be obtained.
If inclusive fitness is wrong, how do you explain eusocialitywhen individuals reduce their ability to have offspring of their own to raise the offspring of others?
It turns out that theres only one condition that has to be reached in the course of evolution for eusociality to emerge: A mother or father must raise their young within reach of adequate resources at a defensible nest. Getting from the solitary lifestyle to one that includes a defensible nest can be done in one evolutionary stepone gene change. This turns the concept of inclusive fitness on its head, because the gene change and the social behavior came first. Kinship is a consequence of that, not a cause.
How do these ideas play out in the natural world?
Lets take the example of a bird with helpers at the nest. Supporters of inclusive fitness point to a correlation between the amount of help that the young birds give when they stay at home and how closely they are related to the parents and each other. But the young birds are looking after their extended family only until they have families of their own. By analogy, you might stay home and baby-sit for younger siblings after college, but its not out of a sense of kinship toward them. Its because it makes financial sense until you find a job and move out. What these researchers unwittingly do not mention in their studies is that cases of inclusive fitness are quite unusual in an important way. Each of the bird species lives in an area where nest sites and territories are very scarce, very hard for young birds to get.
Can you give an example of such overinterpretation?
I recently had the opportunity to visit an endangered species called the red-cockaded woodpecker in Florida. This is the only species in the world that drills nests in live trees. Why do these birds drill in live trees? Because when they enter the tree it exudes large amounts of sticky sap all around the entrance hole. The birds can fly in and out, but their principal predator, the rat snake, is prevented from entering by this sticky mess. Now, finding the right kind of tree and drilling the hole takes a long time, as much as a year, for a young male red-cockaded woodpecker. It is to his advantage to stay with his parents and help them out while he is doing that. Maybe there is some kin selection going there, but thats not whats causing the behavior of staying at home and helping. When the young male completes his hole, he courts a female, they move in, and they start a nest there of their own. That is the incentive that keeps him there.
How would you interpret this behavior within your new framework?
The alternative hypothesis is that it is to the advantage of kids to stay at home until they can find a place to go. This
is called the anticipation of inheritance. If Mom or Dad dies, youve got their nest and their territory. If they dont, you stay, and its to your advantage to help, and its to their advantage to have your help until
you can get a territory of your own. Basic natural selection explains it; no kin selection required.
Seen that way, it is difficult to understand why anyone attributed this kind of behavior to kin selection in the
Thats what I point out in our Nature critique. Researchers have gone at it backward. Instead of studying whats going on and seeking the best explanation, they start by looking for a test to demonstrate its really kin selection.
What about the classic kin-selection example, worker bees sacrificing themselves for their queen? How else can you explain that?
The best way to think of what has been called altruism in social insects is to return to an individual level of selection: that is, queen to queen. Think of the workers as robots and near-replicants of the queen herself. From the beginning these subordinate replicants are just extensions of the queen. It really is queen against queen, since they are the only ones that produce offspring.
But whether or not bees are altruistic, altruism certainly exists in humans. Humans are different because we seem to have true multilevel selection (pdf). On one level, individual selection goes on inside groups, with people competing against each other and producing what we think of as selfish behavior. On another level, selection goes on between groups. Group selection tends to reinforce altruistic behavior in individuals because without altruistic individuals, the group is at a disadvantage in competition and combat with other groups. But that is not kin selection.
It seems as if kin selection could actually damage the group. For instance, nepotism weakens a group, doesnt it?
n the level of the group, nepotism is counter-evolutionary. A group of altruists will beat a society of selfish individuals every time. Group selection favors biological traits like communication and cooperation that are needed for the group to remain cohesive and powerful. In humans, theres a constant struggle between group selection and individual selection that is unique. Humans managed to find a way to strike a balance. It took a lot of intelligence, but that is a story for another day.
From an evolutionary perspective, then, does kinship matter at all in humans?
You can have kin selection incidentally. You can certainly increase your genes by giving up your job and your marriage and taking care of your sisters kids. If you did it very well, that could result in an increase in your genes. But my point is that it doesnt lead anywhere in terms of evolution. Inclusive fitness theory said that social behavior advances because kin find one another and bond together to spread their genes, and then a society emerges. But Im afraid its the other way around. When people bond together, kin or not, they can become competitive as a group.
Despite all this, your colleagues are digging in and defending kin selection with passion. How do you respond?
Its gonna be a battle royaland not pretty. You might know Schopenhauers three stages of response to a new idea. The three are one, ridicule, and Ive been through that already. Two, outrage. And three, the declaration that its obvious.
You seem to be passing through stage two right now.
One letter to Nature is signed by 144 people. Their argument has been around for four decades, but nothing in the letter addresses the challenges we raised: that the mathematical ground of inclusive fitness theory is unsound and that, when you compare competing hypotheses, outcomes are much more directly and convincingly explained by mainstream natural selection.
But for now it seems like the bulk of scientific opinion is against you.
Science is not done by polling. Have you ever heard of 100 Scientists Against Einstein? It was a pamphlet signed by 100 physicists to overthrow his theory of relativity. After they published it, Einstein remarked, Why 100 authors? If I were wrong, then one would have been enough!
Your new take on evolutionary theory seems to echo an older view of human nature: more about competition, less about compassion. Do you agree?
If you look at the humanities and much of the creative artsespecially the dramatic stories of war, alliance, and lovemany literary themes describe the conflict between group and individual selection. When we look at human evolution in this new way, its going to be much more productive. We now have solid grounding for explaining our social behaviors in terms of the multiple levels of selection that actually occur.
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