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Selfish gene revisited

The genetics of cooperation are more subtle than we expected. Is it time to rethink a key evolutionary idea?

THE mating habits of a small lizard are challenging a central tenet of evolutionary theory. One of the best explanations for why animals cooperate is that they help each other because they are closely related, a concept known as kin selection. It now appears that this isn’t always the case. Male side-blotched lizards cooperate with other males who are genetically similar, but are not related.

It’s a subtle but extraordinarily significant difference. Because the behaviour can’t be explained by kin selection, biologists may have to radically redefine the theory, or invoke a new form of evolutionary selection to explain why the lizards act this way. It even suggests a new mechanism by which “selfish” genes propagate themselves.

“It’s an extraordinary study,” says behavioural ecologist Walter Koenig of the Hastings Reserve at the University of California, Berkley. “It will force the field to look again at how evolution is acting, in ways that no one has managed to do.”

Cooperation among animals is commonplace, occurring among everything from meerkats to mole rats and social insects. The usual explanation is that animals cooperate with relatives to help them pass on the genes they share. Even the most extraordinary instances of cooperation, such as the altruism of sterile bees, can be explained by refinements to kin selection theory. Hamilton’s rule, for instance, states that this apparently selfless behaviour occurs in social insects because the reproductive setup of the colony ensures they are more closely related to the queen’s offspring than they would be to their own.

But the side-blotched lizard Uta stansburiana of California appears to be an exception, say biologists Barry Sinervo of the University of California in Santa Cruz and Jean Clobert of the National Ecological Laboratory in Paris.

Side-blotched lizards have colourful patches on their throats, which are blue, orange or yellow. The colour of the patch is determined by a single genetic locus called OBY. That locus and a host of other genes confer a distinctive collection of immune, hormonal and behavioural traits in each colour morph. These traits determine what role each colour morph plays in a unique mating struggle that Sinervo compares to the children’s game rock/scissors/paper.

Orange males are aggressive and try to steal blue males’ territories to gain access to females. Yellow males forgo territories, but they try to mate behind orange males’ backs. Blue males team up to guard their mates from sneaky yellows.

However, Sinervo and Clobert have confirmed that blue males do not cooperate because they are related. For 10 years, the researchers recorded the genetic pedigree of hatchlings born in the lab. They tagged and returned these hatchlings to the wild in a random distribution, ensuring the lizards’ relationships to each other would not unduly influence how they dispersed.

Blue males seek out, and establish territories alongside, other blue males. The two lizards help defend each other’s territories against marauding yellow males. But the researchers discovered that these males were more likely to be very genetically similar – without being related – than a random pair of blue males would be expected to be by chance. And by teaming up against yellow males, the “fitness” of each triples, as measured by the number of offspring they sire (Science, vol 300, p 1949). Using similar techniques, they also found that aggressive orange-throated males use an opposite strategy. They increase their fitness by keeping their distance from genetically similar rivals.

Sinervo believes the lizards use some sensory cue to determine each other’s genetic make-up. That makes sense, as animals are already thought to use cues such as smell to identify kin. He also says that the genes on the OBY locus that confer a blue throat are somehow linked to the other parts of the genome that produce the distinct physiological profile and mating strategy. Since the whole package increases fitness, they are inherited together through a process he calls “genome-wide correlational selection”.

Laurent Keller, an evolutionary geneticist at the University of Lausanne in Switzerland, says it is difficult to see how this can happen if these different parts of the genome do not lie on the same chromosome. “How is it possible that these are linked if they are widely distributed in the genome?”

Experts contacted by èƵ say they do not doubt the quality of Sinervo’s research. But his results are extremely difficult to interpret, and it could take a while before the full implications of the work become clear. “As people start looking at this kind of thing and documenting the genetic underpinnings of it, there are going to be more examples, not only within species, but between species,” says Stephen Shuster, a biologist at Northern Arizona University, Flagstaff.

Sinervo believes that biologists will probably have to refine their theories to account for the phenomenon. Koenig agrees: “Kinship isn’t important in the experimental situation they have created. Some other, previously undetected selective force is at work.”

Selfish gene revisited

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