Cooperation Between Unrelated Male Lizards Adds A New Wrinkle To Evolutionary Theory

Most examples of cooperative behavior in animals involve cooperation between genetically related individuals, which is explained by the theory of "kin selection." Now, researchers have described an example of cooperation between genetically similar but unrelated members of a lizard species common in the western United States. Their findings, published in the June 20 issue of the journal Science, shed new light on the evolution of cooperation and social behavior.

Barry Sinervo, a professor of ecology and evolutionary biology at the University of California, Santa Cruz, has been studying the side-blotched lizard (Uta stansburiana) since 1989. He recently teamed up with French ecologist Jean Clobert to analyze ten years worth of data from Sinervo's ongoing field studies. The two scientists are coauthors of the new paper in Science.

"At first, I thought we were seeing kin selection, so it was astounding to find that the lizards that were cooperating were not related," Sinervo said. "There are many examples of kin selection, but we've found some really nonstandard things happening in this species."

The side-blotched lizard has three different color morphs (a "morph" is a morphologically distinct subset of a species). The orange, yellow, and blue color morphs differ not only in their throat color, but also in their behavior. Orange males are very aggressive and mate with lots of females by taking over the territories of other males--Sinervo calls them "usurpers." Yellow males are "sneakers" who don't defend territories but mimic females and sneak behind the backs of territorial males to cuckold them. And blue males are mate guarders, keeping a close eye on their mates; they recognize and chase off yellow sneakers, but lose out in confrontations with orange usurpers.

In previous papers, Sinervo has described these strategies as a kind of "rock-paper-scissors" game, where orange defeats blue, blue defeats yellow, and yellow defeats orange. The result is an evolutionarily stable situation in which no single color morph can dominate the population.

In the new study, Sinervo and Clobert found that blue males tend to establish territories in close proximity to other blue males. Furthermore, DNA analysis showed that neighboring blue males are more similar genetically than would be expected by chance. Yet Sinervo's long-term data on the pedigrees of lizards in the study area showed that the genetically similar blue neighbors are not kin.

"They are so similar they might as well be kin, but we can track the pedigrees back and show that in no case are they brothers or cousins or father-son pairs," Sinervo said.

Once they've set up neighboring territories, the genetically similar blue males apparently work together to guard their mates. The result is an average "fitness" level (measured in terms of the number of offspring they produce) three times higher than that of blue males without such neighbors. Orange males, in contrast, suffer a decrease in fitness if they have a genetically similar neighbor, and they tend to avoid settling near other orange males.

"Orange males are so aggressive, if they end up next to a genetically similar male they just annihilate each other in terms of fitness," Sinervo said.

Throat color in the side-blotched lizard is controlled by genes at a single "locus" or position on a chromosome. The chromosomes come in pairs, and the particular combination of two "alleles" or versions of the throat-color gene determines an individual's color pattern.

The remarkable thing about the color morphs of side-blotched lizards is that an enormous range of behavioral, physiological, and life-history traits are correlated with throat color. Genes for different traits can be linked physically if they occur close together on a chromosome, but according to Sinervo, throat color is linked to far more traits than could possibly be physically linked on the same chromosome.

"It's almost as if the whole genome is tightly tethered to this one master locus," he said. "In order to be a really 'good' blue, you have to have all these other alleles [of different genes] lined up in the right combination, and the same is true for orange and yellow color morphs. So there is strong selection for these different fitness combinations."

The male color morphs show differences not only in the way they interact with other males, but also in how they disperse from their birthplace and choose a territory to settle in, as well as in their hormone levels, immune systems, and other physiological traits. In females, throat color is linked to a different set of traits, which Sinervo has also described in previous papers.

"The whole genome crystallizes into three types," Sinervo said. "The alleles for all these different traits should be independent and separated on the chromosomes, yet the genes are interacting through this one locus."

The selection pressures that favor color morphs with distinctive sets of traits arise from the social system and behavioral interactions between individuals, he said.

"A lot of animals probably have that type of social selection going on. The lizards are really good for elucidating it because it is so conspicuous in them," Sinervo said.

This phenomenon of runaway social selection centered on the throat-color locus has led to the evolution of cooperation in the blue males, Sinervo said. This represents a new idea for how social cooperation evolves, which he and Clobert call "morphotypic" selection, as opposed to kin selection.

"Other researchers have interpreted genetic similarity as indicating a kin relationship, whereas we were able to show that they are genetically similar but not kin," Sinervo said.

This morphotypic level of selection may be a precursor to true kin selection, he added. The distinctive color morphs may also be a step toward the evolution of distinct species.

"We think we're hot on the trail of speciation," Sinervo said. "It's like they're trying to speciate, but they can't because the males screw it up."

In the "rock-paper-scissors" competition for mates, males force themselves on females who might otherwise choose a different mate on the basis of genetic compatibility. The best combinations might be male-female pairs of the same color morph, but the usurpers and sneakers scramble up those nice combinations, Sinervo said.

"These combinations build up again in the next generation, only to be partly scrambled by another round of rock-paper-scissors dynamics," he said.

The cooperative blue males are much more monogamous than the orange usurpers and yellow sneakers, Sinervo noted.

"They're the sensitive male lizards of the new millennium," he quipped.