June 23, 2003
Cooperation between unrelated male lizards adds
a new wrinkle to evolutionary theory
By Tim Stephens
Blue-throated lizards that help each other achieve reproductive success
are also helping scientists understand how social cooperation evolved.
Throat color of male side-blotched lizards corresponds to
alternative male strategies for reproduction. Orange males, in
top photo, usurp territory. Yellow males, above, are cryptic and
also mimic females. Blue males, in center, cooperate in defense
of territories with another blue male. The side-blotched lizard
is found on rock outcroppings in the inner Coast Range of California,
below. Photos: B. Sinervo
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
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, has
been studying the side-blotched lizard (Uta stansburiana) since
1989. He recently teamed up with French ecologist Jean Clobert to analyze
10 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,"
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
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
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,"
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,"
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