Dec. 11, 2000 ITHACA, N.Y. -- If the objective of the genetic game of life is to distribute one's genes among the greatest number of offspring, an aggressive male with lots of females in a big territory would seem a likely winner.
Or would the loyal male who guards a single mate in a small territory come out ahead in the game? How about the landless loner who sneaks into other males' territories and mates with their females?
Thinking about the traditional children's game rock-paper-scissors (also known as paper- scissors-stone or roshambo), evolutionary biologists at Cornell University and the University of California at Santa Cruz have learned why nature allows all three genetic strategies to continue: Just as in the rock-paper-scissors game, each sexual strategy has advantages over one competitor and a vulnerability to another, so that all strategies have a reasonable chance of prevailing.
At least, they do for side-blotched lizards (Uta stansburiana ) on the rocky bluffs of coastal California, Kelly R. Zamudio and Barry Sinervo report in the Dec. 5, 2000 issue of Proceedings of the National Academy of Sciences (PNAS). The researchers show that each mating strategy allows its adherents enough reproductive success to perpetuate a contentious system.
"Some animals have been playing the rock-paper-scissors game long before our kids caught on," said Zamudio, a Cornell assistant professor of ecology and evolutionary biology. The rules, she recalls, are: Sharp scissors cut the soft paper; hard rock dulls scissors; but paper, although softer, covers rock. Thus, success in the game depends on each player's strengths and weaknesses.
Zamudio and Sinervo brought an appreciation for game theory as well as the observational skills of field biologists and the gene-screening techniques of molecular biologists to a lizard lair where almost anything goes: o For months during the lizard mating season, the biologists watched orange "bullies," the aggressive and highly territorial males with natural orange coloring on their throats, as they guarded their harems and mated with multiple females. (Side-blotched lizards, which are named for the distinctive markings on their flanks, occur in different throat color and behavioral "morphs," with males displaying bright orange, blue or yellow throats and corresponding mating behaviors, while females generally have lighter yellow throat coloration.)
o Sinervo and Zamudio also observed the blue-throated males as they defended smaller territories with as few as one female apiece throughout the production of the three egg clutches that are typical each summer for U. stansburiana . Most of the offspring from blue throat territories were likely to have genes from the local blue throats, which were not so busy protecting many females in larger territories, the biologists predicted. But there was always the chance that the testosterone-pumped orange throats had their way with some blue throats' females, or that sneaker males had fertilized some eggs.
o Resembling females in coloration, the sneaking yellow-throated males weren't always noticed by orange- or blue-throated males, and the interlopers often succeeded in copulating with females they never guarded. Most vulnerable were the more numerous females in the orange throats' vast territories.
The biologists obtained DNA for more than 400 paternity tests by snipping a tiny piece from the tips of the lizards' toes, a humane procedure that did not disable the animals. The result of the screening, using a process called microsatellite genotyping, could have been predicted by an experienced player of the rock-paper-scissors game (although the exact proportion of orange-, blue- and yellow-throat-sired offspring varies somewhat from year to year):
o The more numerous bullies were successfully producing young with their genes, including the next generation of bully males with orange throats. But they were often cuckhoeded by the sneaker yellow throats.
o The less aggressive, semi-monogamous blue throats were distributing enough genes to keep their morph in the mix -- and more often were the sole parents of all the eggs in their female's clutch.
The yellows specialized in sharing paternity with other male types -- with one surprise that the biologists noted in their PNAS article: Female side-blotched lizards, which can store sperm from several males for months, were more likely to produce eggs fertilized with sperm from sneaker males that had already died. For some reason that continues to puzzle the biologists, sneakers are more successful posthumous fertilizers. Death among the side-blotched lizards has less to do with intra-species battles than with predation by birds, Zamudio noted. Particularly visible and vulnerable, she said, are the orange throats performing their "push-up displays," a sign of aggression among lizards.
While the study explains how three different color morphs with their disparate mating strategies manage to persist, side by side by side, through evolutionary time, the U. stansburiana system is almost unique in the animal kingdom, Zamudio said. Some species of birds and fishes feature similar systems, she said, but evolutionary biologists know of few such systems in mammals.
Including the human animal?
"Well, I can see how some women might think they have known orange throats, blue throats or sneaker males at some point in their lives," Zamudio said, "but, no, we are not claiming any parallels between the reptilian strategies and human behaviors.
"Although, I guess if my husband were a lizard, he'd be a blue throat."
The PNAS article is titled, "Polygyny, mate guarding and posthumous fertilization as alternative male mating strategies." The studies were supported by grants from the National Science Foundation. Barry Sinervo is an associate professor in the Department of Biology at UC-Santa Cruz.
Related World Wide Web sites:
o PNAS online article: http://www.pnas.org/cgi/content/full/011544998v1
o Zamudio laboratory: http://www.es.cornell.edu/zamudio/KZhome.html
o World RPS Society: http://www.worldrps.com/index1.html
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