Getting by in a Game without Winners

GAMES ACROSS THE BOARD

Courtesy Barry Sinervo

The three male morphs of the side-blotched lizard (Uta stansburiana). Morphs are determined by a gene complex that influences behavior and physiology as well as morphology. Aggressive orange males (top) dominate blues (middle), which cooperate to exclude the diminutive female-mimicking yellows (bottom). Yellows close the competitive circle by mating sneakily with females attracted to the oranges' spacious territories

Sinervo and Kerr both expect rock-paper-scissors to be more widespread than is currently recognized. Kerr points out that toxins analogous to colicins are produced by almost every major lineage of bacteria and that evidence exists for similar compounds in yeasts.

Sinervo has recently identified rock-paper-scissors in a second lizard species that has been separated from its side-blotched cousin for an estimated 135 million years. "Either the rock-paper-scissors game is that ancient, or it is a system that evolves quite easily," he says.

Indeed, he suspects that nontransitive systems are "all over the place." They're just harder to see. Unlike his lizards, with their conspicuous throat colors, "the vast majority of mammals are playing their games in an olfactory [dimension] that we, to all intents and purposes, have abandoned," he says.

Sinervo says a search of species that undergo population density cycles, for example, microtine rodents, might prove fruitful. "There should be these alternative male strategies that do well under different density conditions."

But both researchers are looking beyond individual species for rock-paper-scissors. "This need not play out within the same species," says Kerr. "It can play out between different species." He explains: "As long as you've got a toxin producer, as long as you've got resistant and sensitive types, and as long as there are ordered growth rates, then you have the potential at least for nontransitivity." The requirement for spatial structure points to systems of sessile organisms, or those with low dispersal rates, as the likeliest candidates.

Kerr cites a paper from 1979, which revealed nontransitive patterns of dominance within a community of encrusting marine organisms competing for space on coral reef substrates.⁵ It is intriguing, he says, that many of these organisms, which include corals, algae, sponges, ascidians, and ectoprocts, are known toxin producers.

In another scenario, allelopathic compounds manufactured by certain plants hamper the growth of competitors. Ragan Callaway of the University of Montana, who works on the role of allelopathy in biological invasions of introduced species, is impressed with the idea. "It really does set up a lot of potential for nontransitive effects being powerful in terms of really maintaining coexistence and diversity in systems."

But Alastair Fitter of the UK's University of York cautions that allelopathy itself is poorly understood. "There are one or two classic cases that seem to be well established," he says, but the general importance of allelopathy in plant ecosystems remains to be established.

Kerr also sees an analogy between the bacterial system and the ecology of fire-prone habitats such as California's chaparral and South Africa's fynbos, where certain plants have bizarre traits – the retention of dead branches, for example, or volatile leaf compounds – that enhance their flammability. "Plants might become more flammable in order to fend off more sensitive competitors," he says. He notes that many such plants have elaborate mechanisms for persisting through fire events (akin to colicinogenic E. coli being resistant to their own toxins), while other species (such as the third player in the colicin system) are not flammable but are fire-adapted. "This is very tentative," says Kerr. And empirical studies could prove problematic, he says: "People don't take too kindly to you lighting matches in the chaparral."

SURVIVAL OF THE WEAKEST

Considerable obstacles hamper the study of such ecological processes in long-lived organisms over multiple generations. "It's rather easier to construct a realistic microcosm experiment in a microbial system than to recreate a plant system, which is based on soil," says Fitter. "Controlling the biochemistry of that is extremely difficult."

Kerr maintains that the importance of nonhierarchical relationships is currently underappreciated. "I think there's probably a lot out there that is straight hierarchies," he says. "Whether [rock-paper-scissors] still make up a minority after the tallying is done, that's another issue."

And if nontransitive competition turns out to be common, then so might some counterintuitive evolutionary dynamics. Says Kerr: "In a nontransitive world, an organism is basically taking out the enemy of its enemy by being a better grower." This, he says, leads to a phenomenon that has been dubbed "survival of the weakest," in which selection can favor types that exercise some form of restraint in their competitive impact on others.⁶"If A slows down, that liberates B to take out C, which liberates A," he explains. "That makes this something that really is important rather than just being something that's kinda cute," says Callaway.