Probably few researchers in fields outside ecology and mycology recognize the degree to which adjacent plants can share nutrients through their interrelationships with symbiotic fungi, forming what have been termed plant-fungus-plant guilds [1, 15]. A large body of work on beneficial interactions within plant communities reflects a growing interest among ecologists and evolutionary biologists in cooperative interactions in general, their implications for ecological function, and how such interactions evolve. Because the network of relationships among plants and their symbiotic fungal partners is more accessible to experimental manipulation than many other multi-species interactions, these systems have the potential to serve as models for studying the way in which evolution functions in groups.

Forty years ago, Erik Bjorkman injected radiolabeled glucose into the phloem of three Norway spruce trees and measured its transfer to nearby individuals of the plant Monotropa hypopitys [2]. Many similar experiments have since been done with various plant combinations, using traceable isotopes of carbon, phosphorus, nitrogen, and calcium [3, 4, 5, 6, 7, 8, 9, 10, 11, 12]. In all but one case, isotopes were found to move in varying degrees from one plant to another, providing the plant species in question shared mycorrhizal fungi, a diverse group of fungi that colonize roots to form symbioses with approximately 80% of the world's plant species. The single exception was itself revealing: in an association consisting of mycorrhizal fungi and two species of pine, ³²P applied to the hyphae (filaments) of the fungi was distributed to tree seedlings, but when applied to the seedlings did not move into the hyphal network - suggesting movement along gradients from relatively high to relatively low concentration [9]. Experiments in which "receiver" plants are shaded suggest C is also transferred along gradients. However, a recent study using dual C isotopes showed that, while most transfer was from plants in sun to neighbors in shade, some C moved in the opposite direction as well [8].

Transfer studies sometimes produce inconsistent results, particularly when done in field settings rather than in the highly controlled environments of the lab, emphasizing the need to better understand the details of this phenomenon. However, the large number of experiments showing positive results leave little doubt nutrient transfer among plants of different species is real, and that it is greatly facilitated by symbiotic fungi with the ability to physically link the roots of different plants.

Is nutrient transfer among different plant species parasitism, cooperation, or some blend of the two? Parasitism is known to occur in some cases; however, for reasons I'll discuss later, it is unlikely to be the primary explanation. If cooperation, how might it evolve? In traditional neo-Darwinian thinking, individuals are the units of selection, self-interest is the driver, and any genetic trait that causes an individual to sacrifice its own reproductive potential for the benefit of a larger group is selected against and eventually disappears. Though not always explicitly stated, in the traditional view fitness is linked closely to the ability to gather resources, and resource gathering is a competitive, zero-sum game in which giving equates to losing. However, in apparent contradiction to classical theory, altruism and cooperation are well documented in nature [e.g., 13], and considerable thought has been devoted to understanding how that might happen [13, 17, 21].

Three categories of model are invoked to explain how cooperation might arise and persist (the three are not mutually exclusive): kin selection (through sacrifice, an individual saves copies of its own genes in related individuals); group selection (an individual reduces its own reproductive fitness to increase the fitness of some larger group of which it is a member); and various forms of reciprocation [13].

Reciprocation is most frequently modeled using the "iterated prisoner's dilemma" derived from game theory, in which the second-highest possible payoff goes to the individual who cooperates with a partner, while the highest payoff goes to the participant lucky enough to find some sucker who will cooperate while getting nothing in return - a sort of permanent free lunch. Even though this payoff structure favors cheating, when the prisoner's dilemma is iterated multiple times (approximating real life a little more closely), the consistent winner turns out to be a strategy called tit-for-tat. In this approach a participant cooperates on the first move and thereafter responds in kind, with the exception that lack of cooperation is forgiven one time only [15]. (Iteration by the same two partners is crucial, because the participants can gain experience of one another. If the game is not iterated, noncooperation is always the best strategy.) Although quite robust, tit-for-tat is not evolutionarily stable, as it can be invaded by a strategy of pure cooperation, which can in turn be invaded by noncooperation.

A second general class of reciprocation models, termed "byproduct" or "no-cost" mutualism, awards the highest payoff to cooperation, which means there is no incentive to cheat, and furthermore there is no conflict between self-interest and group-interest [11]. Obvious examples are the ubiquitous obligate mutualisms. However, other forms of positive feedback among species abound in nature [15, 24]. Looser, more fluid, and perhaps more indirect than obligate mutualisms, these "extended" relationships nevertheless confer mutual benefits on the participants and therefore can be considered no-cost mutualisms [13].

A few years ago my colleagues and I suggested that plant-fungus-plant guilds might evolve through tit-for-tat [4]. We reasoned that the costs to an individual plant of sharing its symbiotic fungi with competitors are outweighed over evolutionary time by benefits, including, in particular: (1) improved survival of the fungus owing to the continuity in its food supply even when one or more host species are periodically absent (a common result of disturbance and recolonization); (2) smoothing of resource supply that occurs via transfers of chemical elements between plants; and (3) the greater stability of diverse as opposed to simple plant communities. More recently, Wilkinson [16] argued that plant-fungus-plant guilds served the self-interests of all participants, making them a form of no-cost mutualism.

Whatever the explanation, the abundance and high level of generality of mycorrhizal symbioses, combined with the variety of community types in which nutrient transfer has been observed, suggest plant-fungus-plant guilds are widespread. Moreover, they are almost certainly ancient. Mycorrhizal symbioses date to the earliest colonization of land by plants, and were probably a key to the success of that process [18]. In all likelihood, early symbioses were quite general, setting the stage for the early development of plant-fungus-plant guilds. Although some specificity now exists, most mycorrhizal relationships remain general, providing strong evidence that generality and its concomitant effects (such as linkages among plants) confer a selective advantage and produce a structure that is stable against exploitation.

There are at least two possible explanations for the ability of plant-fungus-plant guilds to resist takeover by exploitative strategies (i.e. parasites). First of all, plants are not just dumb suckers. When well fertilized, so that they do not need the nutrients provided by the fungi, plants will curtail mycorrhiza formation, which suggests the relationship is maintained only when the plants are getting something out of it [4]. Second, the flow of carbon along source-sink gradients means a plant that donates can also receive. The fungi act to maintain a certain balance among their hosts by shunting carbon from carbon-rich to carbon-limited plants. This is not detrimental to the carbon-rich plants, because their resource needs center on what the fungus gathers (nutrients and water) more than on carbon. At least some species of mycorrhizal fungi can convert a negative interaction between two plant species to either neutrality or synergism; in some instances this phenomenon is associated with a smoothing of nitrogen and phosphorus distribution between the plants [4, 19].

A probable selective advantage of plant-fungus-plant guilds is their adaptability. Guilds link numerous plant and fungal genotypes into a network of shared resources, expanding the range of genetically based responses to the environment well beyond those available to any single genotype [4, 20]. The end result is neither group nor individual selection, but a blend of the two. In plant-fungus-plant guilds, and probably in other diffuse mutualisms as well, relationships that confer selective advantage on individuals lead to networks of interdependence.

In their report of a recent workshop on the emergence of new levels of organization, Sigmund and Szathmary [22] quote the eminent systems thinker Michael Polanyi "We can recognize a strictly defined progression, rising from the inanimate level to ever higher additional principles of life... Evolution may be seen, then, as a progressive intensification of the higher principles of life" [23]. Sigmund and Szathmary go on to ask what many others have asked: why should we expect the development of an evolutionarily significant pattern to stop at individuals?

If higher units of selection actually exist, it is in the ubiquitous networks of mutualisms that we are most likely to find them. Because plant-fungus-plant guilds are relatively accessible to experiment compared with diffuse mutualisms such as plants and pollinators, they are an ideal model system in which to investigate this sometimes controversial issue.

David Perry is an emeritus professor in the Department of Forest Science, Oregon State University, Corvallis.

Caleb Brown is an illustrator and biologist living in Montana. By day he drives a delivery van, and by night he draws pictures with his computer.

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Endlinks

Mycorrhizal Symbioses - a detailed introduction to the topic.

Mycorrhiza Information Exchange - a clearinghouse of online resources, including forums, literature searches, and directories.

The Root Cellar - basic, child-friendly information on life in the "rhizosphere." Part of the Digital Learning Center for Microbial Ecology's Microbe Zoo.

Prisoner's Dilemma - play the game online, or follow the links to more information.