Fast Friends, Sworn Enemies

ELIZABETH PENNISI
Science, 2003 302:774-775

Abstract:
Even as the bride and groom walk down the aisle, they—or at least their guests—know that marital bliss can be short-lived. Wrinkles can appear in the smoothest relationships and turn lovers into adversaries. Biologists are now realizing that the same holds true in symbiotic relationships. What starts out as a mutually beneficial arrangement can turn into a commensal one, in which just one partner benefits. In the worst case, one symbiont begins to parasitize the other. But sometimes the partners work through adversity to restore balance in their alliance.

A new awareness of the complexity of these interactions is shaking up the ecology and evolutionary biology communities, which are used to thinking of interspecies interactions as stable. “We’ve been stuck classifying these things as mutualist, commensal, or parasitic, but we’ve come increasingly to understand how variable [these relationships] are,” explains Angela Douglas, a symbiologist at the University of York, U.K. Given the range of behaviors covered, the word “symbiosis” needs redefining, says Douglas Zook of Boston University: It should be applied to any interactions that use one or both partners’ resources.

The more biologists look, the more symbiosis they see. Forests thrive only when fungi blanket their roots. Corals rely on photosynthesizing algae. Gut symbionts help humans and other animals digest food. “Symbiosis is a major phenomenon extending across all kingdoms,” says Zook. The idea that different organisms live and work together dates to 1868, when German botanists Albert Bernhard and Heinrich Anton de Bary independently developed the symbiosis concept. The term applied to any association between different organisms, including parasitism. Later mutualism (both parties profit) and commensalism (one benefits but not at the expense of the other) joined parasitism as subsets of symbiosis. For decades, all were included under a single term. In the early 1900s, biologists decided the word symbiosis should apply only to relationships in which both partners benefit, and that’s what most textbooks teach today.

Only recently have researchers begun a wholesale investigation of how these relationships change over time. Plant pathologists have made a few key observations in studying grasses and microscopic fungi that live between their cells. Others have noticed that pathogens in one species or individual are partners in another. All this can lead to complex relationships that sometimes involve more than just two species. Moreover, the cause of a relationship switch is not clear-cut. But environmental factors can play a role, such as food shortages, new hosts, alterations in the chemical milieu, or changes in the local community.

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