Evolutionary ecology, antibiosis, and all that rot.

P ity members of the Animal Kingdom. They must compete for prey that hide, defend themselves, or run away. This competition only intensifies when such prey die uneaten. The carcasses and leaves strewn across the landscape are now available to microbial competitors that are everywhere, grow rapidly, and know how to poison. So how can an animal scavenger make a living? In a study in this issue of PNAS (1) Nicrophorus beetles that raise their grubs on mouse carcasses are shown to use a 2-pronged strategy: avoid the nastiest carcasses and apply the antibiotics. Ecologists have typically studied competition among suites of closely related species (e.g., 5 species of Dendroica warblers) (2). However, in 1977, evolutionary ecologist Dan Janzen (3) pointed out that a large fraction of potential food—fruits, seeds, and carcasses—may be lost to animals through competition with bacteria and fungi. Microbes have a huge advantage, after all, because they are abundant both in the soil and the gut of the carcass. In warm environments, they can also reproductively overrun a carcass before it can be discovered by a hungry animal. Janzen posited that the resulting malodorous hydrogen sulfide and fatty acids that say ‘‘rotten’’ in any language may in fact be microbial messages proclaiming ‘‘this food is taken.’’ Few options were considered open to scavengers, other than to specialize on efficient discovery (i.e., be a vulture) or only eat a carcass when it is ‘‘still warm’’(i.e., be an opportunist) (4). In this view, spoilage, not ingestion, should be the common fate of the dead. Some animals, it turns out, may have additional options. Rozen and colleagues (1), in a clever set of experiments, suggest animals may also employ antibiotics—small molecules like peptides, glycopeptides, terpenes, and alkaloids that are effective at low densities in suppressing microbial competitors (5). They studied the burying beetle, Nicrophorus vespilloides, which uses small mammal carcasses as eat-in nurseries (Fig. 1). Nicrophorus parent their young and tend the carcass in which they burrow. This was doubly fortuitous. First, Rozen and colleagues had an animal that was heavily invested in keeping a carcass’s microbe titer in check. Second, the scientists could measure beetle fitness: the survival, growth rate, and size at maturity of the larval offspring, something often lacking in studies of competition. They found that female Nicrophorus preferred to raise young on freshly thawed mouse carcasses compared with those that sat at room temperature for 7 days (with the expected olfactory result). Furthermore, larvae grown on rotten carcasses were 10% smaller (size is a good predictor of future reproductive success in insects). Moreover, if stuck with a rotten carcass, the mothers could still do something about it. Before their eggs hatched, mothers deposited anal and oral secretions. Brood on old carcasses who were deprived of this prenatal care were smaller and took longer to develop than those raised on fresh carcasses. The authors conclude that there is something in the parental care, especially those secretions, which kept decomposer microbes at bay [carcasses treated with Nicrophorus secretions have been shown to grow less fungi (6) and bacteria (7)]. They acknowledge that how, exactly, the microbes decrease the fitness of beetle larvae and what, precisely, is in the secretions produced by the mothers, are both open questions. Despite the importance of understanding antibiosis in a world of infectious diseases, we know surprisingly little about its evolutionary ecology. Most ecologists study macrobes and have devoted little attention to antibiosis, a form of interference competition—the allocation of resources, not to grow yourself, but to suppress the growth of your competitors. Early models found it hard to conjure scenarios in which an animal engaging in costly, spiteful behavior could invade a new community (8, 9). As it turns out, the secret to successful antibiosis is staying put. When you give antibiotic-producing bacteria a structured medium, they affix to substrate, grow clonally, and produce a ‘‘no mans land,’’ absent competitors, where the antibiotics diffuse outward. Carrion and soil are full of such structure. Moving microbes out of the chemostat and into a more structured, realistic world [as Rozen and colleagues (1) do] has been a dependable recipe for insight