Rethinking crop-disease management in fungus-growing ants.

A nt fungus farming has become a prominent model for studying the evolution of mutualistic cooperation, with recent advances in reconstructing the evolutionary origin and elaborations of the symbiosis (1, 2), discovering additional partners and clarifying their interactions (3, 4), and analyzing host–symbiont conflict suppression (5). The attine ants are rivaled in their farming sophistication only by the Macrotermitinae, which evolved a similar obligate dependence on fungus gardens (6). The discovery of new antagonistic and mutualistic partners in the attine symbiosis has attracted wide attention, but the prevailing coevolutionary paradigm behind key components of this mutualism is now challenged by a study by Sen et al. in this issue of PNAS (7). The attine ants originated some 50 million years ago (2). The 12 genera with 200 described species have realized a number of cultivar shifts (2, 8) and transitions in social complexity that culminated in the leafcutter ants with their enormous colonies, long-lived multiply mated queens, and extensive worker caste differentiation (9). From its very origin, the symbiosis has been haunted by a specific fungal disease caused by species of the genus Escovopsis (4, 10). The discovery of this garden pest (4) became a showcase of nature’s corruptive tendencies and inventiveness when it was shown that the ants had domesticated actinomycete bacteria to help suppress this bane (3). Sen et al. (7) present culture-independent 454-sequencing data and rearing experiments to document that the ant-associated actinomycetes are more diverse than previously thought (not only Pseudonocardia but also Amycolatopsis is found) and that they are rarely specific in their inhibition of other microbes. These findings are incompatible with a long history of specific coevolution between these actinomycetes and Escovopsis (3, 4, 8), but they are consistent with the recurrent acquisition of new strains (11, 12). Sen et al. also show that multiple strains can be isolated from the cuticle of single ants and that some of them may not be mutualists. In addition, their in vitro agar plate encounters often end up with the crop symbiont being inhibited or killed by the actinomycete strains, suggesting that the ants need to apply actinomycete-produced antibiotics with surgical precision and in doses that strictly match the infection problem. However, the pairings used were random, so this evidence does not preclude that natural combinations of resident symbionts in field colonies are better matched (13). These results will change the way we think about the attine ant symbiosis. Extrapolations from rather limited data collected 10 years ago now appear to be oversimplifications in need of more explicit testing and at least partial rectification, a process that was already initiated less explicitly a few years ago (13). This changing insight mirrors the way in which we obtained our current view on coevolution between the higher attine ants and their garden symbionts. The latter were initially considered to be strictly vertically transmitted and to have cospeciated with their hosts (14), an inference that was revised into diffuse coevolution recently (15). Science and discovery proceed by hallmarks like this: We also no longer believe that phytophagous insects in general had tight coevolution with their host plants (16). There may be clades that have such reciprocity, but the burden of proof has become reversed. It now appears to be more straightforward (7) to interpret the actinomycete– ant association as having evolved for mutual benefits (17) than to maintain a strict antagonistic coevolutionary scenario for the actinomycete–Escovopsis interaction (3, 4, 8). Actinomycetes are slow-growing microbes that produce an-