Darwin recognized that natural selection could not favor a trait in one species solely for the benefit of another species. The modern, selfish-gene view of the world suggests that cooperation between individuals, whether of the same species or different species, should be especially vulnerable to the evolution of noncooperators. Yet, cooperation is prevalent in nature both within and between species. What special circumstances or mechanisms thus favor cooperation? Currently, evolutionary biology offers a set of disparate explanations, and a general framework for this breadth of models has not emerged. Here, we offer a tripartite structure that links previously disconnected views of cooperation. We distinguish three general models by which cooperation can evolve and be maintained: (i) directed reciprocation--cooperation with individuals who give in return; (ii) shared genes--cooperation with relatives (e.g., kin selection); and (iii) byproduct benefits--cooperation as an incidental consequence of selfish action. Each general model is further subdivided. Several renowned examples of cooperation that have lacked explanation until recently--plant-rhizobium symbioses and bacteria-squid light organs--fit squarely within this framework. Natural systems of cooperation often involve more than one model, and a fruitful direction for future research is to understand how these models interact to maintain cooperation in the long term.

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▪ Abstract  Agriculture has evolved independently in three insect orders: once in ants, once in termites, and seven times in ambrosia beetles. Although these insect farmers are in some ways quite different from each other, in many more ways they are remarkably similar, suggesting convergent evolution. All propagate their cultivars as clonal monocultures within their nests and, in most cases, clonally across many farmer generations as well. Long-term clonal monoculture presents special problems for disease control, but insect farmers have evolved a combination of strategies to manage crop diseases: They (a) sequester their gardens from the environment; (b) monitor gardens intensively, controlling pathogens early in disease outbreaks; (c) occasionally access population-level reservoirs of genetically variable cultivars, even while propagating clonal monocultures across many farmer generations; and (d) manage, in addition to the primary cultivars, an array of “auxiliary” microbes providing disease suppression and other services. Rather than growing a single cultivar solely for nutrition, insect farmers appear to cultivate, and possibly “artificially select” for, integrated crop-microbe consortia. Indeed, crop domestication in the context of coevolving and codomesticated microbial consortia may explain the 50-million year old agricultural success of insect farmers.

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Gardens of fungus-growing ants (Formicidae: Attini) traditionally have been thought to be free of microbial parasites, with the fungal mutualist maintained in nearly pure ''monocultures.'' We conducted extensive isolations of ''alien'' (nonmutualistic) fungi from ant gardens of a phylogenetically representative collection of attine ants. Contrary to the long-standing assumption that gardens are maintained free of microbial pathogens and parasites, they are in fact host to specialized parasites that are only known from attine gardens and that are found in most attine nests. These specialized garden parasites, belonging to the microfungus genus Escovopsis (Ascomycota: anamorphic Hypocreales), are horizontally transmitted between colonies. Consistent with theory of virulence evolution under this mode of pathogen transmission, Escovopsis is highly virulent and has the potential for rapid devastation of ant gardens, leading to colony mortality. The specialized parasite Escovopsis is more prevalent in gardens of the more derived ant lineages than in gardens of the more ''primitive'' (basal) ant lineages. Because fungal cultivars of derived attine lineages are asexual clones of apparently ancient origin whereas cultivars of primitive ant lineages were domesticated relatively recently from free-living sexual stocks, the increased virulence of pathogens associated with ancient asexual cultivars suggests an evolutionary cost to cultivar clonality, perhaps resulting from slower evolutionary rates of cultivars in the coevolutionary race with their pathogens.

Cultivation of fungi for food by fungus-growing ants (Attini: Formicidae) originated about 50 million years ago. The subsequent evolutionary history of this agricultural symbiosis was inferred from phylogenetic and population-genetic patterns of 553 cultivars isolated from gardens of “primitive” fungus-growing ants. These patterns indicate that fungus-growing ants succeeded at domesticating multiple cultivars, that the ants are capable of switching to novel cultivars, that single ant species farm a diversity of cultivars, and that cultivars are shared occasionally between distantly related ant species, probably by lateral transfer between ant colonies.

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The evolutionary history of the symbiosis between fungus-growing ants (Attini) and their fungi was elucidated by comparing phylogenies of both symbionts. The fungal phylogeny based on cladistic analyses of nuclear 28S ribosomal DNA indicates that, in contrast with the monophyly of the ants, the attine fungi are polyphyletic. Most cultivated fungi belong to the basidiomycete family Lepiotaceae; however, one ant genus, Apterostigma, has acquired a distantly related basidiomycete lineage. Phylogenetic patterns suggest that some primitive attines may have repeatedly acquired lepiotaceous symbionts. In contrast, the most derived attines have clonally propagated the same fungal lineage for at least 23 million years.