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Social-insect fungus farming

2006; Elsevier BV; Volume: 16; Issue: 24 Linguagem: Inglês

10.1016/j.cub.2006.11.016

1879-0445

Duur K. Aanen, Jacobus J. Boomsma,

Plant Parasitism and Resistance

Which social insects rear their own food? Growing fungi for food has evolved twice in social insects: once in new-world ants about 50 million years ago; and once in old-world termites between 24 and 34 million years ago [1Mueller U.G. Gerardo N.M. Aanen D.K. Six D.L. Schultz T.R. The evolution of agriculture in insects.Annu. Rev. Ecol. Evol. Syst. 2005; 36: 563-595Crossref Scopus (404) Google Scholar, 2Aanen D.K. Eggleton P. Rouland-Lefevre C. Guldberg-Froslev T. Rosendahl S. Boomsma J.J. The evolution of fungus-growing termites and their mutualistic fungal symbionts.Proc. Natl. Acad. Sci. USA. 2002; 99: 14887Crossref PubMed Scopus (307) Google Scholar]. The termites domesticated a single fungal lineage — the extant basidiomycete genus Termitomyces — whereas the ants are associated with a larger diversity of fungal lineages (all basidiomycetes). The ants and termites forage for plant material to provision their fungus gardens. Their crops convert this carbon-rich plant material into nitrogen-rich fungal biomass to provide the farming insects with most of their food (Figure 1). No secondary reversals to the ancestral life style are known in either group, which suggests that the transitions to farming were as drastically innovative and irreversible as when humans made this step about 10,000 years ago. Why is insect fungus farming interesting? The two independently evolved agricultural systems are impressive examples of mutualistic symbiosis — reciprocally beneficial relationships between different species. Some of the insect societies that evolved fungus farming are pinnacles of social evolution. Cooperation and social evolution within families is now fairly well understood from kin selection theory [3Bourke A.F.G. Genetics, relatedness and social behaviour in insect societies.in: Fellowes M.D.E. Holloway G.J. Rolff J. Insect Evolutionary Ecology. CABI Publishing, Wallingford2005Crossref Google Scholar], but we are only beginning to understand the direct and indirect evolutionary benefits of cooperation between unrelated individuals of different species [4Foster K.R. Wenseleers T. A general model for the evolution of mutualisms.J. Evol. Biol. 2006; 19: 1283-1293Crossref PubMed Scopus (241) Google Scholar]. What factors stop such cooperative efforts from being corrupted by cheating mutants that reap the benefits without paying the costs? Active partner choice, conditional partner fidelity and host sanctions towards non-cooperative symbionts have been suggested to be crucial factors that help defend against such cheats, and there is at least some evidence from other mutualisms to support these suggestions [5Kiers E.T. Rousseau R.A. West S.A. Denison R.F. Host sanctions and the legume-rhizobium mutualism.Nature. 2003; 425: 78-81Crossref PubMed Scopus (655) Google Scholar]. All these traits vary in fungus-growing social insects, making them good model systems for studying cooperation and conflict. Also, we now know that the ant–fungus symbiosis includes at least two further parties: a genus of specialized fungal parasites that attack fungus gardens; and specialized cultures of mutualistic bacteria that the ants rear on their own bodies to produce antibiotics against this disease [6Currie C.R. Scott J.A. Summerbell R.C. Malloch D. Fungus-growing ants use antibiotic-producing bacteria to control garden parasites.Nature. 1999; 398: 701-704Crossref Scopus (610) Google Scholar]. Recent studies have provided evidence for varying degrees of coevolution between these mutualistic and parasitic lineages [7Currie C.R. Wong B. Stuart A.E. Schultz T.R. Rehner S.A. Mueller U.G. Sung G.H. Spatafora J.W. Straus N.A. Ancient tripartite coevolution in the attine ant-microbe symbiosis.Science. 2003; 299: 386-388Crossref PubMed Scopus (297) Google Scholar, 8Currie C.R. Poulsen M. Mendenhall J. Boomsma J.J. Billen J. Coevolved Crypts and exocrine glands support mutualistic bacteria in fungus-growing ants.Science. 2006; 311: 81-83Crossref PubMed Scopus (250) Google Scholar]. Starting a fungus farm: collecting spores from the wild or inheriting your parent's crop? A young queen of a fungus-growing ant species takes a small clonal fungus fragment from her natal nest along on her mating flight, and uses this to start her own fungus garden in the newly founded colony. Some evolutionarily derived fungus-growing termites have a similar system of vertical symbiont transmission by a single parent, but in most species the first fungus garden is established from environmental spores on the first substrate structure in the centre of the nest. This horizontal mode of symbiont transmission should make it much easier to exchange crops between termite lineages, but for some reason these 'hop-overs' rarely happen between genera [2Aanen D.K. Eggleton P. Rouland-Lefevre C. Guldberg-Froslev T. Rosendahl S. Boomsma J.J. The evolution of fungus-growing termites and their mutualistic fungal symbionts.Proc. Natl. Acad. Sci. USA. 2002; 99: 14887Crossref PubMed Scopus (307) Google Scholar]. In fact, the genus-level symbiont specificity in fungus-growing ants and termites is rather similar, because sexual reproduction (symbiont fruiting) and horizontal exchange also happen within genera of fungus-growing ants [9Green A.M. Mueller U.G. Adams R.M.M. Extensive exchange of fungal cultivars between sympatric species of fungus-growing ants.Mol. Ecol. 2002; 11: 191-195Crossref PubMed Scopus (91) Google Scholar, 10Mikheyev A.S. Mueller U.G. Abbot P. Cryptic sex and many-to-one coevolution in the fungus-growing ant symbiosis.Proc. Natl. Acad. Sci. USA. 2006; 103: 10702-10706Crossref PubMed Scopus (133) Google Scholar]. Why is it important and interesting to know these symbiont transmission modes? Although the fungus-farming symbioses are clear examples of advanced obligate mutualism — reciprocal cooperation for direct fitness benefits to each of the parties — the reproductive interests of the insects and their fungi are not the same. The insect farmers have no interest in their symbiont allocating resources to growing mushrooms for horizontal spore transmission. Similarly, the fungal symbionts have no interest in farmers producing sexual offspring rather than workers that can provide them with more substrate [11Aanen D.K. As you reap, so shall you sow: coupling of inoculating and harvesting stabilizes the mutualism between termites and fungi.Biol. Lett. 2006; 2: 209-212Crossref PubMed Scopus (50) Google Scholar, 12Aanen D.K. Boomsma J.J. The evolutionary origin and maintenance of the mutualism between termites and fungi.in: Bourtzis K. Miller T.A. Insect Symbiosis II. CRC Press, Boca Raton2006Crossref Google Scholar]. Furthermore, an established fungus garden has no interest in a competing strain becoming established, even though the insect farmers would possibly benefit from a genetically more variable crop. These reproductive conflicts play a role in the daily life of social insect farmers: leaf-cutting ants are known to actively suppress symbiont fruiting in lab colonies [13Mueller U.G. Ant versus Fungus versus Mutualism: Ant-cultivar conflict and the deconstruction of the attine ant-fungus symbiosis.Am. Nat. 2002; 160: S67-S98Crossref PubMed Scopus (146) Google Scholar], and resident fungal clones express mycelial incompatibility reactions to eliminate introduced fungal strains [14Poulsen M. Boomsma J.J. Mutualistic fungi control crop diversity in fungus-growing ants.Science. 2005; 307: 741-744Crossref PubMed Scopus (136) Google Scholar]. These conflicts can be understood from levels of selection theory. Both parties gain fitness by cooperating for the common good, but they are also individually selected to express selfish traits when the fitness benefits to be gained exceed the ensuing losses in group-level fitness [15Frank S.A. Host-symbiont conflict over the mixing of symbiotic lineages.Proc. R. Soc. Lond. B. 1996; 263: 339-344Crossref PubMed Scopus (194) Google Scholar]. A major unanswered question is why termites with horizontal symbiont transmission do not suppress fungal fruiting in the same way as ants and termites with vertical symbiont transmission do. Such a parasitic trait would have an immediate colony-level advantage, whereas there would hardly be any colony-level cost since neighboring colonies would produce the fungal spores that the offspring of these cheating farmers need [12Aanen D.K. Boomsma J.J. The evolutionary origin and maintenance of the mutualism between termites and fungi.in: Bourtzis K. Miller T.A. Insect Symbiosis II. CRC Press, Boca Raton2006Crossref Google Scholar]. Do reproductive conflicts threaten the evolutionary stability of fungus farming or are they resolved? Both the ants and the termites cultivate their fungal crops in monocultures. This is remarkable, because there is ample genetic variation of fungal strains across colonies so that horizontal transmission should at least occasionally (in the ants) or regularly (in most termites) establish genetically variable fungus gardens. In the ants, monocultures are actively enforced because fungal incompatibility compounds hitchhike through the ant guts to be expressed in the feces that fertilize new implants of somatic fungal fragments [14Poulsen M. Boomsma J.J. Mutualistic fungi control crop diversity in fungus-growing ants.Science. 2005; 307: 741-744Crossref PubMed Scopus (136) Google Scholar]. The termites, however, propagate their symbionts within colonies by asexual spores that they embed in newly deposited fecal substrate. This system is therefore expected to produce symbiont monocultures by a combination of genetic drift and selection for rapid spore formation, rather than by active competition via incompatibility compounds [11Aanen D.K. As you reap, so shall you sow: coupling of inoculating and harvesting stabilizes the mutualism between termites and fungi.Biol. Lett. 2006; 2: 209-212Crossref PubMed Scopus (50) Google Scholar, 12Aanen D.K. Boomsma J.J. The evolutionary origin and maintenance of the mutualism between termites and fungi.in: Bourtzis K. Miller T.A. Insect Symbiosis II. CRC Press, Boca Raton2006Crossref Google Scholar]. Can we learn something from the sustainable farming practices of insect societies? The farming insect societies had tens of millions of years of natural selection to solve many of the challenges that are also well known to human farmers. They have conveyor belt substrate processing, produce their own pesticides and antibiotics, and practice active waste management [1Mueller U.G. Gerardo N.M. Aanen D.K. Six D.L. Schultz T.R. The evolution of agriculture in insects.Annu. Rev. Ecol. Evol. Syst. 2005; 36: 563-595Crossref Scopus (404) Google Scholar]. Neither the ants, nor the termites, however, have been able to overcome the fundamental laws of host–symbiont conflicts, which imply that only monoculture farming is evolutionarily stable. Our own farming practices evolved culturally by frequent exchange of crops, learning and copying innovative practices. The problem is that, on the larger scale that we apply today, many of these practices are unlikely to be sustainable, even on an ecological time scale. It may be, therefore, that further research on the long-term evolutionary stable farming systems of the ants and termites may provide useful lessons for our own future food production.