Agriculture has been a large part of the ecological success of humans1. A handful of animals, notably the fungus-growing ants, termites and ambrosia beetles2,3,4, have advanced agriculture that involves dispersal and seeding of food propagules, cultivation of the crop and sustainable harvesting5. More primitive examples, which could be called husbandry because they involve fewer adaptations, include marine snails farming intertidal fungi6 and damselfish farming algae7. Recent work has shown that microorganisms are surprisingly like animals in having sophisticated behaviours such as cooperation, communication8,9 and recognition10,11, as well as many kinds of symbiosis12,13,14,15. Here we show that the social amoeba Dictyostelium discoideum has a primitive farming symbiosis that includes dispersal and prudent harvesting of the crop. About one-third of wild-collected clones engage in husbandry of bacteria. Instead of consuming all bacteria in their patch, they stop feeding early and incorporate bacteria into their fruiting bodies. They then carry bacteria during spore dispersal and can seed a new food crop, which is a major advantage if edible bacteria are lacking at the new site. However, if they arrive at sites already containing appropriate bacteria, the costs of early feeding cessation are not compensated for, which may account for the dichotomous nature of this farming symbiosis. The striking convergent evolution between bacterial husbandry in social amoebas and fungus farming in social insects makes sense because multigenerational benefits of farming go to already established kin groups.
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Smith, B. D. (ed.) The Emergence of Agriculture (Scientific American Library, Freeman, 1995)
Aanen, D. et al. The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc. Natl Acad. Sci. USA 99, 14887–14892 (2002)
Farrell, B. et al. The evolution of agriculture in beetles (Curculionidae: Scolytinae and Platypodinae). Evolution 55, 2011–2027 (2001)
Mueller, U. G., Schultz, T., Currie, C., Adams, R. & Malloch, D. The origin of the ant-fungus mutualism. Q. Rev. Biol. 76, 169–197 (2001)
Mueller, 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. 36, 563–595 (2005)
Silliman, B. R. & Newell, S. Y. Fungal farming in a snail. Proc. Natl Acad. Sci. USA 100, 15643–15648 (2003)
Hata, H. & Kato, M. A novel obligate cultivation mutualism between damselfish and Polysiphonia algae. Biol. Lett. 2, 593–596 (2006)
Crespi, B. J. The evolution of social behavior in microorganisms. Trends Ecol. Evol. 16, 178–183 (2001)
Keller, L. & Surette, M. G. Communication in bacteria: an ecological and evolutionary perspective. Nature Rev. Microbiol. 4, 249–258 (2006)
Mehdiabadi, N. J. et al. Kin preference in a social amoeba. Nature 442, 881–882 (2006)
Ostrowski, E. A., Katoh, M., Shaulsky, G., Queller, D. C. & Strassmann, J. E. Kin discrimination increases with genetic distance in a social amoeba. PLoS Biol. 6, e287 (2008)
Douglas, A. E. Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera . Annu. Rev. Entomol. 43, 17–37 (1998)
Moran, N. A., Dunbar, H. E. & Wilcox, J. L. Regulation of transcription in a reduced bacterial genome: nutrient-provisioning genes of the obligate symbiont Buchnera aphidicola. J. Bacteriol. 187, 4229–4237 (2005)
Bäckhed, F., Ley, R. E., Sonnenburg, J. L., Peterson, D. A. & Gordon, J. I. Host-bacterial mutualism in the human intestine. Science 307, 1915–1920 (2005)
Sears, C. L. A dynamic partnership: celebrating our gut flora. Anaerobe 11, 247–251 (2005)
Raper, K. B. The Dictyostelids 87–177 (Princeton Univ. Press, 1984)
Kessin, R. H. Dictyostelium: Evolution, Cell Biology, and the Development of Multicellularity (Cambridge Univ. Press, 2001)
Raper, K. B. Growth and development of Dictyostelium discoideum with different bacterial associates. J. Agric. Res. 55, 289–316 (1937)
Matz, C. & Kjelleberg, S. Off the hook - how bacteria survive protozoan grazing. Trends Microbiol. 13, 302–307 (2005)
Nadson, G. A. Des cultures du Dictyostelium mucoroides Bref. et des cultures pures des amibes en general. Scripta Bot. Horti Univ. Imp. Petropolitanae 15, 188–190 (1899)
Skupienski, F. X. Recherches sur le Cycle Evolutif de Certains Myxomycetes. PhD thesis, l’Universite de Paris. (1920)
Flowers, J. M. et al. Variation, sex, and social cooperation: molecular population genetics of the social amoeba Dictyostelium discoideum . PLoS Genet. 6, e1001013 (2010)
Clark, F. in Soil Biology (eds Burges, A. & Raw, F. ) Ch. 2, 15–49 (Academic, 1967)
Heijnen, C. E., Burgers, S. & Vanveen, J. A. Metabolic activity and population dynamics of rhizobia introduced into unamended and bentonite-amended loamy sand. Appl. Environ. Microbiol. 59, 743–747 (1993)
Horn, E. G. Food competition among the cellular slime molds (Acrasiae). Ecology 52, 475–484 (1971)
Foster, K. R., Shaulsky, G., Strassmann, J. E., Queller, D. C. & Thompson, C. R. L. Pleiotropy as a mechanism to stabilize cooperation. Nature 431, 693–696 (2004)
Gilbert, O. M., Foster, K. R., Mehdiabadi, N. J., Strassmann, J. E. & Queller, D. C. High relatedness maintains multicellular cooperation in a social amoeba by controlling cheater mutants. Proc. Natl Acad. Sci. USA 104, 8913–8917 (2007)
Santorelli, L. A. et al. Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae. Nature 451, 1107–1110 (2008)
Benabentos, R. et al. Polymorphic members of the lag gene family mediate kin discrimination in Dictyostelium . Curr. Biol. 19, 567–572 (2009)
Fortunato, A., Strassmann, J. E., Santorelli, L. & Queller, D. C. Co-occurrence in nature of different clones of the social amoeba, Dictyostelium discoideum. Mol. Ecol. 12, 1031–1038 (2003)
Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001)
Tamura, K., Dudley, J., Nei, M. & Kumar, S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596–1599 (2007)
We thank J. Rudgers, G. Saxer Quance, L. Campbell, E. Ostrowski, O. Gilbert, A. Savage, J. Ahern, K. Crawford, S. Chamberlain, S. Read, D. Nguyen, K. Foster, H. Kaplan, D. Hatton and K. Boomsma for discussions and advice. This material is based on work supported by the US National Science Foundation.
The authors declare no competing financial interests.
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Brock, D., Douglas, T., Queller, D. et al. Primitive agriculture in a social amoeba. Nature 469, 393–396 (2011). https://doi.org/10.1038/nature09668