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Primitive agriculture in a social amoeba

Abstract

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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Figure 1: Fruiting body structure and sorus contents from farmer and non-farmer D.discoideum clones.
Figure 2: Farmers readily reassociate with bacteria, suggesting a persistent interaction.
Figure 3: The advantage of carrying food is context dependent.
Figure 4: Life-history traits differ between farmers and non-farmers.

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Acknowledgements

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.

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Contributions

D.A.B. identified the symbiosis, performed the experiments and analysed the data. T.E.D. constructed and analysed the phylogeny. D.A.B., T.E.D., D.C.Q. and J.E.S. designed the experiments, discussed the results and wrote the manuscript.

Corresponding author

Correspondence to Debra A. Brock.

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The authors declare no competing financial interests.

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The file contains Supplementary Figures 1-4 with legends, Supplementary Tables 1-3 and an additional reference. (PDF 465 kb)

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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

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