Primitive agriculture in a social amoeba

• Published in: Nature (London) Vol. 469; no. 7330; pp. 393 - 396
• Main Authors: Brock, Debra A., Douglas, Tracy E., Queller, David C., Strassmann, Joan E.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 20.01.2011; Nature Publishing Group
• Subjects: 631/181; 631/326/2565/547; Agriculture; Algae; Amoeba; Animal and plant ecology; Animal, plant and microbial ecology; Animals; Antibiotics; Autoecology; Bacteria; Bacteria - growth & development; Bacteria - isolation & purification; Bacteria - metabolism; Biological and medical sciences; Biological Evolution; Crops; Dictyostelium - cytology; Dictyostelium - microbiology; Dictyostelium - physiology; Dictyostelium discoideum; E coli; Farmers; Farming; Feeding Behavior - physiology; Food and nutrition; Formicidae; Fundamental and applied biological sciences. Psychology; Genetic aspects; Harvesting; Humanities and Social Sciences; Identification and classification; Isoptera; letter; Marine; Microbiology; Microorganisms; multidisciplinary; Observations; Protozoa. Invertebrata; Reproduction - physiology; Science; Science (multidisciplinary); Seed dispersal; Social Behavior; Spores - physiology; Sustainable harvest; Symbiosis; United States; Dictyostelium discoideum; Symbiosis; Protozoa; Animal microorganism relation; Environmental factor; Bacteria; Rearing; Intraspecific comparison; Food supply; Mycetozoa
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature09668

First steps in farming The success of our species has been in part because of our use of agriculture, but it is not a uniquely human occupation. Some social insects — such as fungus-growing ants and ambrosia beetles — have developed quite sophisticated cultivation and harvesting routines. A more modest form of fungal husbandry has been adopted by marine snails, but it comes as something as a surprise to discover a primitive form of agriculture in the soil-dwelling social amoeba Dictyostelium discoideum , familiarly known as slime mould. About one-third of D. discoideum clones isolated from the wild refrain from consuming all the available bacteria at a site, instead incorporating them into their reproductive assemblages. This 'harvest' is carried by the spores during dispersal and serves to seed a new bacterial crop at their next location. The connection between farming and sociality — in humans, insects and these symbiotic microbes — may be more than a coincidence since the multigenerational benefits generated are enjoyed by already established kin groups. Agriculture has been central to the success of humans and some social insects. This paper shows that social amoebae can do it too. Some isolates of Dictyostelium discoideum refrain from consuming all the available bacteria at a site and instead they incorporate them into their reproductive assemblages to seed a new bacterial crop at another location. Agriculture has been a large part of the ecological success of humans 1 . A handful of animals, notably the fungus-growing ants, termites and ambrosia beetles 2 , 3 , 4 , have advanced agriculture that involves dispersal and seeding of food propagules, cultivation of the crop and sustainable harvesting 5 . More primitive examples, which could be called husbandry because they involve fewer adaptations, include marine snails farming intertidal fungi 6 and damselfish farming algae 7 . Recent work has shown that microorganisms are surprisingly like animals in having sophisticated behaviours such as cooperation, communication 8 , 9 and recognition 10 , 11 , as well as many kinds of symbiosis 12 , 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.