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2. THE SOCIAL AMOEBA D. DISCOIDEUM

Dictyostelium discoideum is an organism that has been intriguing biologists for most of this century. Although this organism is often called a "cellular slime mold", it is not a mold and it is not consistently slimy. A better common name for it is a "social amoeba". What is most remarkable about the organism is its life cycle. In one part of it life cycle, the "organism" consists of individual dispersed amoebas living on decaying logs, eating bacteria and reproducing by binary fission like most other protozoans. Then, when the local food supply becomes exhausted, a rather astounding event occurs: tens of thousands of these amoeba join together to form moving streams of cells that converge at a central point, and there they aggregate to produce a slug (grex) 2 to 4 millimeters long. The slug migrates as a single body towards light, and when it reaches an illuminated area, migration ceases, and the slug differentiates into a fruiting body composed of spore cells and a stalk, the stalk rising approximately 1 centimeter high above the plane of the surface on which the slug has migrated. Inside the globular end of the fruiting body, each spore cell is cellulose encapsulated. In the denouement, the stalk cells die and the spore cells are widely dispersed to become new amoeba, each of which will begin a separate new population of cells both individual and social. Thus, in this organism, initially identical cells are differentiated into one of two alternative cell types, spore cells and stalk cells. It is an organism where individual cells come together to form a cohesive structure, aggregating into a single organism, a quite remarkable feat of organization that challenges biologists, chemists, and physicists. Much has been learned about this organism in the past few decades, in particular the apparent important role of release of cyclic adenosine monophosphate (cAMP) in the initial aggregation that produces the slug.

SINGLE-GENE GREENBEARD EFFECTS IN THE SOCIAL AMOEBA DICTYOSTELIUM DISCOIDEUM

D.C. Queller et al (Rice University, US) discuss social amoeba, the authors making the following points:

1) Selection can favor an allele that causes self-sacrifice if it enhances the fitness of others who bear the allele (1). Generally, individuals recognize other bearers -- relatives -- by some combination of social context and learning (2). Alternatively, alleles might directly recognize copies of themselves, regardless of average relatedness (3). These so-called "greenbeard alleles", the term originally coined by Dawkins (4), are generally thought to be rare because they must cause a complex of three effects: a perceptible trait (the hypothetical green beard), recognition of this trait in others, and preferential treatment of those recognized (3,4). The few known examples -- poison-antidote systems like bacteriocins (5) and the fire ant gp9 locus --involve or are thought to involve multiple tightly linked genes. However, it has been suggested that a single homophilic cell adhesion gene could cause all three effects.

2) The authors demonstrate that the adhesion gene hypothesis is appropriate for the csA (contact site A) gene of the slime mold, Dictyostelium discoideum. D. discoideum is a highly social eukaryotic microorganism. Most of the time, the single-celled amoebae forage for bacteria in the forest soil. The social phase occurs only when the food runs out. Amoebae use a cyclic AMP signal relay to stream into an aggregation of thousands of cells. Roughly 20% of the cells altruistically die in the process of forming a long rigid stalk that supports the other cells, which differentiate into a cluster of spores. Cells from different clones readily form chimeric fruiting bodies in the laboratory, and they probably do so in the field, as judged from the fact that 19 of 26 small field soil samples containing D. discoideum had multiple clones.

3) The csA gene encodes a cell adhesion protein anchored in the cell membrane. The most distal globular domain, with some homology to the immunoglobulin domain, interacts by homophilic binding to the identical domain of gp80 proteins anchored in other cells. The effects of the csA gene have been explored with a knockout mutant lacking functional gp80 protein. There are two pertinent effects, one a greenbeard effect and another with the opposite effect. The greenbeard effect has been shown in studies in which equal mixtures of wild-type and knockout cells were developed on soil plates. Spores from the resulting chimeric fruiting bodies were 82% wild type, because their homophilic binding allowed them to adhere in aggregation streams and to pull each other into aggregates, whereas most knockout cells were left behind.

4) In summary: Selection can favor reproductive altruism if an altruism allele aids copies of itself by helping relatives. The alternative "greenbeard" mechanism, in which an allele directly recognizes and aids copies of itself in others, is generally thought to be too complex for a single gene to carry out. The csA gene in Dictyostelium discoideum acts as a single-gene greenbeard. When wild-type cells are mixed with csA-knockout cells, the wild type is more altruistic, but is also able preferentially to direct the benefits to other wild-type cells. Both properties derive directly from homophilic cell adhesion of the protein encoded by csA.

References (abridged):

1. W. D. Hamilton, J. Theor. Biol. 7, 1 (1964)

2. R. D. Alexander, Darwinism and Human Affairs (Univ. of Washington, Seattle, WA, 1979).

3. W. D. Hamilton, J. Theor. Biol. 7, 17 (1964)

4. R. Dawkins, The Selfish Gene (Oxford Univ. Press, Oxford, 1976)

5. D. Haig, in Behavioral Ecology: An Evolutionary Approach, J. R. Krebs, N. B. Davies, Eds. (Blackwell, Oxford, ed. 4, 1996), pp. 284-304

Science 2003 299:105

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