Abstract
Studies of social microbes often focus on one fitness component (reproductive success within the social complex), with little information about or attention to other stages of the life cycle or the ecological context. This can lead to paradoxical results. The life cycle of the social amoeba Dictyostelium discoideum includes a multicellular stage in which not necessarily clonal amoebae aggregate upon starvation to form a possibly chimeric (genetically heterogeneous) fruiting body made of dead stalk cells and spores. The lab-measured reproductive skew in the spores of chimeras indicates strong social antagonism that should result in low genotypic diversity, which is inconsistent with observations from nature. Two studies have suggested that this inconsistency stems from the one-dimensional assessment of fitness (spore production) and that the solution lies in tradeoffs between multiple life-history traits, e.g.: spore size versus viability; and spore-formation (via aggregation) versus staying vegetative (as non-aggregated cells). We develop an ecologically-grounded, socially-neutral model (i.e. no social interactions between genotypes) for the life cycle of social amoebae in which we theoretically explore multiple non-social life-history traits, tradeoffs and tradeoff-implementing mechanisms. We find that spore production comes at the expense of time to complete aggregation, and, depending on the experimental setup, spore size and viability. Furthermore, experimental results regarding apparent social interactions within chimeric mixes can be qualitatively recapitulated under this neutral hypothesis, without needing to invoke social interactions. This allows for simple potential resolutions to the previously paradoxical results. We conclude that the complexities of life histories, including social behavior and multicellularity, can only be understood in the appropriate multidimensional ecological context, when considering all stages of the life cycle.
Highlights
The cellular slime mold Dictyostelium discoideum is one of the most studied examples of cooperation and altruism in microbes
Fitness in social microbes is often measured in terms of reproductive success in the social stage, with little regard to other stages of the life cycle or to the ecological context
This approach can lead to seemingly paradoxical results that point to complex
Summary
The cellular slime mold Dictyostelium discoideum is one of the most studied examples of cooperation and altruism in microbes. In the process of aggregation these amoebae do not exclude non-kin; chimeras (multicellular fruiting bodies consisting of at least two genotypes) have been observed both in the lab and in nature [5,6,7,8] These chimeras are functional: the multiple genotypes participate both in stalk formation and in spore production ( not necessarily in equal measures, a phenomenon known as reproductive skew [6]). Studies to date have found significant reproductive skew in D. discoideum chimeras [9,10] and in a variety of other cellular slime molds [11] This was interpreted as a sign of social conflict and strains that were over-represented in the spores were seen as socially dominant [9,10]. The experimentally uncovered dominance relationships seemed to point towards a decrease in species-wide genetic diversity that was inconsistent with the immense diversity and coexistence observed among strains in nature [5,8,9,11]
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