Fitness tradeoffs between spores and nonaggregating cells can explain the coexistence of diverse genotypes in cellular slime molds

• Published in: Proceedings of the National Academy of Sciences - PNAS 2015-03, Vol.112 (9), p.2776-2781
• Main Authors: Tarnita, Corina E., Washburne, Alex, Martinez-Garcia, Ricardo, Sgro, Allyson E., Levin, Simon A.
• Format: Article
• Language: English
• Subjects: Biological Sciences; Cells; Coexistence; Dictyostelium - physiology; Dispersal; Ecosystem; Environmental conditions; Genetic diversity; Genotype & phenotype; Genotypes; Life Cycle Stages - physiology; Mold; Molds & molding; Slime; Spores, Protozoan - physiology
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1424242112

Significance Cellular slime molds, including Dictyostelium discoideum , are amoebae whose life cycle includes both single-cellular and multicellular stages, the latter achieved when individual amoebae aggregate upon starvation. In the (not necessarily clonal) aggregate, there is strong selection to be represented in the reproductive spores. This would lead to a reduction in overall genotypic diversity inconsistent with the great diversity found in nature. We suggest that cells that fail to aggregate provide an additional fitness component that can resolve the inconsistency: Strong selection for aggregation only occurs in environments where food is slow to replenish. Otherwise, there is strong selection for unicellularity. These tradeoffs allow a multitude of genotypes to coexist when many environments with different food-recovery characteristics are connected via weak-to-moderate dispersal. Cellular slime molds, including the well-studied Dictyostelium discoideum , are amoebae whose life cycle includes both a single-cellular and a multicellular stage. To achieve the multicellular stage, individual amoebae aggregate upon starvation to form a fruiting body made of dead stalk cells and reproductive spores, a process that has been described in terms of cooperation and altruism. When amoebae aggregate they do not perfectly discriminate against nonkin, leading to chimeric fruiting bodies. Within chimeras, complex interactions among genotypes have been documented, which should theoretically reduce genetic diversity. This is however inconsistent with the great diversity of genotypes found in nature. Recent work has shown that a little-studied component of D. discoideum fitness—the loner cells that do not participate in the aggregation—can be selected for depending on environmental conditions and that, together with the spores, they could represent a bet-hedging strategy. We suggest that in all cellular slime molds the existence of loners could resolve the apparent diversity paradox in two ways. First, if loners are accounted for, then apparent genotypic skew in the spores of chimeras could simply be the result of different investments into spores versus loners. Second, in an ecosystem with multiple local environments differing in their food recovery characteristics and connected globally via weak-to-moderate dispersal, coexistence of multiple genotypes can occur. Finally, we argue that the loners make it impossible to define altruistic behavior, winners or losers,