The functions of symbionts in natural populations can be difficult to completely discern. The three
Paraburkholderia
bacterial farming symbionts of the social amoeba
Dictyostelium discoideum
have been shown in the laboratory environment to allow the amoebas to carry, rather than fully digest, food bacteria.
During the evolution of multicellularity, cells undergo an evolutionary transition in individuality, such that groups become the subject of Darwinian evolution. Comparative work, supported by theory, suggests that a life cycle in which cells 'stay together' following cellular division (termed clonal development) should facilitate this transition. While central to our understanding of multicellular evolution, this hypothesis has never been directly tested in a single experimental system. We circumvent this limitation by creating an isogenic yeast system capable of either clonal or aggregative development. We evolved 20 populations of either clonally-reproducing 'snowflake' yeast or aggregative 'floc' yeast with daily selection for rapid growth followed by sedimentation, an environment where multicellularity is adaptive. While both genotypes adapted to this regime, growing faster and having higher survival during the group-selection phase, there was a stark difference in evolutionary dynamics. Competitions reveal that evolved floc obtained nearly all of their increased fitness from faster growth, not improved group survival, while snowflake yeast mainly benefited from higher group-dependent fitness. Through a combination of genome sequencing and mathematical modeling, we identify a trade-off: clonal development can allow selection to act more efficiently on group-beneficial traits, but dramatically increases the overall rate of genetic drift due to mutational bottlenecking. Our results demonstrate how simple differences in the mode of group formation can have profound impacts on the transition to multicellularity: clonal development, but not aggregation, precipitated a transition from cells to groups as the primary level of Darwinian individuality.
The relationship between the social amoeba Dictyostelium discoideum and its endosymbiotic bacteria Paraburkholderia provides a model system for studying the development of symbiotic relationships. Laboratory experiments have shown that any of three species of Paraburkholderia symbiont allow D. discoideum food bacteria to persist through the amoeba lifecycle and survive in amoeba spores, rather than being fully digested. This phenomenon is termed "farming", as it potentially allows spores dispersed to food poor locations to grow their own. The occurrence and impact of farming in natural populations, however, has been a challenge to measure. Here, we surveyed natural D. discoideum populations and found that only one of the three symbiont species, P. agricolaris, remained prevalent. We then explored the effect of Paraburkholdia on the amoeba microbiome, expecting that by facilitating bacterial food carriage it would diversify the microbiome. Contrary to our expectations, Paraburkholderia tended to infectiously dominate the D. discoideum microbiome, in some cases decreasing diversity. Similarly, we found little evidence for Paraburkholderia facilitating the carriage of particular food bacteria. These findings change our understanding of farming and suggest the possibility that Paraburkholderia could be playing multiple roles for its host, as inferred metagenomic analysis indicates a potential role of P. agricolaris in toxin degradation.
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