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Evolution of an obligate social cheater to a superior cooperator

Abstract

Obligate relationships have evolved many times and can be parasitic or mutualistic. Obligate organisms rely on others to survive and thus coevolve with their host or partner. An important but little explored question is whether obligate status is an evolutionarily terminal condition or whether obligate lineages can evolve back to an autonomous lifestyle. The bacterium Myxococcus xanthus survives starvation by the social development of spore-bearing fruiting bodies. Some M. xanthus genotypes defective at fruiting body development in isolation can nonetheless exploit proficient genotypes in chimaeric groups. Here we report an evolutionary transition from obligate dependence on an altruistic host to an autonomous mode of social cooperation. This restoration of social independence was caused by a single mutation of large effect that confers fitness superiority over both ancestral genotypes, including immunity from exploitation by the ancestral cheater. Thus, a temporary state of obligate cheating served as an evolutionary stepping-stone to a novel state of autonomous social dominance.

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Figure 1: Total spore production, OC-derived sub-population frequencies and developmental population phenotypes during the original six-cycle competition between OC and GJV2.
Figure 2: Pure-culture spore production of strains GJV2, OC and PX.
Figure 3: Log-transformed ratios of PX sporulation efficiency relative to that of GJV2 and OC in direct pairwise competitions at multiple mixing frequencies.
Figure 4: Frequency of PX in direct competition with GJV2 over six cycles of development.
Figure 5: Fruiting morphology effects of the PX-specific mutation.
Figure 6: Developmental expression of the putative acetyltransferase immediately downstream of the PX mutation.

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Acknowledgements

We thank S. Elena, K. Foster, M. Grbic and our laboratory members for discussions and/or comments on the manuscript. We also thank S. Deiss and H. Keller for technical assistance. This work was partially funded by a grant from the Deutsche Forschungsgemeinschaft. Author Contributions F.F. (primarily) and G.J.V. (secondarily) performed population-level experiments, Y.-T.N.Y performed the analysis of mutation function, S.V.K. performed the real-time PCR analysis and all four authors contributed to writing the paper.

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Correspondence to Gregory J. Velicer.

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Fiegna, F., Yu, YT., Kadam, S. et al. Evolution of an obligate social cheater to a superior cooperator. Nature 441, 310–314 (2006). https://doi.org/10.1038/nature04677

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