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Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae

Abstract

Cooperation is central to many major transitions in evolution, including the emergence of eukaryotic cells, multicellularity and eusociality1. Cooperation can be destroyed by the spread of cheater mutants that do not cooperate but gain the benefits of cooperation from others1,2. However, cooperation can be preserved if cheaters are facultative, cheating others but cooperating among themselves2. Several cheater mutants have been studied before, but no study has attempted a genome-scale investigation of the genetic opportunities for cheating. Here we describe such a screen in a social amoeba and show that cheating is multifaceted by revealing cheater mutations in well over 100 genes of diverse types. Many of these mutants cheat facultatively, producing more than their fair share of spores in chimaeras, but cooperating normally when clonal. These findings indicate that phenotypically stable cooperative systems may nevertheless harbour genetic conflicts. The opportunities for evolutionary moves and countermoves in such conflicts may select for the involvement of multiple pathways and numerous genes.

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Figure 1: Cheater selection.
Figure 2: Cheating ability and sporulation of isolated mutant strains.
Figure 3: Spatial distribution of cheater and wild-type cells in developing chimaeras.

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Acknowledgements

We thank past and present members of our groups, especially A. Khare, E. Roberge, K. Foster and N. Mehdiabadi, for discussions and for technical assistance; R. H. Kessin for the fbxA- strain and for discussions; and W. F. Loomis for encouragement and advice. This work was supported by a grant from the National Science Foundation; L.A.S. was supported by a Wray–Todd Fellowship. C.R.L.T. was supported by the Wellcome Trust International Prize Traveling Research Fellowship.

Author Contributions L.A.S., C.R.L.T., E.V., J.S. and C.D. conducted the experimental work. A.P. and R.S. performed computational analyses. A.K., C.R.L.T., D.C.Q., G.S. and J.E.S. conceived of the study and wrote the paper. All authors discussed the results and commented on the manuscript.

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Correspondence to Gad Shaulsky.

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The file contains Supplementary Notes; Supplementary Figures 1-5 with Legends; and Supplementary Tables 1-3. (PDF 1005 kb)

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Santorelli, L., Thompson, C., Villegas, E. et al. Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae. Nature 451, 1107–1110 (2008). https://doi.org/10.1038/nature06558

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