1. Department of Ecology and Evolutionary Biology, Rice University, Houston, Texas 77005, USA
2. Department of Molecular and Human Genetics,
3. Department of Biochemistry and Molecular Biology,
4. Graduate Program in Structural Computational Biology and Molecular Biophysics, Baylor College of Medicine, Houston, Texas 77030, USA
5. Present address: Faculty of Life Sciences, Michael Smith Building, University of Manchester, Manchester M13 9PT, UK.

Correspondence to: Gad Shaulsky^1,2,4 Correspondence and requests for materials should be addressed to G.S. (Email: gadi@bcm.tmc.edu).

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 others^{1, 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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