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

• Published in: Nature Vol. 451; no. 7182; pp. 1107 - 1110
• Main Authors: Shaulsky, Gad, Santorelli, Lorenzo A, Thompson, Christopher R. L, Villegas, Elizabeth, Svetz, Jessica, Dinh, Christopher, Parikh, Anup, Sucgang, Richard, Kuspa, Adam, Strassmann, Joan E, Queller, David C
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 28-02-2008; Nature Publishing; Nature Publishing Group
• Subjects: Amoeba; Amoeba - genetics; Amoeba - physiology; Animal ethology; Animals; Biological and medical sciences; Cell Aggregation; Cellular biology; Chimera - genetics; Chimera - physiology; Cooperation; Cooperative Behavior; Dictyostelium - cytology; Dictyostelium - genetics; Dictyostelium - physiology; Evolutionary biology; Fundamental and applied biological sciences. Psychology; General aspects; General aspects and techniques; Genes, Protozoan - genetics; Genome - genetics; Genomics; Humanities and Social Sciences; letter; Microorganisms; multidisciplinary; Mutants; Mutation; Mutation - genetics; Myxococcus xanthus - genetics; Myxococcus xanthus - physiology; Phenotype; Protozoa; Psychology. Psychoanalysis. Psychiatry; Science; Science (multidisciplinary); Social Behavior; Spores, Protozoan - genetics; Spores, Protozoan - physiology; Protozoa; Eusociality; Dictyostelium discoideum; Case study; Myxococcales; Cheating; Social interaction; Myxococcus xanthus; Cooperation; Bacteria; Genetics; Myxococcaceae; Mutation; Mycetozoa
• ISSN: 0028-0836; 1476-4687; 1476-4679
• DOI: 10.1038/nature06558

Cooperation is central to many major transitions in evolution, including the emergence of eukaryotic cells, multicellularity and eusociality. Cooperation can be destroyed by the spread of cheater mutants that do not cooperate but gain the benefits of cooperation from others. However, cooperation can be preserved if cheaters are facultative, cheating others but cooperating among themselves. 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.