Synergistic cooperation promotes multicellular performance and unicellular free-rider persistence

• Published in: Nature communications Vol. 8; no. 1; p. 15707
• Main Authors: Driscoll, William W, Travisano, Michael
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 05.06.2017; Nature Publishing Group; Nature Portfolio
• Subjects: 14/63; 631/158/855; 631/158/857; 631/181/2469; 631/181/2475; Biological Evolution; Cluster Analysis; Cooperation; Ecology; Evolution; Flocculation; Genotype; Green Fluorescent Proteins - metabolism; Humanities and Social Sciences; Kluyveromyces - genetics; Kluyveromyces - physiology; Microscopy, Confocal; multidisciplinary; Phenotype; Saccharomyces cerevisiae - genetics; Saccharomyces cerevisiae - physiology; Science; Science (multidisciplinary); Species Specificity; Yeast; United States > US; Minnesota
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/ncomms15707

The evolution of multicellular life requires cooperation among cells, which can be undermined by intra-group selection for selfishness. Theory predicts that selection to avoid non-cooperators limits social interactions among non-relatives, yet previous evolution experiments suggest that intra-group conflict is an outcome, rather than a driver, of incipient multicellular life cycles. Here we report the evolution of multicellularity via two distinct mechanisms of group formation in the unicellular budding yeast Kluyveromyces lactis . Cells remain permanently attached following mitosis, giving rise to clonal clusters (staying together); clusters then reversibly assemble into social groups (coming together). Coming together amplifies the benefits of multicellularity and allows social clusters to collectively outperform solitary clusters. However, cooperation among non-relatives also permits fast-growing unicellular lineages to ‘free-ride’ during selection for increased size. Cooperation and competition for the benefits of multicellularity promote the stable coexistence of unicellular and multicellular genotypes, underscoring the importance of social and ecological context during the transition to multicellularity. Multicellularity can arise by cells aggregating or remaining connected after cell division. Here, Driscoll and Travisano show that both mechanisms operate in experimentally evolved strains of the yeast Kluyveromyces lactis , with transient aggregation facilitating the coexistence of unicellular and multicellular genotypes.