In Saccharomyces cerevisiae, the FLO1 gene encodes flocculins that lead to formation of multicellular flocs, that offer protection to the constituent cells. Flo1p was found to preferentially bind to fellow cooperators compared to defectors lacking FLO1 expression, enriching cooperators within the flocs. Given this dual function in cooperation and kin recognition, FLO1 has been termed a “green beard gene”. Because of the heterophilic nature of the Flo1p bond however, we hypothesize that kin recognition is permissive and depends on the relative stability of the FLO1+/flo1− versus FLO1+/FLO1+ detachment force F. We combine single-cell measurements of adhesion, individual cell-based simulations of cluster formation, and in vitro flocculation to study the impact of relative bond stability on the evolutionary stability of cooperation. We identify a trade-off between both aspects of the green beard mechanism, with reduced relative bond stability leading to increased kin recognition at the expense of cooperative benefits. We show that the fitness of FLO1 cooperators decreases as their frequency in the population increases, arising from the observed permissive character (F+− = 0.5 F++) of the Flo1p bond. Considering the costs associated with FLO1 expression, this asymmetric selection often results in a stable coexistence between cooperators and defectors.
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Data from the single-cell force spectroscopy and flocculation assay have been made available. The simulation code and framework have been made publicly available at https://doi.org/10.5281/zenodo.6472861.
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The authors thank Karin Voordeckers for providing us with the yeast strains; Carmen Bartic and Olivier Deschaume for expertise and support with the SCFS experiments. This work was supported by the KU Leuven Research Fund (CELSA/18/031,C24/18/046). B.S. acknowledges support from the Research Foundation Flanders (FWO) grant 12Z6118N. Research in the lab of K.J.V. is supported by KU Leuven, Vlaams Instituut voor Biotechnologie (VIB) and FWO.
This work was supported by the KU Leuven Research Fund (CELSA/18/031, C24/18/046). BS acknowledges support from the Research Foundation Flanders (FWO) grant 12Z6118N. Research in the lab of KJV is supported by KU Leuven, Vlaams Instituut voor Biotechnologie (VIB) and FWO.
The author declares no competing interests.
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Belpaire, T.E.R., Pešek, J., Lories, B. et al. Permissive aggregative group formation favors coexistence between cooperators and defectors in yeast. ISME J (2022). https://doi.org/10.1038/s41396-022-01275-y