Cryptic multicellularity in wild yeast brings selective advantages under stress

Abstract

Multicellularity has evolved dozens of times in many branches across the Tree of Life, in each case producing a new kind of individual that has the potential for division of labor among its constituent cells. In many of these instances, nascent multicellularity has remained facultative, manifesting only under conditions where it provides a decisive fitness advantage to the genome in which it has arisen. Here we investigate the mechanistic basis for, and the selective advantages of, cryptic multicellularity in wild strains of the yeast Saccharomyces cerevisiae. Meiotic purification of this trait, followed by genome sequencing, indicates that the genome of diploid champagne yeast DB146 is homozygous at the AMN1 locus (Antagonist of Mitotic exit Network) for an allele that dysregulates post-mitotic cell separation. Expression of this trait in haploid derivatives of DB146 results in clonal multicellular clusters in which daughters remain attached to mother cell walls. Systematic analysis of viability in haploid and diploid DB146 derivatives subjected to benign conditions as well as to starvation, desiccation, and low temperature at different cell titers demonstrates that haploid multicellular variants exhibit higher survivorship under conditions that wild yeast likely experience when they overwinter. Examining a collection of other wild strains, we find that [~]20% exhibit ploidy-dependent expression of clonal multicellularity. Altogether, our data suggest that in yeast that sporulate when starved, cryptic multicellularity may come under balancing selection because haploid multicellular progeny enjoy a transient survival advantage that fades once favorable growth conditions resume.