Experimental evolution of multicellularity via cuboidal cell packing in fission yeast.
The evolution of multicellularity represents a major transition in life's history, enabling the rise of complex organisms. Multicellular groups can evolve through multiple developmental modes, but a common step is the formation of permanent cell-cell attachments after division. The characteristics of the multicellular morphology that emerges have profound consequences for the subsequent evolution of a nascent multicellular lineage, but little prior work has investigated these dynamics directly. Here, we examine a widespread yet understudied emergent multicellular morphology: cuboidal packing. Extinct and extant multicellular organisms across the tree of life have evolved to form groups in which spherical cells divide but remain attached, forming approximately cubic subunits. To experimentally investigate the evolution of cuboidal cell packing, we used settling selection to favor the evolution of simple multicellularity in unicellular, spherical  Schizosaccharomyces pombe  yeast. Multicellular clusters with cuboidal organization rapidly evolved, displacing the unicellular ancestor. These clusters displayed key hallmarks of an evolutionary transition in individuality: groups possess an emergent life cycle driven by physical fracture, group size is heritable, and they respond to group-level selection via multicellular adaptation. In 2 out of 5 lineages, group formation was driven by mutations in the  ace2  gene, preventing daughter cell separation after division. Remarkably,  ace2  mutations also underlie the transition to multicellularity in  Saccharomyces cerevisiae  and  Candida glabrata , lineages that last shared a common ancestor   >   300 million years ago. Our results provide insight into the evolution of cuboidal cell packing, an understudied multicellular morphology, and highlight the deeply convergent potential for a transition to multicellular individuality within fungi.
Pineau RM, Kahn PC, Lac DT, Belpaire TER, Denning MG, Wong W, Ratcliff WC, Bozdag GO