Experimental evolution of multicellularity via cuboidal cell packing in fission yeast.

IF 3.4 1区 生物学 Q2 EVOLUTIONARY BIOLOGY Evolution Letters Pub Date : 2024-06-14 eCollection Date: 2024-10-01 DOI:10.1093/evlett/qrae024
Rozenn M Pineau, Penelope C Kahn, Dung T Lac, Tom E R Belpaire, Mia G Denning, Whitney Wong, William C Ratcliff, G Ozan Bozdag
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引用次数: 0

Abstract

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.

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来源期刊
Evolution Letters
Evolution Letters EVOLUTIONARY BIOLOGY-
CiteScore
13.00
自引率
2.00%
发文量
35
审稿时长
10 weeks
期刊介绍: Evolution Letters publishes cutting-edge new research in all areas of Evolutionary Biology. Available exclusively online, and entirely open access, Evolution Letters consists of Letters - original pieces of research which form the bulk of papers - and Comments and Opinion - a forum for highlighting timely new research ideas for the evolutionary community.
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