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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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Toward open-ended fraternal transitions in individuality
The emergence of new replicating entities from the union of simpler entities characterizes some of the most profound events in natural evolutionary history. Such transitions in individuality are essential to the evolution of the most complex forms of life. Thus, understanding these transitions is critical to building artificial systems capable of open-ended evolution. Alas, these transitions are challenging to induce or detect, even with computational organisms. Here, we introduce the DISHTINY (Distributed Hierarchical Transitions in Individuality) platform, which provides simple cell-like organisms with the ability and incentive to unite into new individuals in a manner that can continue to scale to subsequent transitions. The system is designed to encourage these transitions so that they can be studied: Organisms that coordinate spatiotemporally can maximize the rate of resource harvest, which is closely linked to their reproductive ability. We demonstrate the hierarchical emergence of multiple levels of individuality among simple cell-like organisms that evolve parameters for manually designed strategies. During evolution, we observe reproductive division of labor and close cooperation among cells, including resource-sharing, aggregation of resource endowments for propagules, and emergence of an apoptosis response to somatic mutation. Many replicate populations evolved to direct their resources toward low-level groups (behaving like multicellular individuals), and many others evolved to direct their resources toward high-level groups (acting as larger-scale multicellular individuals).
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- Award ID(s):
- 1655715
- PAR ID:
- 10104637
- Date Published:
- Journal Name:
- Artificial life
- Volume:
- 25
- Issue:
- 2
- ISSN:
- 1064-5462
- Page Range / eLocation ID:
- 117-133
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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