Evolutionary consequences of nascent multicellular life cycles

Pentz, Jennifer; MacGillivray, Kathryn A.; DuBose, James G.; Conlin, Peter L.; Reinhardt, Emma M.; Libby, Eric; Ratcliff, William C.

doi:10.1101/2022.07.21.500805

Cited by 4 publications

(4 citation statements)

References 89 publications

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“…All extant lineages of complex multicellularity develop clonally, rather than through aggregation of unrelated cells. This is well-explained by evolutionary theory as a key trait facilitating multicellular adaptation and cellular specialization (10). Clonal multicellularity, however, greatly reduces Ne.…”

Section: Resultsmentioning

confidence: 96%

A non-adaptive explanation for macroevolutionary patterns in the evolution of complex multicellularity

Bingham,

Ratcliff

2023

Preprint

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Abstract“Complex multicellularity”, conventionally defined as large organisms with many specialized cell types, has evolved five times independently in eukaryotes, but never within prokaryotes. A number hypotheses have been proposed to explain this phenomenon, most of which posit that eukaryotes evolved key traits (e.g., dynamic cytoskeletons, alternative mechanisms of gene regulation, or subcellular compartments) which were a necessary prerequisite for the evolution of complex multicellularity. Here we propose an alternative, non-adaptive hypothesis for this broad macroevolutionary pattern. By binning cells into groups with finite genetic bottlenecks between generations, the evolution of multicellularity greatly reduces the effective population size (Ne) of cellular populations, increasing the role of genetic drift in evolutionary change. While both prokaryotes and eukaryotes experience this phenomenon, they have opposite responses to drift: mutational biases in eukaryotes tend to drive genomic expansion, providing additional raw genetic material for subsequent multicellular innovation, while prokaryotes generally face genomic erosion. These effects become more severe as organisms evolve larger size and more stringent genetic bottlenecks between generations— both of which are hallmarks of complex multicellularity. Taken together, we hypothesize that it is these idiosyncratic lineagespecific mutational biases, rather than cell-biological innovations within eukaryotes, that underpins the long-term divergent evolution of complex multicellularity across the tree of life.

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Section: Resultsmentioning

confidence: 96%

A non-adaptive explanation for macroevolutionary patterns in the evolution of complex multicellularity

Bingham,

Ratcliff

2023

Preprint

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“…Aggregative multicellularity comes with a well-known evolutionary challenge: one aggregate can combine cells of different ancestries and potentially different genotypes, thus raising the possibility of conflict (113)(114)(115). Aggregates are notably vulnerable to cheater genotypes, which reap the benefits of multicellularity without contributing their fair share of the cost of multicellular development.…”

Section: Evolutionary Implications Of Mixed Clonal-aggregative Multic...mentioning

confidence: 99%

Mixed clonal-aggregative multicellularity entrained by extreme salinity fluctuations in a close relative of animals

Ros-Rocher,

Reyes-Rivera,

Foroughijabbari

et al. 2024

Preprint

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Multicellularity evolved multiple times independently during eukaryotic diversification. Two distinct mechanisms underpin multicellularity: clonal development (serial cell division of a single precursor cell) and aggregation (in which independent cells assemble into a multicellular entity). Clonal and aggregative development are traditionally considered to be mutually exclusive and to result from independent acquisitions of multicellularity. Here, we show that the choanoflagellate Choanoeca flexa, a close relative of animals that forms contractile monolayers of cells (or "sheet colonies"), develops by an unconventional intermediate mechanism that we name "clonal-aggregative multicellularity". We find that C. flexa sheets can form through purely clonal processes, purely aggregative processes, or a combination of both, depending on experimental conditions. To assess the ecological relevance of these findings, we characterize the natural context of multicellular development in the native environment of C. flexa on the island of Curaçao. We show that the C. flexa life cycle is environmentally regulated by extreme salinity fluctuations in splash pools undergoing cycles of evaporation and refilling. Upon desiccation, C. flexa colonies dissociate into drought-resistant quiescent cells, which resume activity and reform multicellular sheets after rehydration. We hypothesize that clonal-aggregative development reflects selection for fast transitions into and out of multicellularity in the ephemeral context of coastal splash pools. Our findings underscore the potential of the exploration of biodiversity to reveal new fundamental biological phenomena and expand the known option space for both multicellular development and for the origin of animal multicellularity.

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“…Similarly, the morphology of multicellular groups is heavily dependent on the traits of the unicellular ancestor. How cells divide and attach to one another has fundamental consequences for the biophysical properties and evolutionary dynamics of these lineages 8,9 .…”

Section: Introductionmentioning

confidence: 99%

Experimental evolution of multicellularity via cuboidal cell packing in fission yeast

Pineau,

Kahn,

Lac

et al. 2023

Preprint

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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 which emerges has profound consequences for the subsequent evolution of a nascent multicellular lineage, but little prior work has examined 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, sphericalSchizosaccharomyces pombeyeast. 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 2/5 lineages, group formation was driven by mutations in theACE2gene, preventing daughter cell separation after division. Remarkably,ACE2mutations also underlie the transition to multicellularity inSaccharomyces cerevisiaeandC. galabrata, lineages 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 highlights the deeply convergent potential for a transition to multicellular individuality within fungi.

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Evolutionary consequences of nascent multicellular life cycles

Cited by 4 publications

References 89 publications

A non-adaptive explanation for macroevolutionary patterns in the evolution of complex multicellularity

A non-adaptive explanation for macroevolutionary patterns in the evolution of complex multicellularity

Mixed clonal-aggregative multicellularity entrained by extreme salinity fluctuations in a close relative of animals

Experimental evolution of multicellularity via cuboidal cell packing in fission yeast

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