Bingham, E. P. | Search bioRxiv

bioRxiv2023

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

"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.

evolutionary biology↗

bioRxiv2023

Entanglement in living systems

Many organisms exhibit branching morphologies that twist around each other and become entangled. Entanglement occurs when different objects interlock with each other, creating complex and often irreversible configurations. This physical phenomenon is well-studied in non-living materials, such as granular matter, polymers, and wires, where it has been shown that entanglement is highly sensitive to the geometry of the component parts. However, entanglement is not yet well understood in living systems, despite its presence in many organisms. In fact, recent work has shown that entanglement can evolve rapidly, and play a crucial role in the evolution of tough, macroscopic multicellular groups. Here, through a combination of experiments, simulations, and numerical analyses, we show that growth generically facilitates entanglement for a broad range of geometries. We find that experimentally grown entangled branches can be difficult or even impossible to disassemble through translation and rotation of rigid components, suggesting that there are many configurations of branches that growth can access that agitation cannot. We use simulations to show that branching trees readily grow into entangled configurations. In contrast to non-growing entangled materials, these trees entangle for a broad range of branch geometries. We thus propose that entanglement via growth is largely insensitive to the geometry of branched-trees, but instead will depend sensitively on time scales, ultimately achieving an entangled state once sufficient growth has occurred. We test this hypothesis in experiments with snowflake yeast, a model system of undifferentiated, branched multicellularity, showing that lengthening the time of growth leads to entanglement, and that entanglement via growth can occur for a wide range of geometries. Taken together, our work demonstrates that entanglement is more readily achieved in living systems than in their non-living counterparts, providing a widely-accessible and powerful mechanism for the evolution of novel biological material properties.

biophysics↗