Cellular organization in lab-evolved and extant multicellular species obeys a maximum entropy law
Thomas C Day, Stephanie S Höhn, Seyed A Zamani-Dahaj, David Yanni, Anthony Burnetti, Jennifer Pentz, Aurelia R Honerkamp-Smith, Hugo Wioland, Hannah R Sleath, William C Ratcliff, Raymond E Goldstein, Peter J Yunker
Abstract
The prevalence of multicellular organisms is due in part to their ability to form complex structures. How cells pack in these structures is a fundamental biophysical issue, underlying their functional properties. However, much remains unknown about how cell packing geometries arise, and how they are affected by random noise during growth - especially absent developmental programs. Here, we quantify the statistics of cellular neighborhoods of two different multicellular eukaryotes: lab-evolved ‘snowflake’ yeast and the green alga Volvox carteri . We find that despite large differences in cellular organization, the free space associated with individual cells in both organisms closely fits a modified gamma distribution, consistent with maximum entropy predictions originally developed for granular materials. This ‘entropic’ cellular packing ensures a degree of predictability despite noise, facilitating parent-offspring fidelity even in the absence of developmental regulation. Together with simulations of diverse growth morphologies, these results suggest that gamma-distributed cell neighborhood sizes are a general feature of multicellularity, arising from conserved statistics of cellular packing.