Department of Applied Mathematics and Theoretical Physics, Centre for Mathematical Sciences, University of Cambridge, Cambridge, United Kingdom
Seyed A Zamani-Dahaj
School of Physics, Georgia Institute of Technology, Atlanta, United States; School of Biological Sciences, Georgia Institute of Technology, Atlanta, United States; Quantitative Biosciences Graduate Program, Georgia Institute of Technology, Atlanta, United States
David Yanni
School of Physics, Georgia Institute of Technology, Atlanta, United States
Anthony Burnetti
School of Biological Sciences, Georgia Institute of Technology, Atlanta, United States
Jennifer Pentz
School of Biological Sciences, Georgia Institute of Technology, Atlanta, United States; Department of Molecular Biology, Umeå University, Umeå, Sweden
Aurelia R Honerkamp-Smith
Department of Applied Mathematics and Theoretical Physics, Centre for Mathematical Sciences, University of Cambridge, Cambridge, United Kingdom
Hugo Wioland
Department of Applied Mathematics and Theoretical Physics, Centre for Mathematical Sciences, University of Cambridge, Cambridge, United Kingdom
Hannah R Sleath
Department of Applied Mathematics and Theoretical Physics, Centre for Mathematical Sciences, University of Cambridge, Cambridge, United Kingdom
William C Ratcliff
School of Biological Sciences, Georgia Institute of Technology, Atlanta, United States
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.
