Abstract

Early multicellular organisms must gain adaptations to outcompete their unicellular ancestors, as well as other multicellular lineages. The tempo and mode of multicellular adaptation is influenced by many factors including the traits of individual cells. We consider how a fundamental aspect of cells, whether they reproduce via binary fission or budding, can affect the rate of adaptation in primitive multicellularity. We use mathematical models to study the spread of beneficial, growth rate mutations in unicellular populations and populations of multicellular filaments reproducing via binary fission or budding. Comparing populations once they reach carrying capacity, we find that the spread of mutations in multicellular budding populations is qualitatively distinct from the other populations and in general slower. Since budding and binary fission distribute age-accumulated damage differently, we consider the effects of cellular senescence. When growth rate decreases with cell age, we find that beneficial mutations can spread significantly faster in a multicellular budding population than its corresponding unicellular population or a population reproducing via binary fission. Our results demonstrate that basic aspects of the cell cycle can give rise to different rates of adaptation in multicellular organisms.

Highlights

  • The evolution of multicellularity gave rise to organisms whose scale and complexity significantly exceed those of their unicellular ancestors [1,2]

  • We find that in aging unicellular populations, binary fission leads to faster adaptation, while in multicellular populations budding can either inhibit or significantly increase rates of adaptation depending on which cell mutates

  • We explore the effects of budding versus binary fission using a simple model of multicellularity

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Summary

Introduction

The evolution of multicellularity gave rise to organisms whose scale and complexity significantly exceed those of their unicellular ancestors [1,2]. Central to the success of any nascent multicellular organism was the ability to gain adaptations and outcompete its ancestors along with other unicellular and multicellular lineages present in the environment [9]. The existence of certain characteristics in unicellular ancestors may potentiate the evolution of novel multicellular phenotypes. It has been proposed that the existence of temporally alternating phenotypes found in the unicellular ancestors of metazoans, dictyostelid social amoebas, and the volvocine algae were co-opted for spatial cellular differentiation during the evolution of multicellularity [22,26,27,28]. Traits that evolved first in unicellular organisms can influence the tempo and mode of multicellular evolution in that lineage

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