Fragmentation modes and the evolution of life cycles.

Yuriy Pichugin,Paul B Rainey,Arne Traulsen,Jorge Peña,Natalia L Komarova

doi:10.1371/journal.pcbi.1005860

Abstract

Reproduction is a defining feature of living systems. To reproduce, aggregates of biological units (e.g., multicellular organisms or colonial bacteria) must fragment into smaller parts. Fragmentation modes in nature range from binary fission in bacteria to collective-level fragmentation and the production of unicellular propagules in multicellular organisms. Despite this apparent ubiquity, the adaptive significance of fragmentation modes has received little attention. Here, we develop a model in which groups arise from the division of single cells that do not separate but stay together until the moment of group fragmentation. We allow for all possible fragmentation patterns and calculate the population growth rate of each associated life cycle. Fragmentation modes that maximise growth rate comprise a restrictive set of patterns that include production of unicellular propagules and division into two similar size groups. Life cycles marked by single-cell bottlenecks maximise population growth rate under a wide range of conditions. This surprising result offers a new evolutionary explanation for the widespread occurrence of this mode of reproduction. All in all, our model provides a framework for exploring the adaptive significance of fragmentation modes and their associated life cycles.

Highlights

A requirement for evolution—and a defining feature of life—is reproduction [1,2,3,4]
Some colonial bacteria propagate by fission or by releasing single cells, while others split in highly sophisticated ways; in multicellular organisms reproduction typically proceeds via a single-cell bottleneck phase
Focusing on fragmentation modes of a simple kind we parametrise all possible modes of group fragmentation and identify those modes leading to the fastest population growth

Summary

Introduction

A requirement for evolution—and a defining feature of life—is reproduction [1,2,3,4]. Perhaps the simplest mode of reproduction is binary fission in unicellular bacteria, whereby a single cell divides and produces two offspring cells. In the bacterium Neisseria, a diplococcus, two daughter cells remain attached forming a twocelled group that separates into two groups of two cells only after a further round of cell division [6]. Staphylococcus aureus, another coccoid bacterium, divides in three planes at right angles to one another to produce grape-like clusters of about 20 cells from which single cells separate to form new clusters [7]. Magnetotactic prokaryotes form spherical clusters of about 20 cells, which divide by splitting into two sized clusters [8]

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