De novo origins of multicellularity in response to predation

Matthew D Herron,Frank Rosenzweig,William C Ratcliff,I-Chen Kimberly Chen,Joshua M Borin,Jillian Walker,Margrethe Boyd,Jacob C Boswell,Charles A Knox

doi:10.1038/s41598-019-39558-8

Abstract

The transition from unicellular to multicellular life was one of a few major events in the history of life that created new opportunities for more complex biological systems to evolve. Predation is hypothesized as one selective pressure that may have driven the evolution of multicellularity. Here we show that de novo origins of simple multicellularity can evolve in response to predation. We subjected outcrossed populations of the unicellular green alga Chlamydomonas reinhardtii to selection by the filter-feeding predator Paramecium tetraurelia. Two of five experimental populations evolved multicellular structures not observed in unselected control populations within ~750 asexual generations. Considerable variation exists in the evolved multicellular life cycles, with both cell number and propagule size varying among isolates. Survival assays show that evolved multicellular traits provide effective protection against predation. These results support the hypothesis that selection imposed by predators may have played a role in some origins of multicellularity.

Highlights

Ratcliff and colleagues have shown that selection for an increased rate of settling out of liquid suspension consistently results in the evolution of multicellular ‘snowflake’ colonies in the yeast Saccharomyces cerevisiae[8] and results in the evolution of simple multicellular structures in C. reinhardtii[9]
We present experiments in which we used the ciliate predator Paramecium tetraurelia to select for the de novo evolution of multicellularity in outcrossed populations of C. reinhardtii
Our results show that the transition to a simple multicellular life cycle can happen rapidly in response to an ecologically relevant selective pressure

Summary

Introduction

As Leo Buss emphasized in The Evolution of Individuality, the very existence of integrated multicellular organisms is an outcome of evolutionary processes, not a starting condition[1]. It seems, to be a common outcome: multicellular organisms have evolved from unicellular ancestors dozens of times[2,3,4]. Comparative methods and the fossil record, have proven valuable in reconstructing how these transitions may have occurred Both approaches have been critical to our understanding of early multicellular evolution, each has its limitations. Because C. reinhardtii has no multicellular ancestors, these experiments represent a completely novel origin of obligate multicellularity[14,15]

Methods

Results

Conclusion