Genetics of a de novo origin of undifferentiated multicellularity.

Matthew D Herron,Frank Rosenzweig,William C Ratcliff,Jacob Boswell

doi:10.1098/rsos.180912

Abstract

The evolution of multicellularity was a major transition in evolution and set the stage for unprecedented increases in complexity, especially in land plants and animals. Here, we explore the genetics underlying a de novo origin of multicellularity in a microbial evolution experiment carried out on the green alga Chlamydomonas reinhardtii. We show that large-scale changes in gene expression underlie the transition to a multicellular life cycle. Among these, changes to genes involved in cell cycle and reproductive processes were overrepresented, as were changes to C. reinhardtii-specific and volvocine-specific genes. These results suggest that the genetic basis for the experimental evolution of multicellularity in C. reinhardtii has both lineage-specific and shared features, and that the shared features have more in common with C. reinhardtii's relatives among the volvocine algae than with other multicellular green algae or land plants.

Highlights

How and why organismal complexity increases are central questions in evolutionary biology
The time points used in the RNA-Seq experiment were chosen to bracket milestones in the life cycle: at 3 h, clusters appear dormant; at 6 h, unicellular propagules are actively swimming; at 9 and 12 h, many have lost motility and begun to develop into multicellular clusters; and at 48 h, clusters have reached a large size
Many of the gene ontologies related to mitosis that are overrepresented among genes underexpressed at 3 h are overrepresented among genes overexpressed at 9 h, including several related to cell cycle and reproductive processes

Summary

Introduction

How and why organismal complexity increases are central questions in evolutionary biology. Large increases in organismal complexity resulted from a series of events in which existing individuals combined to become components of a new kind of individual with parts specialized to play various roles Such events are known as major transitions [3] or evolutionary transitions in individuality [4,5,6] and include the emergence of cellular life from groups of interacting molecular replicators, of eukaryotes from two. For most lineages, evidence of the earliest steps in the transition has been decimated by extinction and obscured by the limitations of the fossil record Most such comparisons are with extant unicellular relatives, which are only approximate stand-ins for unicellular relatives; after all, they have been evolving just as long since the initial divergence as have the multicellular groups with which we are comparing them. Using a combination of whole-genome sequencing, bulked segregant analysis and genome-wide transcriptional analysis, we identify changes in gene structure and expression that distinguish an evolved multicellular clone from its unicellular ancestor

Whole-genome sequencing

Bulked segregant analysis

RNA-Seq

Discussion