Evolution of Multicellularity

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Population and Evolutionary Genetics and Genomics".

Deadline for manuscript submissions: closed (31 January 2021) | Viewed by 30363

Special Issue Editor


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Guest Editor
Algal Genetics Group, Laboratoire de Biologie Integrative des Modeles Marins, Roscoff, France
Interests: brown algal developmental biology; brown algal life cycles; brown algal genetics and genomics

Special Issue Information

The emergence of multicellular organisms was perhaps the most spectacular of the major transitions during the evolutionary history of life on this planet. Transitions to multicellularity are generally considered to have occurred in two stages, with the acquisition of simple multicellularity occurring more easily than the subsequent emergence of complex multicellular lifeforms. To become multicellular, organisms need to acquire cell–cell adhesion mechanisms and the capacity to exchange signals and nutrients between cells. It is also important that the cells that make up an organism function collectively, a situation that is usually made possible by clonal multiplication from a single initial cell. Over the past two decades, analysis of a broad range of both unicellular and multicellular organisms has provided important insights into the genetic and cellular features that underlie key features of multicellularity; however, there remain many outstanding questions to be addressed. For example, to what extent do evolutionary pressures drive transitions to multicellularity by acting on advantageous features, such as increased size in prey–predator interactions and division of labour between different cell types within the organism (differentiation)? Similarly, does the acquisition of multicellular characteristics itself drive the process to some extent by committing cells to increasing levels of cooperation ("ratcheting")? Do these questions apply differently to organisms that form by aggregation of multiple unicells compared with those derived by mitotic proliferation from a single initial cell? At the genetic level, is it possible to define a genomic toolkit responsible for multicellularity and, if this toolkit exists, did its emergence principally involve gain and loss of genes or were changes in gene regulation more important? To what extent did the independent emergence of multicellularity across the different major eukaryotic lineages involve similar mechanisms and, if they did, to what degree can we consider these events to have been independent, considering that these lineages can all be traced back to a common, unicellular ancestor? What is the relationship between multicellularity and other biological features such as sexual traits? Finally, how does multicellularity relate to the definition of a biological individual?
This Special Issue aims to address some of these questions, covering the evolution of both simple and complex multicellularity and including both experimental and theoretical approaches to understanding this important evolutionary transition.

Dr. J. Mark Cock
Guest Editor

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Keywords

  • cell–cell adhesion
  • cell–cell signalling
  • development
  • differentiation
  • eukaryotes
  • evolution
  • evolutionary transition
  • genetic toolkit
  • multicellularity
  • unicellular.

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Published Papers (6 papers)

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Editorial

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2 pages, 170 KiB  
Editorial
Evolution of Multicellularity
by J. Mark Cock
Genes 2021, 12(10), 1532; https://doi.org/10.3390/genes12101532 - 28 Sep 2021
Viewed by 2019
Abstract
The emergence of multicellular organisms was, perhaps, the most spectacular of the major transitions during the evolutionary history of life on this planet [...] Full article
(This article belongs to the Special Issue Evolution of Multicellularity)

Research

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17 pages, 2345 KiB  
Article
Signatures of Transcription Factor Evolution and the Secondary Gain of Red Algae Complexity
by Romy Petroll, Mona Schreiber, Hermann Finke, J. Mark Cock, Sven B. Gould and Stefan A. Rensing
Genes 2021, 12(7), 1055; https://doi.org/10.3390/genes12071055 - 9 Jul 2021
Cited by 9 | Viewed by 6239
Abstract
Red algae (Rhodophyta) belong to the superphylum Archaeplastida, and are a species-rich group exhibiting diverse morphologies. Theory has it that the unicellular red algal ancestor went through a phase of genome contraction caused by adaptation to extreme environments. More recently, the classes Porphyridiophyceae, [...] Read more.
Red algae (Rhodophyta) belong to the superphylum Archaeplastida, and are a species-rich group exhibiting diverse morphologies. Theory has it that the unicellular red algal ancestor went through a phase of genome contraction caused by adaptation to extreme environments. More recently, the classes Porphyridiophyceae, Bangiophyceae, and Florideophyceae experienced genome expansions, coinciding with an increase in morphological complexity. Transcription-associated proteins (TAPs) regulate transcription, show lineage-specific patterns, and are related to organismal complexity. To better understand red algal TAP complexity and evolution, we investigated the TAP family complement of uni- and multi-cellular red algae. We found that the TAP family complement correlates with gain of morphological complexity in the multicellular Bangiophyceae and Florideophyceae, and that abundance of the C2H2 zinc finger transcription factor family may be associated with the acquisition of morphological complexity. An expansion of heat shock transcription factors (HSF) occurred within the unicellular Cyanidiales, potentially as an adaption to extreme environmental conditions. Full article
(This article belongs to the Special Issue Evolution of Multicellularity)
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29 pages, 3099 KiB  
Article
The Consequences of Budding versus Binary Fission on Adaptation and Aging in Primitive Multicellularity
by Hanna Isaksson, Peter L. Conlin, Ben Kerr, William C. Ratcliff and Eric Libby
Genes 2021, 12(5), 661; https://doi.org/10.3390/genes12050661 - 28 Apr 2021
Cited by 5 | Viewed by 4397
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, [...] Read more.
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. Full article
(This article belongs to the Special Issue Evolution of Multicellularity)
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Review

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27 pages, 2970 KiB  
Review
Role and Evolution of the Extracellular Matrix in the Acquisition of Complex Multicellularity in Eukaryotes: A Macroalgal Perspective
by Bernard Kloareg, Yacine Badis, J. Mark Cock and Gurvan Michel
Genes 2021, 12(7), 1059; https://doi.org/10.3390/genes12071059 - 10 Jul 2021
Cited by 35 | Viewed by 7866
Abstract
Multicellular eukaryotes are characterized by an expanded extracellular matrix (ECM) with a diversified composition. The ECM is involved in determining tissue texture, screening cells from the outside medium, development, and innate immunity, all of which are essential features in the biology of multicellular [...] Read more.
Multicellular eukaryotes are characterized by an expanded extracellular matrix (ECM) with a diversified composition. The ECM is involved in determining tissue texture, screening cells from the outside medium, development, and innate immunity, all of which are essential features in the biology of multicellular eukaryotes. This review addresses the origin and evolution of the ECM, with a focus on multicellular marine algae. We show that in these lineages the expansion of extracellular matrix played a major role in the acquisition of complex multicellularity through its capacity to connect, position, shield, and defend the cells. Multiple innovations were necessary during these evolutionary processes, leading to striking convergences in the structures and functions of the ECMs of algae, animals, and plants. Full article
(This article belongs to the Special Issue Evolution of Multicellularity)
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16 pages, 1443 KiB  
Review
Evolution of Multicellular Complexity in The Dictyostelid Social Amoebas
by Koryu Kin and Pauline Schaap
Genes 2021, 12(4), 487; https://doi.org/10.3390/genes12040487 - 27 Mar 2021
Cited by 14 | Viewed by 5780
Abstract
Multicellularity evolved repeatedly in the history of life, but how it unfolded varies greatly between different lineages. Dictyostelid social amoebas offer a good system to study the evolution of multicellular complexity, with a well-resolved phylogeny and molecular genetic tools being available. We compare [...] Read more.
Multicellularity evolved repeatedly in the history of life, but how it unfolded varies greatly between different lineages. Dictyostelid social amoebas offer a good system to study the evolution of multicellular complexity, with a well-resolved phylogeny and molecular genetic tools being available. We compare the life cycles of the Dictyostelids with closely related amoebozoans to show that complex life cycles were already present in the unicellular common ancestor of Dictyostelids. We propose frost resistance as an early driver of multicellular evolution in Dictyostelids and show that the cell signalling pathways for differentiating spore and stalk cells evolved from that for encystation. The stalk cell differentiation program was further modified, possibly through gene duplication, to evolve a new cell type, cup cells, in Group 4 Dictyostelids. Studies in various multicellular organisms, including Dictyostelids, volvocine algae, and metazoans, suggest as a common principle in the evolution of multicellular complexity that unicellular regulatory programs for adapting to environmental change serve as “proto-cell types” for subsequent evolution of multicellular organisms. Later, new cell types could further evolve by duplicating and diversifying the “proto-cell type” gene regulatory networks. Full article
(This article belongs to the Special Issue Evolution of Multicellularity)
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Other

13 pages, 421 KiB  
Opinion
Exon Shuffling Played a Decisive Role in the Evolution of the Genetic Toolkit for the Multicellular Body Plan of Metazoa
by Laszlo Patthy
Genes 2021, 12(3), 382; https://doi.org/10.3390/genes12030382 - 8 Mar 2021
Cited by 7 | Viewed by 2643
Abstract
Division of labor and establishment of the spatial pattern of different cell types of multicellular organisms require cell type-specific transcription factor modules that control cellular phenotypes and proteins that mediate the interactions of cells with other cells. Recent studies indicate that, although constituent [...] Read more.
Division of labor and establishment of the spatial pattern of different cell types of multicellular organisms require cell type-specific transcription factor modules that control cellular phenotypes and proteins that mediate the interactions of cells with other cells. Recent studies indicate that, although constituent protein domains of numerous components of the genetic toolkit of the multicellular body plan of Metazoa were present in the unicellular ancestor of animals, the repertoire of multidomain proteins that are indispensable for the arrangement of distinct body parts in a reproducible manner evolved only in Metazoa. We have shown that the majority of the multidomain proteins involved in cell–cell and cell–matrix interactions of Metazoa have been assembled by exon shuffling, but there is no evidence for a similar role of exon shuffling in the evolution of proteins of metazoan transcription factor modules. A possible explanation for this difference in the intracellular and intercellular toolkits is that evolution of the transcription factor modules preceded the burst of exon shuffling that led to the creation of the proteins controlling spatial patterning in Metazoa. This explanation is in harmony with the temporal-to-spatial transition hypothesis of multicellularity that proposes that cell differentiation may have predated spatial segregation of cell types in animal ancestors. Full article
(This article belongs to the Special Issue Evolution of Multicellularity)
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