The Evolution of Multicellularity

Matthew D. Herron, Peter L. Conlin, William C. Ratcliff, Matthew D. Herron, Peter L. Conlin, William C. Ratcliff, Matthew D. Herron, Peter L. Conlin, William C. Ratcliff

• Publisher: CRC Press
• Year: 2022
• ISBN:
  9781000542578
• Edition: 1
• Topic: Biological Sciences
• Subtopic: Cell Biology
• Index: Biological Sciences

Among the most important innovations in the history of life is the transition from single-celled organisms to more complex, multicellular organisms. Multicellularity has evolved repeatedly across the tree of life, resulting in the evolution of new kinds of organisms that collectively constitute a significant portion of Earth's biodiversity and have transformed the biosphere. This volume examines the origins and subsequent evolution of multicellularity, reviewing the types of multicellular groups that exist, their evolutionary relationships, the processes that led to their evolution, and the conceptual frameworks in which their evolution is understood. This important volume is intended to serve as a jumping-off point, stimulating further research by summarizing the topics that students and researchers of the evolution of multicellularity should be familiar with, and highlighting future research directions for the field.

Chapter 13 of this book is freely available as a downloadable Open Access PDF at http://www.taylorfrancis.com under a Creative Commons Attribution-Non Commercial-No Derivatives (CC-BY-NC-ND) 4.0 license.

1IntroductionThe Evolution of Multicellularity in Context

Matthew D. Herron

School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA

Peter L. Conlin

School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA

William C. Ratcliff

School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA

DOI: 10.1201/9780429351907-1

CONTENTS

• 1.1 Introduction
• 1.2 Background
• 1.3 Rationale for the Structure of This Book
• 1.4 Conclusion
• Acknowledgments
• References

If indeed it is true that all living bodies are productions of nature, we are driven to the belief that she can only have produced them one after another and not all in a moment. Now if she shaped them one after another, there are grounds for thinking that she began exclusively with the simplest, and only produced at the very end the most complex organisations both of the animal and vegetable kingdoms.

(Lamarck, 1809, p. 129)

1.1 INTRODUCTION

Barbara Kingsolver called it “audacious” to send a piece of writing out into a world that “already contains Middlemarch” (Kingsolver, 2001). To ask readers to spend time on your creation, when they could instead choose from a raft of powerful, wise, and profound novels that already exist, it had, she concluded, “better be important.” In the context of this collection, our Middlemarch is the outstanding work that has already been done on the evolution of multicellularity. Excellent books by David Kirk (1998), John Tyler Bonner (2000), and Richard Kessin (2001), as well as collections edited by David Whitworth (2008), by Iñaki Ruiz-Trillo and Aurora Nedelcu (2015), and by Karl Niklas and Stuart Newman (2016), have been dedicated to the topic, not to mention thousands of scholarly papers.

Our audacity comes from the conviction that an open niche still exists, a sort of book on multicellularity that hasn’t previously been written. Our goal has been to organize a set of chapters that would collectively serve as an in-depth review of the subfield of evolutionary biology that deals with the origins of multicellularity. We intend the book to serve as a jumping-off point, stimulating further research by summarizing the topics that students and researchers of the evolution of multicellularity should be familiar with.

We hope that it will provide a sufficient overview so that a reader unfamiliar with the relevant literature (a beginning graduate student, for example) will come away with an understanding of the major issues. What types of multicellular organisms exist? What are their evolutionary relationships? What processes led to their origins and subsequent evolution? In what conceptual frameworks can their evolution be understood? Crucially, what questions remain to be answered (see Chapter 18 for a detailed discussion)? In addition to providing an overview for newcomers to the field, we hope the book will serve as a reference for more established researchers.

1.2 BACKGROUND

The idea that multicellular animals and plants evolved from single-celled organisms has been around for as long as there has been a coherent theory of evolution. Jean-Baptiste Lamarck, for example, believed that (mostly) unicellular “infusoria” were constantly arising through spontaneous generation and evolving into more complex forms due to the motion of fluids within their bodies (Lamarck, 1809, 1815) (more details on Lamarck’s views can be found in Chapter 13). Although Charles Darwin considered Lamarck’s ideas about spontaneous generation “superfluous (and groundless)” (Darwin, 1887, p. 210), he agreed that animals and plants likely descend from “some one primordial form” (Darwin, 1859, p. 425).

In the post-Darwin world, descent of multicellular organisms from unicellular ancestors has by and large been taken as a given. Furthermore, plants and animals have long been considered to have independently evolved multicellularity. Ernst Haeckel, for example, proposed that animals descended from protozoa and plants from protophyta (Haeckel, 1894) (more details on Haeckel’s views can be found in Chapter 13). Henry Cadwalader Chapman thought it “probable that Monera in past time divided into animal and vegetal Monera,” which gave rise to the animals and plants (including red, green, and brown algae), respectively (Chapman, 1873, p. 83). August Weismann agreed that animals and plants descended from distinct unicellular ancestors (Weismann, 1889).

As the big picture of phylogenetic relationships among kingdoms and phyla began to emerge, it became clear that two origins of multicellularity would not suffice. For example, the fundamental distinction between cells with and without nuclei, recognized by Haeckel (1869) and formalized in the taxonomy of Copeland (1938), necessitates an independent origin in the filamentous cyanobacteria. This did not, however, resolve the extreme heterogeneity of Copeland’s Kingdom Protoctista (“Nucleate organisms not of the characters of plants [including green algae] and animals” [Copeland, 1956, p. 4]). The recognition of fundamental differences among the phyla within the kingdom, including, for example, red algae, brown algae, and ciliates, further implied that the multicellular members of each of these groups represent at least one additional independent origin of multicellularity.

Further advances in phylogenetic systematics have shown that even within some of these taxa, multicellularity has evolved more than once. This is almost certainly the case in the green algae (Chapter 9), the fungi (Chapter 14), and the Amoebozoa (Chapter 5), for example. In 2007, Grosberg and Strathmann estimated “at least 25” independent origins of multicellularity (Grosberg and Strathmann, 2007, p. 622), but this is very likely a serious underestimate. Recent phylogenetic reconstructions based on whole transcriptome data suggest that there may have been this many independent origins of multicellularity in the green algal lineage alone (One Thousand Plant Transcriptomes Initiative, 2019). Furthermore, we should not forget that essentially all estimates of the number of origins are based exclusively on extant taxa; there is no telling how many species may have evolved multicellularity and subsequently gone extinct without leaving much of a fossil record.

In the second half of the twentieth century, the evolution of multicellularity began to be seen as one example of a broader category of transitions leading to new, more inclusive biological units. John Tyler Bonner, for example, wrote of “cases where in one jump a new level of complexity is reached” (Bonner, 1974, p. 58), including the origins of life, of eukaryotic cells, of multicellularity, and of social groupings. Leo Buss interpreted the hierarchy of life, from genes to species, as resulting from a series of transitions from less to more inclusive units of selection (Buss, 1987). In their foundational book, John Maynard Smith and Eörs Szathmáry treated the evolution of multicellularity as an example of a “Major Transition in Evolution,” events in which new levels of biological organization evolved (Maynard Smith and Szathmáry, 1995).

Maynard Smith and Szathmáry’s book established the Major Transitions as a subfield of evolutionary biology, which has expanded greatly in the last 25 years. In both biology and the philosophy of biology, the evolution of multicellularity has been viewed through this lens. Subsequent authors have revised the list of transitions and continue to do so (Herron, 2021, and references therein), but every version we are aware of has included the evolution of multicellularity.

1.3 RATIONALE FOR THE STRUCTURE OF THIS BOOK

Aside from the introductory and concluding chapters, we have organized the book into four sections. The first, Theory and Philosophy, addresses the ways in which the topic of the evolution of multicellularity has informed and been informed by the philosophy of biology (Chapter 2), the theory of multilevel selection (Chapter 3), and the evolution of life cycles (Chapter 4). The evolution of multicellularity has long played a central role in discussions of the nature of biological individuality, which biological units are the bearers of fitness, predictability versus contingency in evolution, how complexity is defined and how it evolves, biological hierarchies, the evolution of cooperation, and the diversity of life cycles, among other topics.

Multicellular life cycles are remarkably diverse. In eukaryotes, though, nearly all involve an alternation of haploid and diploid generations, with fertilization establishing the diploid phase and meiosis restoring the haploid c...

Table of contents

• Cover Page
• Half-Title Page
• Series Page
• Title Page
• Copyright Page
• Contents
• Foreword
• Acknowledgments
• List of Contributors
• Chapter 1 Introduction: The Evolution of Multicellularity in Context
• Section 1 Theory and Philosophy
• Section 2 Aggregative Multicellularity
• Section 3 Clonal Multicellularity
• Section 4 Life Cycles and Complex Multicellularity
• Section 5 Synthesis and Conclusions
• Index