Table Of ContentMulticellularity
Vienna Series in Theoretical Biology
Editor-in-Chief
Gerd B. Müller, University of Vienna and KLI Klosterneuburg
Associate Editors
Johannes Jäger, KLI Klosterneuburg
Thomas Pradeu, CNRS and University of Bordeaux
Katrin Schäfer, University of Vienna
The Evolution of Cognition , edited by Cecilia Heyes and Ludwig Huber, 2000
Origination of Organismal Form: Beyond the Gene in Developmental and Evolutionary Biology , edited by Gerd
B. Müller and Stuart A. Newman, 2003
Environment, Development, and Evolution: Toward a Synthesis , edited by Brian K. Hall, Roy D. Pearson, and
Gerd B. Müller, 2004
Evolution of Communication Systems: A Comparative Approach , edited by D. Kimbrough Oller and Ulrike
Greibel, 2004
Modularity: Understanding the Development and Evolution of Natural Complex Systems, edited by Werner Cal-
lebaut and Diego Rasskin-Gutman, 2005
Compositional Evolution: The Impact of Sex, Symbiosis, and Modularity on the Gradualist Framework of Evolu-
tion , by Richard A. Watson, 2006
Biological Emergences: Evolution by Natural Experiment , by Robert G. B. Reid, 2007
Modeling Biology: Structures, Behaviors, Evolution , edited by Manfred D. Laubichler and Gerd B. Müller, 2007
Evolution of Communicative Flexibility: Complexity, Creativity, and Adaptability in Human and Animal Com-
munication , edited by Kimbrough D. Oller and Ulrike Greibel, 2008
Functions in Biological and Artificial Worlds: Comparative Philosophical Perspectives ,edited by Ulrich Krohs
and Peter Kroes, 2009
Cognitive Biology: Evolutionary and Developmental Perspectives on Mind, Brain, and Behavior ,edited by Luca
Tommasi, Mary A. Peterson, and Lynn Nadel, 2009
Innovation in Cultural Systems: Contributions from Evolutionary Anthropology , edited by Michael J. O’Brien
and Stephen J. Shennan, 2009
The Major Transitions in Evolution Revisited , edited by Brett Calcott and Kim Sterelny, 2011
Transformations of Lamarckism: From Subtle Fluids to Molecular Biology , edited by Snait B. Gissis and Eva
Jablonka, 2011
Convergent Evolution: Limited Forms Most Beautiful , George McGhee, 2011
From Groups to Individuals: Perspectives on Biological Associations and Emerging Individuality , edited by
Frédéric Bouchard and Philippe Huneman, 2013
Developing Scaffolds in Evolution, Culture, and Cognition , edited by Linnda R. Caporael, James Griesemer, and
William C. Wimsatt, 2013
Multicellularity: Origins and Evolution , edited by Karl J. Niklas and Stuart A. Newman, 2015
Multicellularity
Origins and Evolution
edited by Karl J. Niklas and Stuart A. Newman
The MIT Press
Cambridge, Massachusetts
London, England
© 2016 Massachusetts Institute of Technology
All rights reserved. No part of this book may be reproduced in any form by any electronic or mechanical means
(including photocopying, recording, or information storage and retrieval) without permission in writing from the
publisher.
This book was set in Times New Roman by Toppan Best-set Premedia Limited. Printed and bound in the United
States of America.
Library of Congress Cataloging-in-Publication Data is available.
ISBN: 978-0-262-03415-9
10 9 8 7 6 5 4 3 2 1
Contents
Dedication: Werner Callebaut vii
Series Foreword ix
Foreword: The Evolution of Multicellularity xi
John Tyler Bonner
Preface xxi
I FUNCTIONAL AND MOLECULAR PREDISPOSITIONS TO
MULTICELLULARITY 1
1 Fossils, Feeding, and the Evolution of Complex Multicellularity 3
Andrew H. Knoll and Daniel J. G. Lahr
2 Alternative Splicing, Intrinsically Disordered Proteins, Calmodulin, and the
Evolution of Multicellularity 17
Karl J. Niklas and A. Keith Dunker
II PLANTS AND RELATED THEORY 41
3 The Mechanistic Basis for the Evolution of Soma during the Transition to
Multicellularity in the Volvocine Algae 43
Stephan G. König and Aurora M. Nedelcu
4 Physicochemical Factors in the Organization of Multicellular Aggregates
and Plants 71
Juan Antonio Arias del Angel, Eugenio Azpeitia, Mariana Benítez, Ana E.
Escalante, Valeria Hernández-Hernández, and Emilio Mora Van Cauwelaert
5 Angiosperm Multicellularity: The Whole, the Parts, and the Sum 87
Ottoline Leyser
vi Contents
III AMOEBOZOA, FUNGI, AND RELATED THEORY 103
6 Cellular Slime Mold Development as a Paradigm for the Transition from
Unicellular to Multicellular Life 105
Vidyanand Nanjundiah
7 Trade-offs Drive the Evolution of Increased Complexity in Nascent
Multicellular Digital Organisms 131
Peter L. Conlin and William C. Ratcliff
8 The Paths to Artificial Multicellularity: From Physics to Evolution 149
Salva Duran-Nebreda, Raúl Montañez, Adriano Bonforti, and Ricard Solé
IV METAZOA AND RELATED THEORY 169
9 What Are the Genomes of Premetazoan Lineages Telling Us about the Origin
of Metazoa? 171
Iñaki Ruiz-Trillo
10 Sponges as the Rosetta Stone of Colonial-to-Multicellular Transition 185
Maja Adamska
11 A Scenario for the Origin of Multicellular Organisms: Perspective from
Multilevel Consistency Dynamics 201
Kunihiko Kaneko
12 Multicellularity, the Emergence of Animal Body Plans, and the Stabilizing
Role of the Egg 225
Stuart A. Newman
V PHILOSOPHICAL ASPECTS OF MULTICELLULARITY 247
13 Integrating Constitution and Interaction in the Transition from Unicellular to
Multicellular Organisms 249
A rgyris Arnellos and Alvaro Moreno
14 Explaining the Origins of Multicellularity: Between Evolutionary Dynamics
and Developmental Mechanisms 277
Alan C. Love
Contributors 297
Index 299
Werner Callebaut (1952–2014)
The volume editors, the series editors, and the editors at MIT Press jointly dedicate this
volume to the memory of Werner Callebaut, who sadly passed away in November 2014.
Werner was one of the founding editors of the Vienna Series in Theoretical Biology. He
had studied philosophy at Ghent University and subsequently pursued an academic career
that led him via the Universities of Brussels, Limburg, and Ghent to Hasselt University,
viii Werner Callebaut (1952–2014)
where he became a Professor of Philosophy in 1995. Following two visiting periods at the
Konrad Lorenz Institute for Evolution and Cognition Research at Altenberg, he moved to
Austria while continuing a part-time affiliation at Hasselt University. In 1999 he became
the Scientific Manager and subsequently the Scientific Director of the KLI, and among
his tasks were the care of the Vienna Series and the journal B iological Theory .
Werner was the perfect editor. His encyclopedic knowledge in vast areas of philosophy
of science and his devotion to quality and style made for the formidable success of B io-
logical Theory , of which he was the editor-in-chief. He devoted countless hours, day and
night, to “his” journal. He would not only run the standard review processes, but would
contribute comments, suggestions, and corrections to each manuscript, and oftentimes he
engaged in extensive communication with the authors. He also inspired many of the Vienna
Series books and was involved in the preparations for the KLI Altenberg Workshop that
spawned the present volume. Werner contributed valuable insights during the workshop
and gave encouragement to several of the authors joined herein. His remarkable capacity
to elicit more substantial results from any intellectual project he came in touch with also
contributed to the quality of the present one.
Werner was a remarkable man and a valued colleague, whose strong belief in intellectual
exactitude has improved the writings and the thinking of many a scholar. If the present
volume contains more flaws than usual, it is because Werner could not edit the manu-
scripts. He would have loved to see this volume appear. Upon receipt he would have
opened it up at a random page, and his swift editorial eye would immediately have detected
several mistakes. Now those mistakes will remain hidden for years, but we will remember
Werner as our gifted companion who could have detected them. We lift a glass of editor’s
spirit to his memory!
Gerd B. Müller, Stuart A. Newman, Karl J. Niklas
Klosterneuburg, 17 April 2015
Series Foreword
Biology is a leading science in this century. As in all other sciences, progress in biology
depends on the interrelations between empirical research, theory building, modeling, and
societal context. But whereas molecular and experimental biology have evolved dramati-
cally in recent years, generating a flood of detailed empirical data, the integration of these
results into useful theoretical frameworks has lagged behind. Driven largely by pragmatic
and technical considerations, research in biology continues to be less guided by theory
than seems indicated. By promoting the formulation and discussion of new theoretical
concepts in the biosciences, this series intends to help fill important gaps in our under-
standing of some of the major open questions of biology, such as the origin and organiza-
tion of organismal form, the relationship between development and evolution, and the
biological bases of cognition and mind. Theoretical biology has important roots in the
experimental tradition of early-twentieth-century Vienna. Paul Weiss and Ludwig von
Bertalanffy were among the first to use the term t heoretical biology in its modern sense.
In their understanding the subject was not limited to mathematical formalization, as is
often the case today, but extended to the conceptual foundations of biology. It is this com-
mitment to a comprehensive and cross-disciplinary integration of theoretical concepts that
the Vienna Series intends to emphasize. Today, theoretical biology has genetic, develop-
mental, and evolutionary components, the central connective themes in modern biology,
but it also includes relevant aspects of computational or systems biology and extends to
the naturalistic philosophy of sciences. The “Vienna Series” grew out of theory-oriented
workshops organized by the KLI, an international institute for the advanced study of
natural complex systems. The KLI fosters research projects, workshops, book projects,
and the journal B iological Theory , all devoted to aspects of theoretical biology, with an
emphasis on—but not restricted to—integrating the developmental, evolutionary, and
cognitive sciences. The series editors welcome suggestions for book projects in these
domains.
Gerd B. Müller, Johannes Jäger, Thomas Pradeu, Katrin Schäfer
