Developmental Biology A COMPREHENSIVE SYNTHESIS

Volume 7

A Conceptual History of Modern Embryology

Developmental Biology A COMPREHENSIVE SYNTHESIS

Editor LEON W. BROWDER University of Calgary Calgary, Alberta, Canada

Editorial Board

EVERETT ANDERSON Harvard Medical School

JOSEPH T. BAGNARA The University of Arizona

SAMUEL H. BARONDES University of California at San Francisco

ANTONIE W. BLACKLER Cornell University

MARIE A. DiBERARDlNO The Medical College of Pennsylvania

RALPH B. L. GWATKIN The Cleveland Clinic Foundation

Volume 1 OOGENESIS Edited by Leon W. Browder

ELIZABETH D. HAY Harvard Medical School

RALPH S. QUATRANO The DuPont Company

RUDOLF A. RAFF Indiana University

L. DENNIS SMITH University of California at Irvine

IAN M. SUSSEX Yale University

Volume 2 THE CELLULAR BASIS OF MORPHOGENESIS Edited by Leon W. Browder

Volume 3 THE CELL SURFACE IN DEVELOPMENT AND CANCER Edited by Malcolm S. Steinberg

Volume 4 MANIPULATION OF MAMMALIAN DEVELOPMENT Edited by Ralph B. 1. Gwatkin

Volume 5 THE MOLECULAR BIOLOGY OF CELL DETERMINATION AND CELL DIFFERENTIATION Edited by Leon W. Browder

Volume 6 GENOMIC ADAPTABILITY IN SOMATIC CELL SPECIALIZATION Edited by Marie A. DiBerardino and Laurence D. Etkin

Volume 7 A CONCEPTUAL HISTORY OF MODERN EMBRYOLOGY Edited by Scott F. Gilbert

Developmental Biology A COMPREHENSIVE SYNTHESIS

Volume 7

A Conceptual History of Modern Embryology Edited by

SCOTT F. GILBERT Swarthmore College Swarthmore, Pennsylvania

PLENUM PRESS • NEW YORK AND LONDON

Library of Congress Cataloging in Publication Data

(Revised for volume 7)

Developmental biology.

Vol. 4 edited by Ralph B. L. Gwatkin. Vol. 6 edited by Marie A. DiBerardino and Laurence D. Etkin. Vol. 7 edited by Scott F. Gilbert. Includes bibliographies and indexes. Contents: v. 1. Oogenesis-[etc.]-v. 6. Genomic adaptability in somatic cell

specialization - v. 7. A conceptual history of modern embryology. 1. Developmental biology. I. Browder, Leon W.

QH491.D426 1985 574.3 85-3406

Cover illustration: Spemann's hairloop experiment. From Experimentelle Beitriige zu einer Theorie der Entwicklung (1936).

ISBN-13: 978-1-4615-6825-4 e-ISBN-13: 978-1-4615-6823-0 DOl: 10.1007/978-1-4615-6823-0

© 1991 Plenum Press, New York Softcover reprint ofthe hardcover 1st edition 1991

A Division of Plenum Publishing Corporation 233 Spring Street, New York, N.Y. 10013

All rights reserved-

No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher

Contributors

P. G. Abir-Am Department of History of Science, Johns Hopkins University, Baltimore, Maryland 21218

Richard M. Burian Department of Philosophy, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061-0126

Frederick B. Churchill Department of the History and Philosophy of Science, Indiana University, Bloomington, Indiana 47405

Jean-Louis Fischer Centre de Recherche d'Histoire des Sciences, Universite de Paris, Paris, France

Jean Gayon Faculte de Lettres et Philosophie, Universite de Bourgogne, 2100 Dijon, France

Scott F. Gilbert Department of Biology, Swarthmore College, Swarthmore, Pennsylvania 19081

Gerald B. Grunwald Department of Anatomy, Jefferson Medical College, Thomas Jefferson University, Philadelphia, Pennsylvania 19107

Johannes Holtfreter Department of Biology, University of Rochester, Rochester, New York 14627

Jane Maienschein Department of Philosophy, Arizona State University, Tempe, Arizona 85287

Jane M. Oppenheimer Department of Biology, Bryn Mawr College, Bryn Mawr, Pennsylvania, 19010-2899; present address: One Independence Place, 6th Street and Locust Walk, Philadelphia, Pennsylvania 19106

Margaret Saha Department of Biology, University of Virginia, Charlottesville, Virginia 22901

Jan Sapp Department of the History and Philosophy of Science, University of Melbourne, Parkville, Victoria, Australia

Doris T. Zallen Center for the Study of Science in Society and Center for Programs in the Humanities, Virginia Polytechnic Institute and State Univer­sity, Blacksburg, Virginia 24061-0227

v

Preface

"Glory to the science of embryology!" So Johannes Holtfreter closed his letter to this editor when he granted permission to publish his article in this volume. And glory there is: glory in the phenomenon of animals developing their complex morphologies from fertilized eggs, and glory in the efforts of a relatively small group of scientists to understand these wonderful events.

Embryology is unique among the biological disciplines, for it denies the hegemony of the adult and sees value (indeed, more value) in the stages that lead up to the fully developed organism. It seeks the origin, and not merely the maintenance, of the body. And if embryology is the study of the embryo as seen over time, the history of embryology is a second-order derivative, seeing how the study of embryos changes over time. As Jane Oppenheimer pointed out, "Sci­ence, like life itself, indeed like history, itself, is a historical phenomenon. It can build itself only out of its past." Thus, there are several ways in which embryology and the history of embryology are similar. Each takes a current stage of a developing entity and seeks to explain the paths that brought it to its present condition. Indeed, embryology used to be called Entwicklungsgeschichte, the developmental history of the organism. Both embryology and its history interpret the interplay between internal factors and external agents in the causation of new processes and events. The embryologist, of course, has the advantage of seeing this "history" repeating itself every time a new organism is generated.

So it is not surprising that historians, embryologists, embryologists-turned­historians, and historians-turned-embryologists can collaborate on a history of embryology. This is, of course, a history of embryology, and there is no pretense that it is the history of the field (any more than the excellent volumes on oogenesis and morphogenesis in this series can be considered the complete texts in these areas). The predominant theme in this volume is the concept of induc­tion. This was not the way the book was originally planned, but rather, a fortu­itous accident of those who were able to write their chapters during this time. Other themes could have predominated, and I hope that there will be more historical volumes in this series that will address these areas. However, induc­tion has certainly been a pivotal principle in the history of embryology, and it remains an extremely active field of contemporary research. Given the current interest in the molecular mechanisms of neural and "secondary" induction, this history becomes all the more timely.

One of the values of this book for contemporary developmental biologists

vii

viii Preface

should be to clarify some of the concepts that embryologists have bequeathed to developmental biology. The volume begins with a chapter by Frederick Churchill that details the bases for the tradition of comparative embryology. The work of Baer, Pander, and Rathke is central to this endeavor, and it is here that the first observations of mutually interactive tissues were made. When Christian Pander discovered the primary germ layers of the chick embryo, he concluded that

a unique metamorphosis begins in each of these three [germ layers] and hurries toward its goal; although each is not yet independent enough to indicate what it truly is; it still needs the help of its sister travellers, and therefore although already designated for different ends, all three influence each other collectively until each has reached an appropriate level.

This quotation shows that both internal and inductive features of embryo­genesis were recognized very early. Jean-Louis Fischer then provides the context of French comparative anatomy and teratology in which Laurent Chabry per­formed his experiments showing the mosaic development in tunic ate embryos. Fischer also shows how personal and national ideologies can influence the interpretation of experimental results. Next, Jane Maienschein provides a history of the early work in Entwicklungsmechanik, belying the textbook notion of a few "founding fathers" and demonstrating the rich tapestry provided by the work of numerous investigators. One of these investigators, Curt Herbst, is given special attention in the chapter by Jane Oppenheimer. Her study delineates how calcium and lithium ions were first used to study morphogenesis, how the first concepts of induction entered into experimental embryology, and how physiological theories of tropisms influenced research into embryonic cell movements.

The work of Herbst was extremely important in the intellectual development of Hans Spemann. Margaret Saha documents' the evolution of Spemann's concep­tualization of induction by discussing his experiments on lens formation. These studies were critical for the design of Spemann's later experiments and provide insight into how he came to interpret them as he did. The next chapter is an autobiographical essay by Johannes Holtfreter in which he discusses his science and his art. He describes how he came to Spemann's and Mangold's laboratories, how his concept of induction changed over the years, and how he attempted to find the molecules that were responsible for the induction of the neural tube.

Several research programs came out of the studies on induction and mor­phogenesis that were performed by Spemann and Holtfreter. One of these was the study of the cell surface in development. The search for the processes and molecules responsible for intercellular adhesion is shown by Gerald Grunwald to have been full of surprising results and serendipitous observations. Another research program starting from the Freiburg group was Joseph Needham's at­tempt to produce a biochemistry of the embryo. P. G. Abir-Am documents Need­ham's attempts to place the biochemistry of the embryo on a solid theoretical and philosophical foundation. Here we see the complexities of forming a new inter­disciplinary science and the need to free biological thinking from the paradigms of nineteenth-century physics.

Needham's colleague in these endeavors, Conrad Waddington, attempted to weld Entwicklungsmechanik with genetics and evolutionary theory. Together with Salome Gluecksohn-Waelsch and Boris Ephrussi, he helped create the basic tenets of developmental genetics. Richard Burian, Jean Gayon, and Doris

Preface ix

Zallen discuss the ways in which Ephrussi attempted to synthesize genetics and development, while I relate the attempts of Gluecksohn-Schoenheimer and Waddington to use the concepts of induction and competence to reunite these disciplines. One of the most hotly debated topics in those early days of develop­mental genetics was whether all the genotype resided in the nucleus. Both Ephrussi and Waddington were initially partial to the presence of plasmagenes in the cytoplasm. Jan Sapp details the debates on this issue, especially as they pertained to protozoans, organisms that some scientists saw as models for meta­zoan development, but which other scientists saw as interesting exceptions to the general rule of nuclear inheritance.

Developmental biology is the anagenetic descendant of embryology. N. J. Berrill relates that Paul Weiss wrote to him asking Berrill to suggest a name for the science that included embryology and also gene activity, regeneration, cell movement studies, and other areas of developmental biology. Berrill sent the letter back to him with the last two words capitalized. We who study develop­mental biology are the inheritors of embryology'S concepts, organisms, and sense of wonder. From other sources, we have received a new set of tools with a resolving power far greater than what was available a generation ago. Frogs, chicks, and sea urchins (along with nematodes, flies, and leeches) are now being dissected with monoclonal antibodies, antisense mRNAs, and confocal micro­scopes. We are presently seeing a return to those old embryological enigmas that were abandoned for lack of such specific tools. The morphogenesis of the disci­ple continues.

I thank all the authors for their contributions, and Marie DiBerardino, Leon Browder, and Mary Born for their roles in the conception and birth of this volume.

"Glory to the science of embryology!"

Scott F. Gilbert

Contents

Chapter 1 • The Rise of Classical Descriptive Embryology

Frederick B. Churchill

1. Introduction ................................... '" . . .. . . .. . . . . 1 2. Descriptive Embryology in the Baltic Periphery. . . . .. . . .. . ... . . . . 2 3. Christian Pander .............................................. 3 4. Karl Ernst von Baer ........................................... 5 5. Heinrich Rathke .............................................. 12 6. A New Theoretical Framework at Mid-Century .................. 16 7. Evolution and Development.................................... 18 8. Specificity of the Germ Layers ................................. 20 9. Conclusion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22

Notes and References ................... :. . . . . . . . . . . . . . . . . . . . . . 23

Chapter 2 • Laurent Chabry and the Beginnings of Experimental Embryology in France

Jean-Louis Fischer

1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31 2. E. Geoffroy Saint-Hilaire ....................................... 31 3. C. Dareste .................................................... 33 4. Stanislas Warynski and Hermann Fol ........................... 33 5. Laurent Chabry ............................................... 34 6. Edwin Grant Conklin, Albert Dalcq, and Oscar Hertwig .......... 39 7. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 40

Notes and References. . . . . . . . . .. . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . 40

Chapter 3 • The Origins of Entwicklungsmechanik

Jane Maienschein

1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43 2. Foundations of Entwicklungsmechanik ......................... 43 3. Experimental Embryology...................................... 55

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xii Contents

4. Responses. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58 Notes and References ................. ;........................ 59

Chapter 4 • Curt Herbst's Contributions to the Concept of Embryonic Induction

Jane M. Oppenheimer

1. Introduction ............................ ' ... , ... '" ..... '. . . . . .. 63 2. Curriculum Vitae ............................................. 65 3. Personalia. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67 4. Opera Magna ................................................. 70 5. Obiter Dicta .................................................. 79 6. Ab Origine ................................................... 81

Notes and References.......................................... 84

Chapter 5 • Spemann Seen through a Lens

Margaret Saha

1. Introduction. . .. . . . . . . . . . . . . . ... .. . . . . . . . . . . .. . . .. . . . . . . . . . . . . 91 2. Early Years: The Search for a Problem of General Interest ......... 92 3. Lens Induction: A Paradigm for Vertebrate Cell Determination .... 95 4. Determination at Gastrula Stages: Application of the

Lens-Induction Paradigm to the Organizer Experiments. . . . . . . . . .. 102 5. Postscript: A Modern Perspective ..... '. . . . . . . . . . . . . . . . . . . . . . . . .. 105

Notes and References. . . . . . . . . .. . . . . . . . . . . . . . . .. . . .. . . . . . . . . . .. 107

Chapter 6 • Reminiscenses on the Life and Work of Johannes Holtfreter

Johannes Holtfreter

1. Editor's Note ............................................... '" 109 2. Foreword..................................................... 109 3. Reminiscence ........................................ ,......... 110

References. . . . . .. . . . . . . . .. . . . .. . . . . . . .. . . . . . . .. . . . . . . . . . . . . . .. 126

Chapter 7 • The Conceptual and Experimental Foundations of Vertebrate Embryonic Cell Adhesion Research

Gerald B. Grunwald

1. Introduction ..... '. . . . . . . .. . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . .. 129 2. The Invertebrate Zoological Roots of Intercellular Cell Adhesion

Studies ..... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 130 3. The Recognition of Differential Cell Adhesion as a Central

Mechanism of Morphogenesis .................................. 134

Contents xiii

4. Qualitative and Quantitative Quarrels over the Quintessence of Cell Adhesion ................................................ 139

5. Immunological Approaches to the Analysis of Cell Adhesion ..... 146 6. The Role of Calcium in Cell Adhesion .......................... 150 7. Epilogue: From the Embryo to the Gene and Back ............... 153

Notes and References. . . . . . . . . . . . . . . . . .. . . . . . . . .. . . . . . . . . . . . . .. 154

Chapter 8 • The Philosophical Background of Joseph Needham's Work in Chemical Embryology

P. G. Abir-Am

1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 159 2. Joseph Henri Woodger and the Emancipation of Biology. . . . . . . . .. 160 3. Joseph Needham, 1925-1933: Mechanism, Organicism, and the

Philosophical Status of Biochemistry ........................... 163 4. Process and Structure in the Woodger-Needham Rapprochement:

From Philosophical Misunderstandings toward a Theoretical Integration of Biochemistry, Embryology, and "Logistics" ......... 165

5. Conclusions: The Philosophical and Social Context of Biochemical Embryology in the 1930s ...................................... 173 Notes and References ......................................... , 177

Chapter 9 • Induction and the Origins of Developmental Genetics

Scott F. Gilbert

1. Introduction: The Problem of Synthesis ......................... 181 2. Salome Gluecksohn-Schoenheimer and the Path from

Experimental Embryology to Developmental Genetics ............ 183 3. The Concrescence of Genetics and Development: C. H. Waddington 188

Notes and References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 203

Chapter 10 • Boris Ephrussi and the Synthesis of Genetics and Embryology

Richard M. Burian, Jean Gayon, and Doris T. Zallen

1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 207 2. Early Embryological Studies ................................... 208 3. Beadle and Ephrussi on Drosophila Hormones .................. 210 4. Ephrussi and Slonimski on Cytoplasmic Inheritance of Respiratory

Competence in Yeast .......................................... 210 5. Somatic Cell Genetics and the Return to Tissue Culture .......... 213 6. Coda and Conclusion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 217

Notes and References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 222

xiv

Chapter 11 • Concepts of Organization: The Leverage of Ciliate Protozoa

. Jan Sapp

Contents

1. A Discourse on Exceptions .................................... 229 2. Deconstructing the Germ Plasm ................................ 232 3. Revolt from Morphological Theories: Protests and Demonstrations 235 4. Weismannism under a New Banner: Geneticists versus

Embryologists. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 237 5. Plasmagene Theory .............................. " ... . . .... . .. 238 6. "Switching" Concepts and Metaphors .......................... 244 7. Supramolecular Structure and Morphogenetic Fields. . . . . . . . . . . .. 247 8. Concluding Remarks .......................................... 254

Notes and References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 255

Index............................................................ 259