THE DYNAMIC ARCHITECTURE OF A DEVELOPING ORGANISM The Dynamic Architecture of a Developing Organism An Interdisciplinary Approach to the Development of Organisms by L. V. BELOUSSOV SPRINGER-SCIENCE+BUSINESS MEDIA, B.V. A C.I.P. Catalogue record for this book is available from the Library of Congress. ISBN 978-90-481-5026-7 ISBN 978-94-015-8998-7 (eBook) DOl 10.1007/978-94-015-8998-7 Printed on acid-free paper All Rights Reserved © 1998 Springer Science+Business Media Dordrecht Originally published by Kluwer Academic Publishers in 1998 Softcover reprint of the hardcover 1st edition 1998 No part of the material protected by this copyright notice may be reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording or by any information storage and retrieval system, without written permission from the copyright owner. · .. A palm of primacy will be gained by that most happy one who succeeds in reducing the formative powers of the animal organisms to the general forces or vital laws of a World's Entity. Carl Ernst von Baer (1828) We can now already speak about a body as about a mobile border between the future and the past, about a shifted point which behaves as if being permanently pushed by our past towards our future. Henry Bergson (1896) According to our viewpoint ... out of an adequate description of any momentary state of a living system its transition to the next should inevitably follow. Alexander Gurwitsch (written in 1948 - 1950, published in 1991) TABLE OF CONTENTS Introduction Chapter 1. Structure Formation in Physics and Biology: General Outline and Approaches 6 1.1. From the spontaneous creativity of Nature to the inert world of uniform determinism (an historical outlook) 6 1.2. Non-biological structurization in terms of a symmetry theory 8 1.3. Structurization (morphogenesis) in developing organisms 17 1.4. The elements of a self-organization theory relevant to biological morphogenesis 38 1.5. A brief excursion into semiotics: notions of meaning, context and levels, developmentally oriented 68 1.6. Summary of the chapter 73 Chapter 2. A hierarchy of Dynamic Structures in Developing Organisms, as Traced in an Ascending Order 75 2.1. Mechanical stresses, strains and the supramolecular devices, that produce them 76 2.2. Dynamic structures involved in single cells activities 100 2.3. A morphodynamics in cell collectives 108 2.4. Stress-mediated morphogenetical feedbacks: attempts of generalization 145 2.5. Standard morphomechanical situations 158 2.6. Summary of the chapter 163 Chapter 3. The Developmental Successions 165 3.1. Embracing laws for developmental successions: formulating a task 165 3.2. An egg mechanics 169 3.3. A morphomechanical reconstruction of a blastula-neurula period of amphibian's development, with some discources to other taxonomic groups 176 3.4. Developmental successions in Thecate hydroids (Cnidaria, Hydrozoa) 193 3.5. On morphocentric and genocentric approaches: harsh opposition or a hope for fruitful collaboration? 215 3.6. Summary of the chapter 220 Concluding remarks 222 References 226 Index 237 INTRODUCTION For anybody capable of an emotional response to it, any view of a developing organism should give birth to a feeling of amazement and even admiration, whether this development is seen directly, or in the form of a time lapse film, or even if mentally reconstructed from a series of static images. We ask ourselves how such seemingly primitive eggs or pieces of tissue, without any obvious intervention from outside, so regularly transform themselves into precisely constructed adult organisms. If we try to formulate what amazes us most of all about development, the answer will probably be that it is the internal capacity of developing organisms themselves to create new structures. How, then, can we satisfy our amazement in ways that are more or less reasonable, as well as scientifically valuable? This depends, first of all, on what position we choose to regard embryonic development as occupying among other structure creating processes, even including human activities. On the one hand, one might regard the development of organisms as a highly specialized class of processes, unique to themselves and alien to the general laws of nature, or at least not derivable from them and more akin to the deliberate acts of our own human behaviour. In that case our task would become reduced to a search for some specific 'instructions' for each next member of such a class. Whether in an overt or hidden form, some such ideology seems to dominate in present day developmental biology. On the other hand, meanwhile, a very different approach is possible, one which was suggested by the first of the quotations, that of von Baer who was one of the deepest thinkers in embryology, more than a century and a half ago. This alternative approach regards the formative powers of organisms as manifestations of a much wider set of structure creating activities governed by some universal laws to which both the living and the non-living parts of nature would be subject. As we hope to show in this book, our period of scientific history is probably the first in which such ideas can be converted into a set of definite research tasks, rather than remaining as mere romantic notions or philosophical maxims. And we shall begin this conversion by comparing and evaluating the broadest approaches used for comprehending and interpreting structures and the activities that generate them. Within the past few centuries the human mind has elaborated two extreme alternative ways for satisfying, as far as possible, the amazement that can result from the perception of new structures, both natural and man made ones. The first of these two alternatives can be called the aesthetic, or holistic, approach. This is the one which we amateurs instinctively use when perceiving either some work of creative art (whether it is a poem, a piece of music, or an architectural edifice) or remarkable natural events. As a rule we perceive such objects as fundamentally indivisible entities, which only specialists would have any interest (also quite carefully and, of course, only mentally) in dissecting into components. We know also that the main and most attractive property of any real artistic L. V. Beloussov, The Dynamic Architecture of a Developing Organism © Springer Science+Business Media Dordrecht 1998 2 INTRODUCTION creation (as well as a natural object) is a non-predictability of each spatial and/or temporal detail, its non-derivability from its neighbouring and/or a previous parts, with this non predictability even being increased with its further mental dissection. Another way of defining such non-derivability is to claim that objects of aesthetic value have a property of freedom. Certainly, such a freedom is never absolute: all artistic creations (not to say about natural events) are characterised by certain prohibitions. But these can never be codified in an absolutely strict manner (otherwise they would no longer belong to art) and they cannot be recognized by decomposing an object into pieces that are too small. Therefore, such a dissection should be qualified as useless from the heuristic point of view, and perhaps even a sort of crime. Much more can be gained, instead, by enlarging our scope, both in space and in time, for including into it what may be called the context of an observed object, that is, the set of other more or less similar objects, their historical or natural background, etc .. It is obvious, at the same time, that the role of the observer's (a listener's, a reader's) own individuality should be, within such an approach, quite important, active, and unique. No artistic creation has any value at all in the absence of those who perceive it adequately, and this value is changed from one person to another. You, my reader, have your own Beethoven symphony or Rembrandt picture, and I have another. A set of associations born in different persons which observe the same landscape may vary immensely. Within the act of such a perception, the artistic or natural creation and the perceiving individual are really fused together into a unique and indivisible whole. Quite another approach is used while dealing with the structures of any origin which we do not endow by any aesthetical, or holistic, qualities. Whether such structures fulfil or not some clearly outlined functions the usual, accepted way of satisfying our curiosity is now associated as a rule with a decomposition or a dissection of the structures into ever smaller elements, both spatially and temporally. By doing this we assume that the decomposition brings us towards recognition of such strict, unambiguous, and hence inevitable, relationships between the neighbouring elements or the successive events, which will permit us to 'derive' the origination of each spatial and/or temporal element from the preceding and/or neighbouring one. Correspondingly, we now consider the object of our interest as belonging to the 'inevitability world', in the sense that any traces of 'freedom' in its behaviour come to be regarded merely as reflections of deficiencies and gaps in our knowledge. A principle justification for such an approach, which we can call analytical, is belief in the existence of a one-to-one cause-effect correspondence between events which are temporarily and/or spatially adjacent. This is the central to a very influential epistemological principle, that of a uniform determinism, which will be discussed later on in more detail. We would now merely like to point out that by following such an approach the role of the observer becomes reduced to that of a skilled 'decomposer'. To the extent that we believe the result of a successful decomposition may be only one, any manifestations of an observer's individuality are, or course, rendered undesirable. But which of these alternative approaches, the aesthetic or the analytical, is most appropriate to the task of understanding the formation of structures by the developing organism? Over the last one or two centuries the answer has seemed quite obvious to most naturalists. "Nature is a workshop, rather than a temple, and a man is a worker in it" - as INTRODUCTION 3 the Russian plant physiologist Clement Timiryazev quite straightforwardly expressed it. Thus, any aesthetical criteria have been left very much behind by science, which has become almost completely identified with the analytical approach. Meanwhile, today we know, that the question looks far from simple. It is one of the main aims of this book to find a proper balance between the two trends. As a starting point we would like to remind ourselves that within centuries human beings employed, with a considerable success, a way that can be characterised a~ intermediate between the two extremes above described. This was the approach used by a person discovering a new land. On the one hand, in no way could he be satisfied simply by 'apprehending it as a whole' - at no one moment was he able to observe more than a small part of it. But, on the other hand, he had neither the desire nor the physical possibility of 'decompose' it. What he actually did was to describe, step by step, some of the more or less remarkable details of the landscape: sea shore~ river estuaries~ the most prominent hills~ etc .. Soon he realised that he must do two different, although related, things: first, select a scale (or a set of scales) for his description, and, second, establish reference point(s). This is a crucial moment, which, on the one hand, calls for some arbitrary individual decisions, but, on the other hand, requires good knowledge of the properties of the land explored. Consequently freedom of choice becomes intimately entangled with inevitability, as they do in many cases of further investigation. To select a scale means deliberately to ignore some structural details in favour of others, these becoming recorded as precisely as possible. But that need not prevent us from passing later to some other scale of observation, in which some other sets of elements will be targeted. In such ways we apprehend what is called a hierarchical structure of the object described. This raises entirely new questions about the inter relations between elements at different scales: a priori, these cannot be reduced to one-to one inevitable connections. Consider, for example, a river valley. The height of its banks depends, at one level, upon the molecular (crystal) properties of the rocks (in other words, depending on the events of a microscopic scale). At other levels, however, the valley'S orientation relative to the earth's axes, amongst many other macroscopic properties, also affects the heights of the banks. In both cases, however, the dependence is far from being as strict as is demanded by uniform determinism. A next crucial moment in the investigations comes when a discoverer realizes that that land not only has spatial, but also temporal structure, in other words a history. This is a transition from a uni-temporal geography to a multi-temporal geology. Comparable to the linear scales mentioned before, we will now find a hierarchy of temporal scales, and will discover that both are, as a rule, parallel to one another. Thus, some small components of a river valley can change their arrangement within a day or so~ larger components exhibit seasonal changes~ and even greater ones require climatic changes occurring over several centuries. Finally we come to the geological time scale. In such a way we have to consider our land as a set of loosely interconnected dynamic, rather than static, structures~ it is the totality of such structures that we may define as the dynamic architecture of the land. With such knowledge in hand we can make some predictions concerning the 'creative activity' of this land: its availability for establishing factories (or temples, contrary to Timiryazev's claim), or for developing agriculture, or navigation, or for predicting earthquakes. Note, meanwhile, that the things we predict are no more than possibilities, 4 INTRODUCTION or potencies, rather than something inevitable. Again, a component of freedom cannot be completely avoided. A potency itself is a notion with a very deep meaning which we will begin to discuss in Chapter 1. Lastly, we reach in our analysis of the dynamic architecture a rather dangerous point. While studying carefully and with the use of special equipment, for example, a water dynamics within a river valley, we come sooner or later to the conclusion that the river itself, the atmosphere above it, and the soil around it are far from being completely isolated entities; instead, they create a certain indivisible whole involved in the water turnover together with a number of other substances. Does this mean that our structural analysis was in vain? Such a conclusion would also be premature, A proper answer should be that the units which we have distinguished from each other are not, in fact, completely different and isolated entities. Instead, they should be qualified, in physical terms, as the singularities of a common dynamic field. Or, using the expression of David Bohm, an outstanding thinker of the recent past, "all is an unbroken and undivided whole movement... each thing is abstracted only as a relative invariant side or aspect of this movement" (Bohm, 1983). Let us now ask ourselves whether there really is much in common between a land surveyor's approach and that which would be largely adequate for the purposes of studying a developing organism. There is more, than it may seem at first glance. About half a century ago the British embryologist Conrad Waddington (1940) used the analogy of a mountain landscape (which he called the 'epigenetic landscape') for the purpose of representing his views, What he sought to represent by this analogy was exactly what we have called the dynamic architecture of development. Although this type of analogy has unfortunately failed to attract many proponents, we will try to extend this approach further. So far as we will be interested in the dynamic, which is to say the temporally extended, structures their time component will be of special interest to us. Within each time scale we will consider the history of an element (its more or less prolonged past) as a bearer of its active memory, 'pushing - in Bergson's terms, see the second quotation above - an element towards its future', In such a view, each moment of developmental time should be extended into the past (transformed into a finite 'metamoment', see Anisov, 1992) in order for its future to become at least loosely predictable. The plan of this book is as follows. We will start in Chapter 1 by reviewing briefly the main approaches used by the human mind for comprehending the formation of both non living and living structures in nature, We will follow the tortuous path of the evolution of such approaches in physics and biology which, as I hope, are at last converging towards one another after centuries of a mutual neglect and ignorance. Some ideas and notions recently developed within the social sciences will also be employed. After such an excursion in Chapter 2 we will return to biology in order to outline and describe one after another the dynamic structures of the different spatio-temporal levels. Next we will explore their interactions, paying special attention to the possibilities of establishing feedbacks between these different levels. This will permit us to make some generalizations formulated in the terms of a 'morphomechanics', This will bring us closer to our ultimate task: to examine how the dynamic structures of the different scales become integrated into a coherent multilevel hierarchy, which we will define as the dynamic INTRODUCTION 5 architecture or, in a more operational manner, as the developmental successions. Accordingly, the main aim of the Chapter 3 will be to explore a way for reconstructing the developmental successions in the different groups of organisms. The construction of the book permits a reader to select, according to his or her interests, some parts or chapters at the expense of others. Those who do not belong to the developmental biologists proper but are interested in the interdisciplinary connections and in the general scientific trends may restrict themselves by reading the first part of the book and the concluding remarks, missing all the rest. The second and the third chapters are, in contrast, more special. Yet these two parts, however, I have tried to construct in such a way as to make their qualitative conclusions as far as possible independent from mathematical formalism (which is minimized to the greatest possible extent). The process of writing this book has itself been for me kind of a 'temporally extended moment' of talking and discussing questions in my imagination with a number of persons, some of whom died as long as several decades ago, as well as with others who fortunately remain alive and active. Inspite of not sharing all their points of view, I am nevertheless indebted to them in everything. The person to be mentioned first of all should be my teacher Alexander Gurwitsch (1874-1954) who in my view was one of the greatest biological thinkers of the twentieth century, unfortunately too little known outside Russia. Amongst others, who have left us over the years I would like to remember Professors Alexander Liubishev, Pavel Svetlov, Vladimir Beklemishev, Anna Gurwitsch and the prematurely deceased brilliant researchers, Boris Belintzev and Vladimir Mescheryakov. And, finally, I would like to name the persons of a different age, whom I am happy to regard as my scientific friends, and who have enriched me so much by their ideas and views (but in no way are responsible for any possible shortcomings of this book). A very incomplete list of them includes Wolfgang Alt, Juergen Bereiter-Hahn, Vladimir Cherdantzev, Dmitry Chernavsky, Richard Cummings, Joe Frankel, Brian Goodwin, Albert Harris, Michael Lipkind, Jay Mittenthal, Fritz Popp, Guiseppe Sermonti and Alexander Stein. Amongst those, my special and deep thanks go to Albert Harris, who took a burden to look through a great part of the book, both from a linguistic and scientific point of view, and to Fritz Popp, an enthusiastical founder of the International Institute of Biophysics to which I am happy to belong. I would like also to express my thanks to my colleagues at the Faculty of Biology and, in particular, the Laboratory of Developmental Biophysics, Moscow State University, for maintaining an atmosphere of a mutual support and benevolence during all the time we have spent together.