The Ciba Foundation for the promotion of international cooperation in medical and chemical research is a scientific and educational charity established by CIBA Limited-now CIBA-GEIGY Limited-Basle. The Foundation operates independently in London under English trust law. Ciba Foundation Symposia are published in collaboration with Associated Scientific Publishers (Elsevier Scientific Publishing Company, Excerpta Medica, North-Holland Publishing Company) in Amsterdam. Associated Scientific Publishers, P.O. Box 21 1, Amsterdam Cell Patterning Cell Patterning Ciba Foundation Symposium 29 (new series) 1975 - Elsevier Excerpta Medica North-Holland - Associated Scientific Publishers Amsterdam Oxford New York 0 Cop,vright 1975 Ciba Foundation All rights reserved. No part of this publication may be reproduced, stored in a retrieval system or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording, or otherwise, without permission in writing from the publishers. ISBN Excerpta Medica 90 219 4032 9 ISBN American Elsevier 0444-15148-6 Published in 1975 by Associated Scientific Publishers, P.O. Box 211, Amsterdam, and American Elsevier, 52 Vanderbilt Avenue, New York, N.Y. 10017. Suggested series entry for library catalogues: Ciba Foundation Symposia. Suggested publisher’s entry for library catalogues: Associated Scientific Publishers. Ciba Foundation Symposium 29 (new series) Published February 1975 Printed in The Netherlands by Van Gorcurn, Assen Contents S. BRENNER Chairman’s introduction 1 P. A. LAWRENCE The structure and properties of a compartment border: the intersegmental boundary in Oncopeltus 3 Discussion I6 J. FRANKEL Pattern formation in ciliary organelle systems of ciliated protozoa 25 Discussion 44 P. SENGEL Feather pattern development 51 Discussion 66 P. J. BRYANT Regeneration and duplication in imaginal discs 71 Discussion 90 L. WOLPERTJ., LEWIS & D. SUMMERBELL Morphogenesis of the vertebrate limb 95 Discussion 1 19 R. K. HUNT Developmental programming for retinotectal patterns 131 Discussion 150 A. GARC~A-BELLIDO Genetic control of wing disc development in Drosophila 161 Discussion 178 R. L. GARDNER & M. H. JOHNSON Investigation of cellular interaction and deployment in the early mammalian embryo using interspecific chimaeras between the rat and mouse 183 Discussion 196 VI CONTENTS s. KAUFFMAN Control circuits for determination and transdetermination : interpreting positional information in a binary epigenetic code 201 Discussion 21 5 J. B. GURDON Attempts to analyse the biochemical basis of regional differences in animal eggs 223 Discussion 234 K. SANDER Pattern specification in the insect embryo 241 Discussion 256 I. A. MEINERTZHAGEN The development of neuronal connection patterns in the visual systems of insects 265 Discussion 283 R. F. MARK Topography and topology in functional recovery of regenerated sensory and motor systems 289 Discussion 307 R. B. MARCHASE, A. J. BARBERA & s. ROTH A molecular approach to retinotectal specificity 3 15 Discussion 321 s. BRENNER Closing remarks: the genetic outlook 343 Index of contributors 347 Subject index 348 Participants Symposium on Cell Patterning held at the Ciba Foundation, London, 21st-23rd May 1974 Chairman: s. BRENNER MRC Laboratory of Molecular Biology, University Postgraduate Medical School, Hills Road, Cambridge CB2 2QH. P. J. BRYANT Center for Pathobiology, School of Biological Sciences, Uni- versity of California, Irvine, Calif. 92664, USA. J. FRANKEL Department of Zoology, University of Iowa, Iowa City, Iowa 52242, USA A. GARC~A-BELLIDO CSIC, Instituto de Genttica y Antropologia, Velazquez 144, Madrid 6, Spain R. L. GARDNER Department of Zoology, South Parks Road, Oxford OX1 3PS R. M. GAZE Division of Developmental Biology, National Institute for Medical Research, Mill Hill, London NW7 1AA J. B. GURDON MRC Laboratory of Molecular Biology, University Post- graduate Medical School, Hills Road, Cambridge CB2 2QH R. K. HUNT Department of Anatomy and Institute of Neurological Sciences, University of Pennsylvania Medical School, Philadelphia, Pa. 17104, USA M. JACOBSON Department of Physiology and Biophysics, University of Miami School of Medicine, P.O. Box 875, Biscayne Annex, Miami, F1. 33151, USA S. A. KAUFFMAN National Cancer Institute, Department of Health, Education and Welfare, Public Health Service, National Institutes of Health, Bethesda, Maryland 20014, USA VIII PARTICIPANTS M. J. KEATING Division of Developmental Biology, National Institute for Medical Research, Mill Hill, London NW7 1AA P. A. LAWRENCE MRC Laboratory of Molecular Biology, University Post- graduate Medical School, Hills Road, Cambridge CB2 2QH J. LEWIS Department of Biology as Applied to Medicine, The Middlesex Hospital Medical School, London W1P 6DB R. F. MARK Physiology Department, Monash University, Clayton, Victoria 3 168, Australia I. A. MEINERTZHAGEN The Biological Laboratories, Harvard University, 16 Divinity Avenue, Cambridge, Mass. 02138, USA G. MITCHISON MRC Laboratory of Molecular Biology, University Postgradu- ate Medical School, Hills Road, Cambridge CB2 2QH J. D. PITTS Department of Biochemistry, University of Glasgow, Glasgow G12 8QQ M. RAFF Zoology Department, University College London, Gower Street, London WC1 E 6BT s. A. ROTH Mergenthaler Laboratory for Biology, The Johns Hopkins Uni- versity, Baltimore, Maryland 2121 8, USA K. SANDER Biologisches Institut 1 (Zoologie) der Albert-Ludwigs Universitat, 78 Freiburg im Breisgau, Katharinenstrasse 20, Germany L. SAXBN I11 Department of Pathology, University of Helsinki, SF-00290 Helsinki, Finland P. SENGEL Laboratoire de Zoologie, UniversitC Scientifique & MCdicale de Grenoble, Boite postale 53, 38041 Grenoble, France J. B. TUCKER Department of Zoology, Bute Buildings, The University, St. Andrews KY16 9AJ L. WOLPERT Department of Biology as Applied to Medicine, The Middlesex Hospital Medical School, London W1P 6DB Editors: RUTH PORTER and JOHN RIVERS Cell Patterning RUTH PORTER and JOHNRIVERS Copyright 0 Ciba Foundation Chairman’s introduction S. BRENNER MRC Laboratory of Molecular Biology, Cambridge I think we may have a rather difficult few days ahead of us: there is a lot to assimilate, much of which may be unfamiliar to people working in special fields. We shall be discussing a variety of different experimental systems and organisms, and there will be a number of different ways, often intricate, of doing experiments. Interspersed between these descriptions will be speculations about the possible mechanisms involved. I should therefore like to ask speakers to make clear, as briefly as possible, exactly what sorts of experiments they have done and can do and to try to keep separate the experimental facts from the interpretations of them. If we can do this, we may be able to establish some communication between those who work with slime moulds and those who work with embryos and developing nerves. In addition may I remind those who work on the nervous system, that not many people are uufuit with the behavioural and electrophysiological experiments which you do and you may have to provide us with some background. You will see from the programme that we are not following a Linnaean order; we shall not have an insect day or an avian day, and this means that we may have to discuss the same thing several times. For example, the opening talk by Dr Lawrence on compartment borders in Oncopeltus is linked with Dr Garcia-Bellido’s talk on Drosophilu, and thereafter we shall move down the scale to Protozou. One last point-it would be helpful if speakers were to mention the size of the objects they are working with; just say whether it is micrometres, milli- metres or miles. I Cell Patterning RUTH PORTER and JOHNRIVERS Copyright 0 Ciba Foundation The structure and properties of a compartment border: the intersegmental boundary in Oncopeltus PETER A. LAWRENCE MRC Laboratory of Molecular Biology, University Postgraduate Medical School, Cambridge Abstract Garcia-Bellido et al. have described how groups of cells in developing Drosophila become subdivided into ‘compartments’. Cells within any compart- ment have rigid prospective fates such that, while their progeny may give rise to variable regions within a compartment, they can never generate cells in any other compartment. Analysis of the position and shapes of clones allows definition of the compartment boundaries. I report studies on a compartment boundary (likewise demonstrated by clonal analysis) in the hemipteran insects Oncopeltus and Rhodnius. The advantage of this border is that it can easily be identified in the light and electron microscopes. There is an abrupt change of cell shape at the border, which has been analysed by means of serial electron microscope sections. The types of cell junctions at the border and elsewhere are compared and shown to have no qualitative differ- ences. The border is an effective barrier to the growth of peripheral sensory axons, although not apparently to dendrites. The intersegmental boundary allows passage of information relating to cuticle deposition, wounding response, tracheolar movement and intercellular coupling. Making wounds across the border leads to greater effects on polarity of epidermal cells than making similar wounds elsewhere on the tergites. COMPARTMENTS Methods for analysing growth of insects by means of genetically marked clones have been developing rapidly. The ability of X-rays to induce a high rate of somatic crossing over, as well as the existence of mutants which mark the cuticular secretion of each cell, has permitted a sophisticated analysis of cell lineage in Drosophila. Irradiation of staged eggs and larvae has shown that, progressively during development, groups of cells acquire particular properties which affect their behaviour and the behaviour of the clones of progeny that each cell generates. This is expressed partly in the shape of the clones: for example, it was noted (Garcia-Bellido 1968; Bryant 1970; Garcia-Bellido & 3