The Embryonic Development of Drosophila melanogaster

236 Pages·1985·11.693 MB·English

by  José A. Campos-Ortega, Volker Hartenstein (auth.)

lose A. Campos-Ortega
Volker Hartenstein
The Embryonie
Development of
Drosophila melanogaster
With 85 Figures in 112 Separate IllustratiÖns
Springer-Verlag Berlin Heidelberg GmbH
JOSE A. CAMPOS-ORTEGA
VOLKER HARTENSTEIN
Institut für Entwicklungsphysiologie
der Universität zu Köln
Gyrhofstraße 17
5000 Köln 41, FRG
ISBN 978-3-662-02456-0 ISBN 978-3-662-02454-6 (eBook)
DOI 10.1007/978-3-662-02454-6
Library of Congress Cataloging in Publication Data. Campos-Ortega, Jose A. (Jose An
tonio), 1940- . The embryonic development of Drosophila melanogaster. Bibliogra
phy: p. I. Drosophila melanogaster - Development. 2. Embryology - Insects. I. Har
tenstein, Volker, 1957- . II. Title. QL958.C36. 1985. 595.77'4. 85-22069.
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© by Springer-Verlag Berlin Heidelberg 1985
Originally published by Springer-Verlag Berlin Heidelberg New York Tokyo in 1985
Softcover reprint of the hardcover 1 st edition 1985
The use of registered names, trademarks, etc. in this publication does not imply, even in
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Typesetting, printing, and binding: Konrad Triltsch, Graphischer Betrieb, Würzburg
2131/3130-543210
Dedicated to Donald F. Poulson
Preface
" ... but our knowledge is so weak that no
philosoph er will ever be able to completely
explore the nature of even a fly ... " *
Thornas Aquinas
"In Syrnbolurn Apostolorum" 079 RSV p/96
This is a monograph on embryogenesis of the fruit fly Drosophi
la melanogaster conceived as a reference book on morphology of
embryonie development. A monograph of this extent and con
tent is not yet available in the literature of Drosophila embryolo
gy, and we believe that there is areal need for it. Thanks to the
progress achieved during the last ten years in the fields of devel
opmental and molecular genetics, work on Drosophila develop
ment has considerably expanded creating an even greater need
for the information that we present here. Our own interest for
wildtype embryonie development arose several years ago, when
we began to study the development of mutants. While those
studies were going on we repeatedly had occasion to state in
sufficiencies in the existing literature about the embryology of
the wildtype, so that we undertook investigating many of these
problems by ourselves. Convinced that several of our colleagues
will have encountered similar difficulties we decided to publish
the present monograph.
Although not expressely recorded, Thomas Aquinas probably
referred to the domestic fly and not to the fruit fly. Irrespective
of which fly he meant, however, we know that Thomas was right
in any case. The situation today is not different from that in the
thirteenth century and certainly nobody would seriously claim
having completely investigated the "nature" of the fly. Conse
quently, in our work we did not intend to cover all possible as
pects of embryology, in particular we have purposely avoided
dealing with genetic aspects of development, restricting our
selves to morphology. We repeat, our intention was only to pro
vide basic information about the anatomy of normal embryogen
esis illustrating our description with figures of appropriate tech
nical standards.
In this book we have used a rather conventional distribution
of topics, similar to that of other embryological monographs. A
few of these topics, i.e. neurogenesis (Chap. 3), the pattern of
mitotic divisions of embryonie cells (Chap. 4), some aspects of
the morphogenetic movements (Chap.5) and the blastoderm
* The latin quotation is: " ... sed cognitio nostra est adeo debilis quod nul
lus philosophus potuit unquam perfecte investigare naturam unius mus
cae ... " (own free translation)
VIII Preface
fate map (Chap. 8), are based on studies by the authors and their
colleagues, the results of which have al ready appeared in dif
ferent form in other scientific journals. The third chapter deals
chiefly with organogenesis, although we have also considered in
some detail several aspects of the anatomical organization of the
larva which, in fact, do not strictly belong to embryogenesis; for
example, we have invested some effort in investigating the pat
tern of distribution of sensory organs, or peripheral nerves, or
muscles, etc. in the fully developed embryo.
Several persons and institutions have contributed to this
book. Chapter 2 presents a classification of embryogenetic stages
which is based on similar classifications of other authors. The
authorship of this chapter is actually shared by Christiane Nüss
lein-Volhard and Eric Wieschaus, with whom J. A. Campos-Or
tega defined the stages almost identically several years ago. The
work toward this manuscript was initiated at the Institut für Bio
logie III of the University of Freiburg i. Br., FRG, of which both
authors were staff members. Many friends and colleagues helped
us while working in Freiburg. The most important contribution
was by Sigrid Krien, our collaborator of over ten years, who pa
tiently prepared most of the material for this work. Important,
too, was the "moral" support of Rainer Hertel. Many of the
ideas presented in this book originated in discussions with
Ursula Dietrich, Fernando Jimenez, Gerd Jürgens, Ruth Leh
mann, Christiane Nüsslein-Volhard, Gerd Technau and Eric
Wieschaus. We would particularly like to thank Klaus Sander,
who repeatedly contributed with enlightening discussions on the
embryogenesis of insects, insisted about the convenience of
using an appropriate language, and critically read the entire
manuscript correcting several of its mistakes. Finally we want
to thank Gerd Technau for permission to quote his unpublished
results and for the micrographs of Fig.3.6A, and Alfonso
Martinez-Arias for a discussion on tracheal pits. Financial sup
port was provided by the Deutsche Forschungsgemeinschaft
(DFG, grants SFB 46, Ca 60/6-1, Ca 6017-1 and SFB 74).
Köln, September 1985 Jose A. Campos-Ortega
Volker Hartenstein
Contents
Introductory Remarks
Chapter 1 A Summary of Drosophila Embryogenesis 3
Chapter 2 Stages of Drosophila Embryogenesis 9
Stage I ... 10 Stage 6 ... 26 Stage 10 .. .43 Stage 14 ... 65
Stage2 ... 18 Stage 7 ... 31 Stagell ... 48 StageI5 ... 72
Stage3 ... 20 Stage8 ... 34 StageI2 ... 58 StageI6 ... 73
Stage 4 ... 22 Stage 9 ... 41 Stage 13 ... 59 Stage 17 ... 84
Stage 5 ... 24
Chapter 3 Histogenesis and Organogenesis 85
3.1 The Development of the Gut and Annexes 85
3.1.1 The Foregut . . . 86
3.1.2 The Salivary Glands 90
3.1.3 The Midgut . 91
3.1.4 The Hindgut . . . 97
3.2 The Gonads 98
3.3 Somatic and Visceral Musculature 103
3.3.1 The Muscle Pattern of aI-a7 . 106
3.3.2 The Muscle Pattern of tI-t3 . . . 108
3.3.3 The Muscle Pattern of a8-a9. . . 110
3.3.4 The Pattern of Cephalic Muscles 110
3.4 The Dorsal Vessel and the Fat Body 111
3.5 The Epidermis and Annexes 114
3.5.1 The Pattern of Early Ectodermal Mitoses 114
3.5.2 Cell Death . . . . . . . . . . . 115
3.5.3 Cell Differentiation in the Epidermis . . 115
3.5.4 Sensory Organs . . . . . . . . . . . 120
3.5.4.1 Development of Epidermal Sensory Organs
and Peripheral Nerves . . . . . . . 122
3.5.4.2 The Pattern of Sensory Organs of aI-a7 . . 125
3.5.4.3 The Pattern of Sensory Organs of tI-t3 . . 128
3.5.4.4 The Pattern of Sensory Organs of Gnathal
Segments. . . . . . . . . . . . . . . 129
3.5.4.5 The Pattern of Sensory Organs of the Foregut 134
3.5.4.6 The Pattern of Sensory Organs of a8 and Telson 137
x
Contents
3.6 The Trajectory ofPeripheral Nerves 138
3.6.1 The Nerves of al-a7 138
3.6.2 The Nerves of tl-t3 . . . . . . . 140
3.6.3 Gnathal Nerves . . . . . . . . . 141
3.6.4 Cerebral (Supraoesophageal) Nerves 143
3.6.5 Nerves of aB and Telson . . . .. 144
3.7 Neurogenesis . . . . . . . . . . 144
3.7.1 The Formation ofthe Neurogenic Region. 148
3.7.2 The Segregation ofNeuroblasts . . . 150
3.7.3 The Pattern of Germ Band Neuroblasts . . 152
3.7.4 Neuronal Differentiation . . . . . . . . 157
3.8 The Ring Gland and the Stomatogastric Nervous
System ..... . 159
3.9 The Tracheal Tree . . . . . . . . . . . . . . 162
Chapter 4 The Pattern of Embryonie Cell Divisions . .. 165
4.1 The Pattern ofthe First Postblastoderm Mitosis . 166
4.2 The Pattern ofthe Second Postblastoderm Mitosis 168
4.3 The Pattern ofthe Third Postblastoderm Mitosis 169
4.4 The Orientation of Mitotic Spindies . . . . .. 170
Chapter 5 Morphogenetic Movements. . . . . . 172
5.1 Gastrulation .' . . . . . . . . . . . . 173
5.2 The Cephalic and the Transversal Furrows 180
5.3 Germ Band Elongation. . . . . . . . . 181
5.4 The Behaviour of Blastoderm Cells During Early
Morphogenetic Movements . . . . . . . 181
5.5 Morphogenetic Movements Associated with
Organogenesis . . . . . 182
5.6 Germ Band Shortening . 183
5.7 Dorsal Closure . . . . 184
Chapter 6 Cephalogenesis . 185
6.1 Early Events . . 185
6.1.1 Cephalic Furrow 185
6.1.2 Gnathal Segments 186
6.1.3 Procephalon . . 190
6.2 Atrium, Cephalopharyngeal Skeleton
and Frontal Sac . . . . . . . . . . 190
6.3 Atrium Formation and Head Involution 194
Contents XI
Chapter 7 So me Aspects of Segmentation 198
7.1 Pattern Elements . . . . . . . 198
7.1.1 Segmental Borders. . . . . . . 199
7.1.2 Relationships Between Ventral Cord Commissures
and Metamerie Boundaries . . . . 199
7.1.3 Non-Innervated Cutieular Struetures 201
7.1.4 Epidermal Sensory Organs 201
7.1.5 Peripheral Nerves . . . . . . . . 203
7.1.6 Pattern of Muscles. . . . . . . . 204
7.2 Homologies and Differenees Between Segments 204
7.3 Embryology of Segmentation . . 206
Chapter 8 A Fate Map of the Blastoderm 210
8.1 The Fate Map. . . . . . . . . 211
8.2 The Rationale of Fate Map Construetion 213
8.3 The Size of the Blastoderm Anlagen 214
8.3.1 The Mesoderm and the Endoderm 214
8.3.2 The Hindgut and the Terminalia. . 215
8.3.3 The Amnioserosa . . . . . . . . 215
8.3.4 The Thoraeie and Abdominal Epidermis 216
8.3.5 The Gnathal Segments and the Foregut . 216
8.3.6 The Procephalon . . . . . . . . . . 217
References . 218
Subject Index 223
Introductory Remarks
The importance of Drosophila melanogaster for biological research does not
need to be expressly emphasized; it has been sufficiently demonstrated and
documented on a multitude of occasions during the last 80-85 years in which
the fruit fly has been used in experimental work (Allen 1975, 1978). Due to its
very elaborate genetics, the fruit fly is now one of the animals preferred to ap
proach most problems in developmental biology.
The aptitude of Drosophila for embryogenetic studies, and in particular the
property of allowing genetic dissection of embryonic development, was recog
nized almost 50 years aga by Poulson (1937a, 1940, 1943, 1945), who studied
the effects of a few chromosomal deficiencies on embryonic development. In
fact, more important than describing the effects of the lack of certain genes on
development was Poulson's contribution towards establishing the genetic ap
proach to embryogenesis on firm grounds. Poulson was among the first who ex
pressely claimed that genes are involved in directing developmental processes,
on the same line as Goldschmidt's Physiological Genetics (1927, 1938), and
called the attention of experimentors to deficiencies and other chromosomal
mutations with lethai effects on the homozygous animals as tools for investigat
ing the contribution of genes to embryonic development (Poulson 1943, 1945).
The genetic approach to embryonic development has recently experienced
considerable impulses. However, this is certainly not the appropriate place for a
critical appraisal of the new data; it suffices comparing Wright's (1970) stan
dard review on the genetics of embryogenesis in Drosophila with some of the
pertinent, up-to-date papers on aspects of the same topic (e.g. Lewis 1978,
N üsslein-Volhard et al. 1982), to realize how profound progress in this field,
both from the conceptual and the material point ofview, has been.
In the past, studies on embryonic development of Drosophila have gone
hand in hand with the analysis of mutants. Published work on normal embryo
genesis ofthe fruit fly was, and still is, very scarce, at least when compared to the
literature available on genetic and other experimental aspects of Drosophila
embryogenesis. The very promising foundation of modern embryology of dip
terious insects that" represents Weismann's contribution (1983; see Sander
1985a, for a critical appraisal of Weismann's studies on insect development)
was unfortunately followed by only a few glimpses (e.g. Poulson 1950, Son
nenblick 1950, Schoeller 1964, Anderson 1962, 1972). The reader will find most
of these papers cited throughout the pages of this book. The sm all size of the
Drosophila egg, and the technical difficulties associated with it (for example,
the lack during many years of reliable fixation methods for histological analy
ses other than pricking or damaging the egg's integrity), is certainly one of the
reasons for the paucity of publications on normal embryogenesis of the fruit fly.