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Insect Physiology and Biochemistry
Insect Physiology and Biochemistry
Fourth Edition
James L. Nation, Sr.

Fourth edition published 2022
by CRC Press
6000 Broken Sound Parkway NW, Suite 300, Boca Raton, FL 33487-2742
and by CRC Press

4 Park Square, Milton Park, Abingdon, Oxon, OX14 4RN
CRC Press is an imprint of Taylor & Francis Group, LLC
© 2022 James L. Nation, Sr.
Reasonable efforts have been made to publish reliable data and information, but the author and publisher cannot assume responsibility for the
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without intent to infringe.
ISBN: 978-1-032-24704-5 (hbk)

ISBN: 978-1-032-24706-9 (pbk)
ISBN: 978-1-003-27982-2 (ebk)
DOI: 10.1201/9781003279822
Typeset in Times
by codeMantra
Dedication
I dedicate this edition to my parents, Virgil and Ruby Nation, who always
encouraged, supported, and believed in me, and to my wife, Dorothy, and our
children, Marie, Jim, and Patti, all of whom have greatly enriched my life.
Contents
Preface.................................................................................................................................................................................xix
Author Biography................................................................................................................................................................xxi
Chapter 1 Embryogenesis .................................................................................................................................................1

1.1 Introduction ...........................................................................................................................................1
1.2 Morphogenesis.......................................................................................................................................1
1.2.1 Egg, Fertilization, and Zygote Formation ................................................................................1
1.2.2 Variations in Zygotic Nucleus Cleavage, Formation of Energids, and
Blastoderm Formation ..............................................................................................................3
1.2.2.1 Apterygota ................................................................................................................4
1.2.2.2 Hemimetabola...........................................................................................................5
1.2.2.3 Holometabola ............................................................................................................6
1.2.3 Formation of the Germ Band ................................................................................................... 6
1.2.4 Gastrulation ..............................................................................................................................7
1.2.5 Germ Band Elongation .............................................................................................................8
1.2.6 Blastokinesis and Extraembryonic Membranes .......................................................................8
1.3 Genetic Control of Embryogenesis ...................................................................................................... 11
1.3.1 Development of a Model for Patterning ................................................................................. 12
1.3.1.1 The bicoid Gene and Anterior Determination in Drosophila ................................ 12
1.3.1.2 Posterior Group Genes and Posterior Pattern Formation ....................................... 13
1.3.1.3 Genes Required in the Acron and Telson ............................................................... 14
1.3.1.4 Dorsal–Ventral Axis ............................................................................................... 14
1.4 Segmentation Genes ............................................................................................................................ 14
1.5 Homeotic Genes .................................................................................................................................. 15
1.5.1 Homeobox .............................................................................................................................. 16
1.6 Organogenesis ..................................................................................................................................... 16
1.6.1 Neurogenesis .......................................................................................................................... 16
1.6.2 Development of the Gut.......................................................................................................... 17
1.6.3 Malpighian Tubules ................................................................................................................ 17
1.6.4 Tracheal System ..................................................................................................................... 17
1.6.5 Oenocytes ............................................................................................................................... 17
1.6.6 Wing Development ................................................................................................................. 17
1.6.7 Cuticle Secretion in the Embryo ............................................................................................ 18
1.6.8 Cell Movements During Embryogenesis................................................................................ 18
1.6.9 Programmed Cell Death: Apoptosis ...................................................................................... 18
1.7 Hatching .............................................................................................................................................. 18
1.8 Imaginal Discs ..................................................................................................................................... 18
1.9 Summary and Conclusions ..................................................................................................................20
1.10 Review and Self-Study Questions ....................................................................................................... 21
References Added to 4th Edition .................................................................................................................... 21
Foundation References ................................................................................................................................... 23
Chapter 2 Digestion......................................................................................................................................................... 27
2.1 Introduction ......................................................................................................................................... 27
2.2 Relationships between Food Habits and Gut Structure and Function ................................................. 27
2.2.1 Plant vs. Animal Origin: Solid vs. Liquid Diet ...................................................................... 27
2.3 Major Structural Regions of the Gut ...................................................................................................28
2.3.1 Foregut....................................................................................................................................28
2.3.2 Midgut .................................................................................................................................... 30
2.3.3 Hindgut ................................................................................................................................... 30
vii
viii Contents
2.4 Midgut Cell Types ............................................................................................................................... 31

2.4.1 Columnar Cells....................................................................................................................... 31
2.4.2 Regenerative Cells .................................................................................................................. 31
2.4.3 Goblet Cells ............................................................................................................................ 32
2.5 Microvilli or Brush Border of Midgut Cells ....................................................................................... 33
2.6 Glycocalyx ...........................................................................................................................................34
2.7 Peritrophic Matrix ...............................................................................................................................34
2.7.1 Functions of the Peritrophic Matrix ....................................................................................... 35
2.8 Digestive Enzymes .............................................................................................................................. 36
2.8.1 Carbohydrate-Digesting Enzymes ......................................................................................... 37
2.8.2 Lipid Digesting Enzymes ....................................................................................................... 37
2.8.3 Protein-Digesting Enzymes.................................................................................................... 37
2.8.4 Do Proteinase Inhibitors in the Food Influence Evolution of Proteinase Secreted? .............. 38
2.9 Hormonal Influence on Midgut ........................................................................................................... 39
2.10 Countercurrent Circulation of Midgut Contents and Absorption of Digested Products .....................40
2.11 Transepithelial and Oxidation–Reduction Potential of the Gut .......................................................... 41
2.12 Gut pH ................................................................................................................................................. 42
2.13 Hematophagy: Feeding on Vertebrate Blood ......................................................................................44
2.14 Digestive System Morphology and Physiology in Major Insect Orders .............................................44
2.14.1 Orthoptera ..............................................................................................................................44
2.14.2 Dictyoptera .............................................................................................................................44
2.14.3 Isoptera ................................................................................................................................... 45
2.14.4 Hemiptera ............................................................................................................................... 45
2.14.5 Homoptera ..............................................................................................................................46
2.14.6 Coleoptera ..............................................................................................................................46
2.14.7 Hymenoptera ..........................................................................................................................46
2.14.8 Diptera .................................................................................................................................... 47
2.14.9 Lepidoptera............................................................................................................................. 47
2.15 Insect Gut as a Potential Target for Population Management and Control of the Spread of
Plant and Animal Disease Organisms .................................................................................................48
2.16 Summary/Conclusions .........................................................................................................................48
Foundation References ...................................................................................................................................51
Chapter 3 Nutrition ......................................................................................................................................................... 57

3.1 Introduction ......................................................................................................................................... 57
3.2 Importance of Balance and Self-Selection of Nutritional Components .............................................. 58
3.3 Ability of Insects to Self-Select Nutritional Components ................................................................... 59
3.4 Requirements for Specific Nutrients ...................................................................................................60
3.4.1 Nitrogen Source: Proteins and Amino Acids .........................................................................60
3.4.2 Amino Acids .......................................................................................................................... 61
3.4.3 Carbohydrates......................................................................................................................... 62
3.4.4 Lipids ...................................................................................................................................... 63
3.4.5 Sterols ..................................................................................................................................... 63
3.4.6 Polyunsaturated Fatty Acids ..................................................................................................64
3.4.7 Vitamins .................................................................................................................................64
3.4.8 Minerals ................................................................................................................................. 65
3.5 Techniques and Dietary Terms Used in Insect Nutrition Studies ....................................................... 67
3.6 Criteria for Evaluating Nutritional Quality of a Diet .......................................................................... 67
3.7 Measures of Food Intake and Utilization ............................................................................................ 67
3.8 Phagostimulants................................................................................................................................... 68
3.9 Feeding Deterrents .............................................................................................................................. 69
3.10 Summary and Conclusions .................................................................................................................. 70
Foundation References ................................................................................................................................... 72
Contents ix
Chapter 4 Integument and Molting ................................................................................................................................. 77

4.1 Introduction ......................................................................................................................................... 77
4.2 Structure of the Integument................................................................................................................. 77
4.2.1 Cuticulin Envelope ................................................................................................................. 78
4.2.2 Epicuticle ................................................................................................................................ 78
4.2.3 Procuticle ................................................................................................................................ 78
4.2.4 Pore Canals and Wax Channels ............................................................................................. 79
4.2.5 Epidermal Cells ...................................................................................................................... 79
4.3 Molting and Formation of New Cuticle............................................................................................... 82
4.3.1 Apolysial Space ...................................................................................................................... 83
4.3.2 Molting Fluid Secretion.......................................................................................................... 83
4.3.3 New Cuticle Formation .......................................................................................................... 83
4.3.4 Reabsorption of Molting Fluid ...............................................................................................84
4.4 Ecdysis .................................................................................................................................................84
4.4.1 Shedding the Old Cuticle: Ecdysis of the Adult ..................................................................... 86
4.4.2 Post-Ecdysis Wing Expansion and Water Proofing the New Cuticle ..................................... 87
4.4.3 Sclerotization of Cuticle ......................................................................................................... 87
4.5 Chemical Composition of Cuticle .......................................................................................................90
4.5.1 Chitin ...................................................................................................................................... 91
4.5.2 Biosynthesis of Chitin ............................................................................................................ 93
4.5.3 Cuticular Proteins................................................................................................................... 95
4.5.4 Resilin.....................................................................................................................................96
4.5.5 Stage-Specific Differences in Cuticle Proteins ......................................................................97
4.5.6 Protective Functions of Cuticle Proteins ................................................................................97
4.5.7 Cuticular Lipids ...................................................................................................................... 98
4.6 Mineralization of Insect Cuticles ........................................................................................................99
4.7 Capture of Atmospheric Water on Cuticular Surfaces ...................................................................... 100
4.8 Summary and Conclusions ................................................................................................................ 100
4.9 Review and Self-Study Questions ..................................................................................................... 101
References Added to 4th Edition .................................................................................................................. 101
Foundation References ................................................................................................................................. 102
Chapter 5 Hormones and Development ........................................................................................................................ 107

5.1 Introduction ....................................................................................................................................... 107
5.2 Interplay of PTTH, Ecdysteroids, and Juvenile Hormone Controls Development ........................... 107
5.3 Brain Neurosecretory Cells and Prothoracicotropic Hormone (PTTH) ........................................... 111
5.3.1 Source and Chemistry .......................................................................................................... 111
5.3.2 Bioassay for PTTH Activity ................................................................................................. 111
5.3.3 Stimuli for Secretion of PTTH ............................................................................................. 112
5.3.4 Secretion of PTTH after Brain Activation by Stretch Receptors ......................................... 113
5.3.5 Gated PTTH Secretion in Tobacco Hornworm .................................................................... 113
5.3.6 Secretion of PTTH after Brain Activation by Cold Exposure ............................................. 113
5.3.7 Regulation of Tissue and Hemolymph Levels of PTTH ...................................................... 114
5.3.8 Mode of Action of PTTH ..................................................................................................... 114
5.4 Prothoracic Glands and Ecdysteroids ................................................................................................ 114
5.4.1 Biosynthesis of Ecdysone ..................................................................................................... 116
5.4.2 Conversion of Ecdysone into 20-Hydroxyecdysone............................................................. 117
5.4.3 Molecular Diversity in the Structure of the Molting Hormone............................................ 118
5.4.4 Assays for Ecdysteroids........................................................................................................ 118
5.4.5 Radioimmunoassay for Ecdysone and Related Ecdysteroids............................................... 119
5.4.6 Assay by Physicochemical Techniques ................................................................................ 119
5.4.7 Tissues and Cell Cultures Used in Assays ........................................................................... 120
5.4.8 Degradation of Ecdysone ..................................................................................................... 121
5.4.9 Virus Degradation of Host Ecdysteroids.............................................................................. 121
5.4.10 Dependence of Some Parasitoids on Host Ecdysteroids ...................................................... 121
5.5 Corpora Allata and Juvenile Hormones ............................................................................................ 121
x Contents
5.5.1 Glandular Source and Chemistry of Juvenile Hormones ..................................................... 121

5.5.2 Assays for JH Activity.......................................................................................................... 123
5.5.3 Regulation of the Tissue and Hemolymph Levels of JH ...................................................... 123
5.5.4 Growth Regulators and Compounds Cytotoxic to the Corpora Allata ................................ 125
5.5.5 Cellular Mode of Action and Receptors for JH.................................................................... 127
5.5.6 Downstream Transcription Factors ...................................................................................... 129
5.6 Mode of Action of Ecdysteroids at the Gene Level........................................................................... 129
5.6.1 Chromosomal Puffs.............................................................................................................. 129
5.6.2 Identification and Isolation of an Ecdysteroid Receptor ...................................................... 131
5.6.3 Differential Tissue and Cell Response to Ecdysteroids ....................................................... 132
5.7 Possible Timer Gene in the Molting Process..................................................................................... 133
5.8 Ecdysone–Gene Interaction Ideas Stimulated Vertebrate Work ....................................................... 134
5.9 Development of Eyespots in Wings of Lepidoptera .......................................................................... 134
Chapter 6 Biological Rhythms ...................................................................................................................................... 143

6.1 Introduction ....................................................................................................................................... 143
6.2 Characteristics of Circadian and Photoperiodic Rhythms ................................................................ 143
6.3 Molecular Basis for the Circadian Clock .......................................................................................... 144
6.4 Evidence for Clock Genes in Many Insects....................................................................................... 146
6.4.1 Circadian Regulation of Hormone Secretion ....................................................................... 148
6.4.2 Circadian Clock Influence in Peripheral Organs and Tissues.............................................. 149
6.4.3 Circadian Clock Influence in Social Behavior of Honeybees .............................................. 150
6.4.4 Circadian Clock Influence in Reproduction ......................................................................... 150
6.5 Photoperiodic Response: One Clock, Two Clocks, or Multiple Clocks?........................................... 153
6.6 Clock Models Based on Experimental Responses of Insects to Varying Light/Dark Regimes ....... 154
6.6.1 Hourglass Model .................................................................................................................. 155
6.6.2 External Coincidence Model ................................................................................................ 155
6.6.3 Internal Coincidence Model ................................................................................................. 156
6.6.4 Resonance Model ................................................................................................................. 156
6.6.5 Summary Results from Model Experiments........................................................................ 156
Chapter 7 Diapause ....................................................................................................................................................... 165

7.1 Introduction ....................................................................................................................................... 165
7.2 Diapause: A Survival Strategy .......................................................................................................... 165
7.3 Phases of Diapause ............................................................................................................................ 167
7.3.1 Prediapause: Induction and Preparation............................................................................... 168
7.3.2 Diapause: Initiation and Maintenance.................................................................................. 169
7.3.3 Diapause Termination .......................................................................................................... 169
7.4 Hormonal Control of Diapause ......................................................................................................... 169
7.4.1 Embryonic Diapause ............................................................................................................ 169
7.4.2 Larval Diapause ................................................................................................................... 170
7.4.3 Pupal Diapause ..................................................................................................................... 170
7.4.4 Adult Diapause/Reproductive Diapause .............................................................................. 171
7.5 Role of Daily and Seasonal Biological Clocks in Diapause .............................................................. 172
7.6 Diapause and Gene Expression ......................................................................................................... 172
7.7 Nutrient Accumulation for Diapause and the Storage and Conservation of Nutrients
During Diapause ................................................................................................................................ 172
Contents xi
7.8 Molecular Studies of Diapause .......................................................................................................... 173

7.9 A Pre-Diapause Strategy – Cold Tolerance ....................................................................................... 174
Chapter 8 Intermediary Metabolism............................................................................................................................. 181

8.1 Introduction ....................................................................................................................................... 181
8.2 Energy Demands for Insect Flight .................................................................................................... 182
8.3 Metabolic Stores ................................................................................................................................ 183
8.3.1 Carbohydrate Resources ...................................................................................................... 183
8.3.1.1 Trehalose Resources ............................................................................................. 183
8.3.1.2 Glycogen: Storage and Synthesis .......................................................................... 185
8.4 Hormones Controlling Carbohydrate Metabolism ............................................................................ 186
8.5 Pathways of Metabolism Supporting Intense Muscular Activity, Such as Flight ............................. 186
8.5.1 Glycolysis ............................................................................................................................. 186
8.5.1.1 The Glycerol-3-Phosphate Shuttle and Regeneration of NAD+ ............................ 188
8.5.1.2 Significance and Control of the Glycerol-3-Phosphate Shuttle ............................ 190
8.5.2 The Krebs Cycle ................................................................................................................... 190
8.5.2.1 Control of Krebs Cycle Metabolism and Regulation of Carbohydrate
Metabolism in Flight Muscles .............................................................................. 192
8.5.3 The Electron Transport System ............................................................................................ 192
8.5.4 Proline as a Fuel for Flight ................................................................................................... 194
8.5.5 Mobilization and Use of Lipids for Flight Energy ............................................................... 197
8.5.5.1 Transport of Lipids by Lipophorin .......................................................................200
8.5.5.2 Activation of Fatty Acids, Entry into Mitochondria, and β-Oxidation ................ 201
8.6 Summary and Conclusions ................................................................................................................202
8.7 Review and Self-Study Questions .....................................................................................................203
Foundation References .................................................................................................................................204
Chapter 9 The Nervous System: Anatomy and Physiology ..........................................................................................207

9.1 Introduction .......................................................................................................................................207
9.2 Central Nervous System (CNS) .........................................................................................................208
9.3 The Brain ...........................................................................................................................................208
9.3.1 Protocerebrum ......................................................................................................................209
9.3.2 Deutocerebrum ..................................................................................................................... 211
9.3.3 Tritocerebrum ....................................................................................................................... 211
9.4 Ventral Ganglia.................................................................................................................................. 212
9.5 Oxygen and Glucose Supply to the Brain and Ganglia ..................................................................... 213
9.6 The Neuropil...................................................................................................................................... 213
9.7 Hemolymph–Brain (CNS) Barrier .................................................................................................... 213
9.8 Neurons: Building Blocks of a Nervous System ............................................................................... 214
9.8.1 Afferent or Sensory Neurons ............................................................................................... 214
9.8.2 Efferent or Motor Neurons ................................................................................................... 214
9.8.3 Interneurons ......................................................................................................................... 215
9.8.4 Glial Cells............................................................................................................................. 215
9.9 Nerve Cell Responses to Stimuli ....................................................................................................... 216
9.9.1 Graded Responses ................................................................................................................ 216
9.9.2 Spike Potentials .................................................................................................................... 216
9.10 The Physiological Basis for Neuronal Responses to Stimuli ............................................................ 216
9.10.1 Membrane Ion Channels: Bioelectric Potentials .................................................................. 216
9.10.2 The Resting Potential ........................................................................................................... 219
9.10.3 The Action Potential: Sodium Activation ............................................................................ 220
xii Contents
9.10.4 Sodium Inactivation and Repolarization .............................................................................. 221

9.10.5 Measurement of Ion Fluxes: Voltage Clamp Technique ...................................................... 222
9.10.6 Conduction of the Action Potential: Local-Circuit Theory ................................................. 222
9.11 The Synapse: Excitatory and Inhibitory Postsynaptic Potentials ...................................................... 223
9.11.1 Acetylcholine-Mediated Synapses .......................................................................................224
9.11.2 Nicotinic and Muscarinic Receptors in Insects ................................................................... 225
9.11.3 Electric Transmission across Synapses ................................................................................ 225
9.11.4 Neuromuscular Junctions ..................................................................................................... 226
Chapter 10 The Nervous System: Selected Roles in Behavior ....................................................................................... 231

10.1 Introduction ....................................................................................................................................... 231
10.2 Neuropeptides .................................................................................................................................... 231
10.3 Selected Behaviors ............................................................................................................................ 232
10.3.1 Sleep in Insects ..................................................................................................................... 232
10.3.2 Learning in Insects............................................................................................................... 234
10.3.3 Gustation and Feeding in Insects ......................................................................................... 235
10.4 Motor Programs................................................................................................................................. 237
10.4.1 A Motor Program that Controls Walking ............................................................................ 237
10.4.2 A Motor Pattern for Rhythmic Breathing ............................................................................ 238
10.4.3 Escape Behavior and Trapping of Prey: Role of Giant Axons ............................................. 238
Acknowledgments ........................................................................................................................................ 241
10.6 Self-Study Questions ......................................................................................................................... 241
Chapter 11 Muscles Physiology and Kinematics ............................................................................................................ 247

11.1 Introduction ....................................................................................................................................... 247
11.2 Basic Muscle Structure and Function ................................................................................................ 247
11.2.1 Macro- and Microstructure of Muscle .................................................................................248
11.2.2 Muscle Attachments to the Exoskeleton .............................................................................. 249
11.2.3 Skeletal Muscle..................................................................................................................... 250
11.2.4 Polyneuronal Innervation and Multiterminal Nerve Contacts ............................................. 250
11.2.5 The Transmitter Chemical at Nerve–Muscle Junctions ....................................................... 252
11.3 Synchronous and Asynchronous Muscles ......................................................................................... 252
11.4 Muscle Proteins and Physiology of Contraction................................................................................ 254
11.4.1 The Active State: Binding of Myosin Heads to Actin and the Sliding of Filaments ........... 254
11.4.2 Release of Myosin Heads from Actin .................................................................................. 255
11.5 Muscles Involved in General Locomotion, Running, and Jumping .................................................. 256
11.5.1 Adaptations for Running, Walking, and Survival ................................................................ 256
11.5.2 Adaptations for Jumping ...................................................................................................... 257
11.6 Sound Production: Tymbal and Stridulatory Muscle ........................................................................ 258
11.6.1 Tymbal Morphology and Physiology ................................................................................... 258
11.6.2 Stridulatory Muscle Physiology ........................................................................................... 259
11.7 Insect Chill Response: Neuromuscular Physiology...........................................................................260
11.8 Morphology and Physiology of Nonskeletal Muscle .........................................................................260
11.8.1 Visceral Muscles ..................................................................................................................260
11.8.2 Heart Muscle ........................................................................................................................ 261
11.8.3 Alary Muscles ...................................................................................................................... 261
Contents xiii

Chapter 12 Insect Flight.................................................................................................................................................. 267

12.1 Introduction ....................................................................................................................................... 267
12.2 Thoracic Structure, Wing Hinges, and Muscle Groups Involved in Flight ....................................... 268
12.3 Wing Strokes ..................................................................................................................................... 269
12.4 Multiple Contractions from Each Volley of Nerve Impulses to Asynchronous Muscles .................. 270
12.5 Flight in Dragonflies and Damselflies ............................................................................................... 270
12.6 Aerodynamics of Lift and Drag Forces Produced by Wings ............................................................ 272
12.6.1 Lift Forces Generated by Clap and Fling Wing Movements ............................................... 272
12.6.2 Lift Forces Derived from Drag and Delayed Stall ............................................................... 273
12.7 Hovering Flight.................................................................................................................................. 274
12.8 Control of Pitch and Twisting of Wings ............................................................................................ 275
12.9 Power Output of Flight Muscles ........................................................................................................ 275
12.10 Metabolic Activity of Wing Muscles................................................................................................. 276
12.11 Flight Behavior .................................................................................................................................. 277
References Added to 4th Edition ..................................................................................................................278
Chapter 13 Sensory Systems ........................................................................................................................................... 283

13.1 Introduction ....................................................................................................................................... 283
13.2 External and Internal Receptors Monitor the Environment ..............................................................284
13.3 General Functional Classification of Sensory Receptors ..................................................................284
13.3.1 Receptors with Multiple Pores ............................................................................................. 285
13.3.2 Receptors with a Single Pore................................................................................................ 285
13.3.3 Receptors without Pores ....................................................................................................... 285
13.4 Mechanoreceptors ............................................................................................................................. 286
13.4.1 Structure of a Simple Tactile Hair: A Mechanoreceptor Sensillum .................................... 286
13.4.2 Hair Plates ............................................................................................................................ 286
13.4.3 Chordotonal Sensilla ............................................................................................................ 286
13.4.4 Subgenual Organs................................................................................................................. 287
13.4.5 Tympanal Organs: Specialized Organs for Airborne Sounds .............................................. 288
13.4.6 Johnston’s Organ ..................................................................................................................290
13.4.7 Simple Chordotonal Organs ................................................................................................. 291
13.4.8 Thermoreceptors and Hygroreceptors.................................................................................. 291
13.4.9 Infrared Reception ............................................................................................................... 292
13.5 Chemoreceptors ................................................................................................................................. 293
13.5.1 Olfactory Sensilla: Dendritic Fine Structure ....................................................................... 293
13.5.2 Contact Chemoreceptors–Gustatory Receptors ................................................................... 294
13.5.3 Specialists vs. Generalists among Chemoreceptors ............................................................. 295
13.5.4 Stimulus-Receptor Excitation Coupling ............................................................................... 296
Chapter 14 Vision ........................................................................................................................................................... 301

14.1 Introduction ....................................................................................................................................... 301
14.2 Compound Eye Structure ..................................................................................................................302
14.3 Dioptric Structures ............................................................................................................................ 303
14.4 Corneal Layering ............................................................................................................................... 305
xiv Contents
14.5 Retinula Cells .................................................................................................................................... 305

14.6 Rhabdomeres ..................................................................................................................................... 305
14.7 Electrical Activity of Retinula Cells ................................................................................................. 305
14.8 Neural Connections in the Optic Lobe ..............................................................................................306
14.9 Ocelli .................................................................................................................................................306
14.10 Larval Eyes: Stemmata ......................................................................................................................307
14.11 Dermal Light Sense ...........................................................................................................................307
14.12 Chemistry of Insect Vision ................................................................................................................307
14.13 Visual Cascade ..................................................................................................................................309
14.14 Regulation of the Visual Cascade .....................................................................................................309
14.15 Color Vision ....................................................................................................................................... 310
14.16 Vision is Important in Behavior ........................................................................................................ 312
14.17 Nutritional Need for Carotenoids in Insects...................................................................................... 312
14.18 Detection of Plane-Polarized Light ................................................................................................... 313
14.19 Visual Acuity ..................................................................................................................................... 314
Chapter 15 Circulatory System ....................................................................................................................................... 321

15.1 Introduction: Circulatory System ..................................................................................................... 321
15.2 Dorsal Vessel: Heart and Aorta ......................................................................................................... 321
15.2.1 Alary Muscles ...................................................................................................................... 324
15.2.2 Ostia ..................................................................................................................................... 324
15.2.3 Heartbeat .............................................................................................................................. 325
15.2.4 Ionic Influences on Heartbeat .............................................................................................. 326
15.2.5 Nerve Supply to the Heart .................................................................................................... 326
15.2.6 Cardioactive Secretions ........................................................................................................ 326
15.3 Accessory Pulsatile Hearts ................................................................................................................ 327
15.4 Hemocytes ......................................................................................................................................... 328
15.4.1 Functions of Hemocytes ....................................................................................................... 330
15.4.2 Hemocytopoietic Tissues and Origin of Hemocytes ............................................................ 330
15.4.3 Number of Circulating Hemocytes ...................................................................................... 332
15.5 Hemolymph ....................................................................................................................................... 333
15.5.1 Functions of Hemolymph and Circulation ........................................................................... 333
15.5.2 Hemolymph Volume............................................................................................................. 335
15.5.3 Coagulation of Hemolymph ................................................................................................. 335
15.5.4 Hemolymph pH and Hemolymph Buffers............................................................................ 336
15.5.5 Chemical Composition of Hemolymph ................................................................................ 337
15.5.5.1 Inorganic Ions ....................................................................................................... 337
15.5.5.2 Free Amino Acids................................................................................................. 338
15.5.5.3 Proteins ................................................................................................................. 338
15.5.5.4 Other Organic Constituents .................................................................................. 338
15.6 Rate of Circulation ............................................................................................................................ 338
15.7 Hemoglobin ....................................................................................................................................... 339
References Added to 4th Edition ..................................................................................................................340
Chapter 16 Immunity ...................................................................................................................................................... 345

16.1 Introduction ....................................................................................................................................... 345
16.2 Physical Barriers to Invasion ............................................................................................................. 345
16.3 Recognition of Nonself ......................................................................................................................346
16.4 Cellular Immune Reactions ............................................................................................................... 347
Contents xv
16.5 Synthesis of Antifungal and Antibacterial Peptides ......................................................................... 349

16.6 Toll, IMD, JNK, and JAK-STAT Are Pathways for Defense Responses .......................................... 350
16.6.1 Toll Pathway ......................................................................................................................... 351
16.6.2 IMD Pathway ....................................................................................................................... 352
16.6.3 JNK Pathway ........................................................................................................................ 352
16.6.4 JAK-STAT Pathway ............................................................................................................. 352
16.7 C-Type Lectins .................................................................................................................................. 352
16.8 Serpins ............................................................................................................................................... 352
16.9 Ecology, Behavior, and Immunity ..................................................................................................... 353
16.9.1 Effects of Climate Change on Insect Immune Responses ................................................... 353
16.9.2 Limitation of Nutritional Resources May Alter Immune Response .................................... 354
16.10 Cost of Defense: To Defend or Not? What Are the Trade-Offs?....................................................... 354
16.11 Coevolutionary Race between Parasitoid Escape Mechanisms and
Host Defense Mechanisms ................................................................................................................ 355
16.12 Autoimmune Consequences of Some Defense Reactions ................................................................. 356
16.13 Gender Differences in Immune Responses ....................................................................................... 356
Chapter 17 Respiration ................................................................................................................................................... 365

17.1 Introduction ...................................................................................................................................... 365
17.2 Structure of the Tracheal System ...................................................................................................... 366
17.2.1 Tracheae and Tracheole Structure ........................................................................................ 366
17.2.2 Plasticity in the Tracheal System ......................................................................................... 367
17.2.3 Spiracle Structure and Function ........................................................................................... 367
17.2.4 Tracheal Epithelium ............................................................................................................. 369
17.2.5 Development of New Tracheoles .......................................................................................... 369
17.2.6 Air Sacs ................................................................................................................................ 370
17.2.7 Molting of Tracheae ............................................................................................................. 370
17.3 Tracheal Supply to Tissues and Organs............................................................................................. 371
17.3.1 Adaptations of Tracheae to Supply Flight Muscles .............................................................. 371
17.4 Ventilation and Diffusion of Gases within the System ..................................................................... 373
17.4.1 Simple Diffusion is Usually Not Adequate .......................................................................... 373
17.4.2 Active Ventilation of Tracheae ............................................................................................. 373
17.4.3 Diffusion from Tracheoles to Mitochondria ........................................................................ 376
17.5 Discontinuous Gas Exchange ............................................................................................................ 376
17.6 Water Balance during Flight ............................................................................................................. 378
17.7 Gas Exchange in Aquatic Insects ...................................................................................................... 379
17.7.1 Compressible Gas Gills ........................................................................................................ 379
17.7.2 Incompressible Gas Gills: A Plastron .................................................................................. 380
17.7.3 Use of Aquatic Plants as Air Source .................................................................................... 380
17.7.4 Cutaneous Respiration: Closed Tracheal System in Some Aquatic Insects ........................ 381
17.8 Respiration in Endoparasitic Insects ................................................................................................. 383
17.9 Respiratory Pigments ........................................................................................................................ 383
17.10 Respiration in Eggs and Developing Embryos .................................................................................. 383
17.11 Nonrespiratory Functions of the Tracheal System ............................................................................ 384
Chapter 18 Excretion ...................................................................................................................................................... 391

18.1 Introduction ....................................................................................................................................... 391
18.2 Malpighian Tubules ........................................................................................................................... 391
xvi Contents
18.3 Malpighian Tubule Cells.................................................................................................................... 393

18.4 Formation of Primary Urine in Malpighian Tubules......................................................................... 394
18.5 Proton Pump as Driving Mechanism for Urine Formation and Homeostasis................................... 394
18.6 Possibilities for Selectively Disrupting Water and Ion Homeostasis for Insect Control.................... 396
18.7 Selective Reabsorption in the Hindgut............................................................................................... 397
18.7.1 Anatomical Specialization of Hindgut Epithelial Cells........................................................ 397
18.7.2 Secretion and Reabsorption in the Ileum.............................................................................. 399
18.7.3 Reabsorption in the Rectum.................................................................................................. 399
18.8 Role of the Excretory System in Maintaining Homeostasis.............................................................. 399
18.8.1 Electrolyte Homeostasis........................................................................................................400
18.8.2 Water Homeostasis................................................................................................................ 401
18.8.2.1 Diuretic Hormones................................................................................................ 401
18.8.2.2 Antidiuretic Hormones..........................................................................................403
18.8.3 Acid–Base Homeostasis........................................................................................................403
18.8.4 Nitrogen Homeostasis...........................................................................................................403
18.8.4.1 Ammonia Excretion...............................................................................................403
18.8.4.2 Uric Acid Synthesis and Excretion........................................................................405
18.9 Cryptonephridial Systems..................................................................................................................407
18.10 Summary and Conclusions.................................................................................................................408
18.11 Review and Self-Study Questions......................................................................................................408
References Added to 4th Edition...................................................................................................................409
Foundation References.................................................................................................................................. 410
Chapter 19 Semiochemicals............................................................................................................................................. 415

19.1 Introduction........................................................................................................................................ 415
19.2 Classes of Semiochemicals................................................................................................................ 415
19.3 Importance of the Olfactory Sense in Insects.................................................................................... 416
19.4 Active Space Concept......................................................................................................................... 418
19.5 Pheromones Classified According to Behavior Elicited..................................................................... 418
19.6 Pheromone Parsimony........................................................................................................................ 418
19.7 Chemical Characteristics of Semiochemicals.................................................................................... 419
19.8 Insect Receptors and Odorant-Binding Proteins................................................................................ 421
19.8.1 Pheromone-Binding Proteins................................................................................................ 421
19.8.2 Signal Transduction and Receptor Response........................................................................ 423
19.8.3 Pheromone Inactivation and Clearing of the Receptor......................................................... 424
19.8.4 Do Insects Smell the Blend or Just the Major Components?................................................ 425
19.9 Information Coding and Processing................................................................................................... 426
19.9.1 Structure of Odor Plumes...................................................................................................... 426
19.9.2 Pheromone Signal Processing............................................................................................... 428
19.10 Hormonal Control of Pheromone Synthesis and Release................................................................... 429
19.11 Biosynthesis of Pheromones............................................................................................................... 430
19.12 Geographical and Population Differences and Evolution of Pheromone Blends............................... 433
19.13 Practical Applications of Pheromones................................................................................................ 434
19.14 Summary and Conclusions................................................................................................................. 436
19.15 Review and Self-Study Questions...................................................................................................... 436
References Added to 4th Edition................................................................................................................... 437
Foundation References.................................................................................................................................. 439
Chapter 20 Reproduction................................................................................................................................................. 447

20.1 Introduction........................................................................................................................................ 447
20.2 Female Reproductive System............................................................................................................. 447
20.2.1 Structure of Ovaries.............................................................................................................. 447
20.2.1.1 Panoistic Ovarioles................................................................................................449
20.2.1.2 Telotrophic Ovarioles............................................................................................449
20.2.1.3 Polytrophic Ovarioles............................................................................................449
Contents xvii
20.2.1.4 Oviposition............................................................................................................ 450

20.2.2 Nutrients for Oogenesis ........................................................................................................ 450
20.2.3 Hormonal Regulation of Ovary Development and Synthesis of Egg Proteins .................... 451
20.3 Vitellogenins and Yolk Proteins ........................................................................................................ 456
20.3.1 Biochemical Characteristics of Vitellogenins and Yolk Proteins ........................................ 456
20.3.2 Yolk Proteins of Higher Diptera........................................................................................... 457
20.4 Sequestering of Vitellogenins and Yolk Proteins by Oocytes ........................................................... 457
20.4.1 Patency of Follicular Cells ................................................................................................... 457
20.4.2 Egg Proteins Produced by Follicular Cells .......................................................................... 458
20.4.3 Proteins in Addition to Vitellogenin and Yolk Proteins in the Egg ..................................... 459
20.5 Formation of the Vitelline Membrane ............................................................................................... 459
20.6 The Chorion .......................................................................................................................................460
20.7 Gas Exchange in Eggs .......................................................................................................................460
20.8 Male Reproductive System ................................................................................................................460
20.8.1 Apyrene and Eupyrene Sperm of Lepidoptera ..................................................................... 463
20.8.2 Male Accessory Glands........................................................................................................ 463
20.8.3 Transfer of Sperm .................................................................................................................464
20.9 Sex Determination .............................................................................................................................464
20.10 Chromosomal Systems for Gender Determination ...........................................................................465
Chapter 21 Insect Symbioses .......................................................................................................................................... 475

21.1 Introduction ....................................................................................................................................... 475
21.2 Symbioses among Leaf-Cutting Ants, Fungi, and Bacteria .............................................................. 476
21.3 Biology of Termites ........................................................................................................................... 478
21.3.1 Symbionts in Termites .......................................................................................................... 479
21.3.2 Lignocellose Structure .........................................................................................................480
21.3.3 Nitrogen Metabolism ............................................................................................................480
21.3.4 Fungal Culture...................................................................................................................... 481
21.4 Bark and Ambrosia Beetles and Their Symbionts ............................................................................ 481
21.4.1 Ambrosia Beetles ................................................................................................................. 481
21.4.2 Bark Beetles ......................................................................................................................... 483
21.4.3 Fungal Role in Supplementing Limited Nutrients in Wood and Phloem............................. 483
21.4.4 Evolution of Fungal Feeding in Bark Beetles ...................................................................... 485
21.4.5 Bacteria as Part of the Bark Beetle Holobiont ..................................................................... 485
21.4.6 Anthropogenic Effects upon Bark Beetles and Their Symbionts ........................................ 485
21.5 Buchnera in Aphids ........................................................................................................................... 486
21.6 Tsetse Fly Symbionts ......................................................................................................................... 486
21.7 Wolbachia .......................................................................................................................................... 487
21.7.1 Cytoplasmic Incompatability Inducing Effect of Wolbachia .............................................. 488
21.7.2 Parthenogenesis-Inducing Effect of Wolbachia ................................................................... 489
21.7.3 Feminizing Strains of Wolbachia ........................................................................................ 489
21.8 Burkholderia in Insects ..................................................................................................................... 490
21.10 Self-Study Questions ......................................................................................................................... 491
Chapter 22 Global Climate Change: Present and Future Impact on Insects .................................................................. 503
22.1 Introduction ....................................................................................................................................... 503
22.2 How Have Insects Responded to Climate: Will Climate Change Bring
Greater Damage by Insect Pests? ...................................................................................................... 505
xviii Contents
22.3 Acclimation of Insects to Lower Thermal Limits: Their Response to

Fluctuating and Extreme Cold............................................................................................................506
22.4 Response of Insects to Upper Thermal Limits................................................................................... 508
22.5 Will Tropical Insect Be More or Less Impacted by Climate Warming?...........................................509
22.6 Insect Ecophysiology and Climate Change........................................................................................509
22.7 Climate Change is Driving Insect Distributions................................................................................ 510
22.8 Climate Change: Insect Vectors and Infectious Diseases.................................................................. 511
Acknowledgments......................................................................................................................................... 514
References..................................................................................................................................................... 514
Chapter 23 The Genomics Revolution in Entomology.................................................................................................... 521

23.1 Introduction........................................................................................................................................ 521
23.2 Transposable Elements....................................................................................................................... 523
23.2.1 Horizontal and Vertical Transmission of TEs in Insects...................................................... 523
23.2.2 Additional Ways Transposons Aid Insects............................................................................ 523
23.3 Evolutionarily Ancient and Conserved RNAI Pathways in Insects................................................... 523
23.3.1 Functions of microRNA........................................................................................................ 525
23.3.2 The PIWI RNA (piRNA) Pathway: Protection for Germline Cells...................................... 526
23.3.3 Function of Short Interfering RNA (siRNA) in Insect Antiviral Immunity......................... 526
23.4 Applications of Interfering RNA in Insects....................................................................................... 527
23.5 CRISPR/Cas 9 Technology................................................................................................................ 529
23.5.1 Applications of CRISPR/Cas9 System to Edit Genes in Insects.......................................... 530
23.5.2 Using CRISPR/Cas9 to Explore Gene Function................................................................... 532
23.6 Introducing Gene Editing into Educational Programs....................................................................... 532
Acknowledgments......................................................................................................................................... 534
References..................................................................................................................................................... 534
Index................................................................................................................................................................................... 539
Preface
Research and publications in insect physiology and bio- to two anonymous reviewers of the 3rd edition, who in early
chemistry are in an exponential climb. New journals abound spring 2020 wrote detailed reviews about each chapter and
and insect publications occur in a bewildering array of provided wonderful support and suggestions for a 4th revi-
journals that publish papers on many other types of organ- sion and for adding Climate Change and Genomics.
isms. The literature is widespread and scattered. It is hard I thank the following for helpful comments, criticism,
to keep up in even one or two specialties; although most and suggestions for the three new chapters in this edi-
journals are now on the Internet, it is impossible to read all tion: Man-Yeon Choi and Seung-Joon Ahn (Chapter 10,
the new papers published each month that one might like to Behavior), Daniel Janzen, Winnie Hallwachs, Timothy
read and still have time to do research and/or teach classes. Bonebrake, and Andrei Sourakov (Chapter 22, Climate
The problem is even more acute for graduate students or Change), and Bryony C. Bonning and Adam Wong
undergraduates who are just getting acquainted with insect (Chapter 23, Genomics).
physiology and biochemistry. Even though the Internet I am indebted to the many persons who gave photo-
offers wonderful advantages, understanding and integrat- graphs to use in the book, as follows: Jiri Hulcr, M.T.
ing new advances into a whole picture is still difficult. Kasson, Lyle Buss, Marie Nation Becker, Rochelle Nation,
My aim in this 4th edition of Insect Physiology and Hanife Genc, Maria and Tom Eisner, Jerry Butler, Ethel
Biochemistry is to produce a book that will provide a Villabos and Todd Shelly, Ritsuo Nishida, Clay Smith,
framework onto which one can layer constantly emerging Alexandra Shapiro, Jimmy Becnel, K. Tomioka, N. Peschel
new information, or rearrange and add new framework, as and C. Helfrich-Förster, Thomas Chouvenc, Guy Bloch,
needed. I hope the book will aid working scientists who D.L. Musolin, C. Hermann, Brian Forschler, Jarrod Scott,
are not insect biologists, but who conduct research in genet- Y. Hongoh, Man.-Yeon. Choi, Peter Teal, Paul Shirk, Al
ics, microbiology, symbioses, and the myriad of projects in Handler, Coby Schal, D.O. Deonier, Robin Giblin-Davis,
which insects are merely good research animals. During C. Bordereau, C.R. Currie, Amr Mohamed, and Tyson L.
this revision, I have been fascinated to discover that a great Hedrick.
deal of human-related problems, including diabetes, mental I thank Alice Oven at CRC Press for requesting and
disorders, and gene expression, to mention just a few, are encouraging me to begin this 4th edition and for help along
being studied in model insects because of the genetic unity the way. Thanks to Ms. Shikha Garg for preparing my
of life. copy for production, and for helping correct some of my
Nearly all topics included in the last edition have been oversights and errors. I am especially grateful to Marsha
kept, some new ones added, and each chapter has been Hecht and Vijay Shanker, Taylor and Francis Group, CRC
updated with additional recent citations (including many Press for producing a beautiful book. Especial thanks are
2021 citations). Three new chapters – The Nervous System: due to Vijay Shanker for excellent final editing, for correct-
Selected Behaviors (Chapter 10), Global Climate Change: ing my typographical errors, and ensuring that textual and
Present and Future Impacts on Insects (Chapter 22), and Reference Cited citations are in agreement. I thank Kathy
The Genomic Revolution in Entomology (Chapter 23) – Milne who converted my drawings into computer illustra-
have been added to the 4th edition. Additional new fea- tions. I thank the Department of Entomology & Nematology,
tures in this edition include color illustrations throughout University of Florida, Gainesville, for allowing me to hold
the book, a box of HIGHLIGHTS at the beginning of each the title of Emeritus Professor after retirement. Finally, I
chapter, SUMMARY AND CONCLUSIONS, and a box of think my wife, Dorothy, who has exhibited extraordinary
SUMMARY POINTS at the end of each chapter, the link to patience as I waded through hundreds of research papers
the Web for new literature citations in the 4th edition, and and days on the Internet to update this edition.
incorporation of important information in a box, or some-
times several boxes, in most chapters. James L. Nation, Sr.
I thank again those who read and advised me on previous Professor Emeritus
editions, Dr. Jiri Hulcr, Dr. Kirsten S. Pelz-Stelinski, Dr. N. Entomology & Nematology
Krishnan, Dr. Glenn Hall, Dr. Marie Nation Becker, Dr. Jon University of Florida, Gainesville
Harrison, Dr. Tom Miller, and Dr. Guy Bloch. I am grateful e-mail: JLN@ufl.edu
xix
Author Biography
James L. Nation is cur- the Distinguished Faculty Award from Florida Blue Key
rently Professor Emeritus Fraternity for outstanding service to the University of
in the Entomology & Florida. In 2006, he received an award from the Florida
Nematology Department, Entomological Society in recognition of Achievement for
College of Agriculture and Teaching in Higher Education. He introduced a graduate
Life Sciences, University course in Insect Physiology for entomology students at
of Florida, Gainesville, Florida A & M University, Tallahassee, FL in the fall term,
FL. He taught graduate 2006. The course was taught principally by interactive TV
courses in the Department from Gainesville, with a few visits to the A&M campus.
of Entomology & Nema- At the annual HONORS BANQUET on April 15, 2010,
tology, conducted resea- he was selected as the 2010/2011 Honors Professor of the
rch, and taught Global Year at the University of Florida. He edited (with two oth-
Environmental Issues in ers) the Journal of Chemical Ecology from 1995 to 2000
the Honors Program and the Florida Entomologist, An International Journal
before retiring in June 2003 after 43 years of teach- for the Americas from 2004 to 2010. In 2011, he received
ing and research at the University of Florida. He contin- an award from the Florida Entomological Society in rec-
ued to teach, on a contract basis, in the undergraduate ognition of Editorial Services to the Society for editing
Honors Program at the University of Florida (Global the Florida Entomologist. He has authored or co-authored
Environmental Issues, 3 credit course, and Origin of more than 85 scientific publications in refereed journals,
Humans, 1 credit course) until retirement in 2020. and short articles in the Encyclopedia of Entomology (John
Dr. Nation holds a BS degree (1957) from Mississippi Capinera, Editor). He is the author of Insect Physiology
State University (Entomology with Chemistry minor) and and Biochemistry (CRC Press), a textbook for graduate and
a Ph.D. (1960) from Cornell University (Entomology with undergraduate studies. The first edition was published in
specialization in insect physiology and insect biochem- 2002, a revised 2nd edition was published in April 2008,
istry). He was voted Teacher of the Year by the graduate and a 3rd revised edition was published in August 2015.
students in the Entomology & Nematology Department at This 4th revision is updated, including additional citations
the University of Florida in 1989–1990, 1994–1995, 1996– and three completely new chapters. His e-mail address is
1997, 1998–1999, and 2000–2001. In 2001, he received JLN@ufl.edu.
xxi
1 Embryogenesis
HIGHLIGHTS
• A proteinaceous chorion is put on the egg while it is in the ovary.
• Sperm released from the spermatheca of the female enter the egg through the micropyle, a narrow channel
through the chorion, as the egg passes down the oviduct.
• Usually, the egg nucleus is diploid until the entry of the sperm stimulates meiotic division leading to the
haploid egg nucleus. Union of a sperm nucleus with the egg nucleus produces the zygote and stimulates the
zygote to begin divisions.
• Zygotic divisions result in large numbers of nuclei surrounded with a small field of cytoplasm but without
cell membranes; these nuclei and cytoplasm migrate into a single layer near the periphery of the egg and
form the blastoderm.
• Maternal genes are present and active in the nurse cells of the mother during oogenesis, and they pass
maternal gene transcripts (mRNAs, tRNAs, proteins) into the developing oocyte in the ovary.
• Gap genes divide the embryo into large domains; then pair-r ule genes divide the domains into paraseg-
ments, and finally, segment polarity genes control formation of true segments.
• Homeotic genes function during parasegment formation and give each segment its characteristic identity.
• Drosophila is a model for genetic studies of embryogenesis and offers important insights into the develop-
ment of higher organisms including humans.
1.1 INTRODUCTION silkworm, Bombyx mori, has been published (Miya, 1985),

and the early stages of embryogenesis are described for sev-
The three major divisions in the Insecta, the Apterygota, eral species of fireflies by Kobayashi and Ando (1985).
Hemimetabola, and Holometabola, are not directly ances- The complete analysis of the genome of Drosophila
tral to each other, and consequently embryological devel- melanogaster (Adams et al., 2000), its many mutants,
opments in the groups, although similar in some respects, ease and economy of rearing, and a great host of work-
often diverge. The Apterygota (Protura, Collembola, ers means that more details of the genetics of embryogen-
Diplura, and Thysanura) never evolved wings and lack esis are available for D. melanogaster than for any other
metamorphosis. The immatures look like small versions insect, although the genomes of numerous insects are now
of the adults. The Hemimetabola (Orthoptera, Hemiptera, available. A timeline for some of the major morphogenetic
and others) evolved wings and have gradual metamorpho- events may be helpful (Table 1.1), but one should keep in
sis, but no pupal stage. Immatures have some adult features mind that Drosophila is a fast-developing insect, and many
but lack fully developed wings until the adult stage. The other insects do not develop so rapidly. Earlier reviews of
Holometabola (Coleoptera, Hymenoptera, Lepidoptera, the development and genetics of Drosophila were provided
Diptera, and others) evolved adult wings and have com- by Gehring and Hiromi (1986), Gehring (1987), French
plete metamorphosis, with a pupal stage. Immature forms (1988), Nüsslein-Volhard (1991), Lawrence (1992), and Bate
are typically wormlike, and thus look very different from and Martinez-Arias (1993). Melton (1991) provided a good
the adults. Wingless adults occur in the Hemimetabola and comparative review of certain aspects of animal develop-
Holometabola, but the wingless condition evolved second- ment. The role of kinesins – microtubular motor proteins –
arily from winged forms. in embryonic development has been reviewed by Konjikusic
The goals for this chapter are to describe the morpho- et al. (2021).
genetic events and the action of genes in formation of the
embryo. The work by Johannsen and Butt (1941) is still a
very valuable source for understanding variations in mor- 1.2 MORPHOGENESIS
phogenesis, as are reviews by Andersen (1972a, 1972b),
1.2.1 Egg, Fertilization, and Zygote Formation
Jura (1972), Sander et al. (1985), Campos-Ortega and
Hartenstein (1985), Panfilio et al. (2006), and Panfilio Insect eggs are centrolecithal, which means that the eggs
(2008). A review of morphology of embryogenesis in the have a central yolk surrounded by a layer of cytoplasm.
DOI: 10.1201/9781003279822-1 1
2 Insect Physiology and Biochemistry
TABLE 1.1
Developmental Stages of Drosophila Embryogenesis
Developmental Stages during Drosophila Embryogenesis
Morphological Events (25°C) Hoursa

Stage 1 25 minutes Cleavage divisions 1 and 2 0:25
Stage 2 40 minutes Divisions 3-8 occur 1:05
Stage 3 15 minutes Pole bud formation, division 9 occurs 1:20
Stage 4 50 minutes Final 4 divisions, syncytial blastoderm formed, stage 4 ends at beginning of cellularization 2:10
Stage 5 40 minutes Cellularization occurs 2:50
Stage 6 10 minutes Early stages of gastrulation 3:00
Stage 7 10 minutes Gastrulation complete 3:10
Stage 8 30 minutes Formation of amnioproctodeal invagination and rapid germ band elongation 3:40
Stage 9 40 minutes Transient segmentation of mesodermal layer, stomodeal invagination 4:20
Stage 10 60 minutes Stomodeum invaginates, germ band growth continues 5:20
Stage 11 120 minutes Growth stage, no major morphogenetic changes, parasegmental furrows develop 7:20
Stage 12 60 minutes Germ band shortens 9:20
Stage 13 60 minutes Germ band shortening complete, head involution begins 10:20
Stage 14 60 minutes Closure of midgut, dorsal closure 11:20
Stage 15 30 minutes Gut forms complete tube and encloses yolk sac 13:00
Stage 16 3 hours Intersegmental grooves evident, shortening of ventral nerve cord 16:00
Stage 17 Stage 17 extends to hatching
Source: Data from Campos-Ortega and Hartenstein (1985).

Note: Times and stages probably will be different in other species of insects.
a The time is elapsed time after the egg has been laid in hours.
The yolk is a nutrient source to be used by the develop- the egg contents (Figure 1.1). The cytoplasm is a layer of
ing embryo. A vitelline membrane surrounds the periph- variable thickness in eggs of different groups. In some,
eral cytoplasm (sometimes called the periplasm), and a there is so little cytoplasm that it is not visually obvi-
proteinaceous chorion provides a protective cover for ous, as for example, in eggs of the Apterygota. The egg
FIGURE 1.1 Diagram of egg structure.

Embryogenesis 3
nucleus may lie at the periphery of the egg, on top of the

yolk and surrounding cytoplasm, or it may lie in the cyto-
plasm. When an egg is laid, the egg nucleus usually is
still in the diploid state. The entry of sperm as the egg
passes down the oviduct of the female initiates matura-
tion divisions. The first maturation division divides the
chromosomes equally, but the nuclear plasm is divided
unequally, resulting in a large egg nucleus and a small
polar body (Figure 1.2). The egg nucleus divides once
more to become the haploid female gamete, with produc-
tion of another small polar body. The first polar body may
or may not divide again. If it does divide, two more polar
bodies are produced; in any case, polar bodies eventually
are reabsorbed into the yolk. The haploid female nucleus
usually migrates toward the center of the egg and unites FIGURE 1.3 The first few cleavages of the yolk may be com-
on the way with the sperm nucleus; the developing organ- plete, as in some Collembola, but complete cleavage ceases after
ism is then called the zygote. a few divisions. (a) The first division is depicted as beginning after
the nucleus has divided by mitosis; (b) the division into two cells
is illustrated; (c) cleavage into four cells is underway, and the four
1.2.2 Variations in Zygotic Nucleus may divide into eight cells, after which the yolk usually is not
Cleavage, Formation of Energids, cleaved equally with subsequent nuclear divisions; and (d) a ball
of cells has formed with a yolk that has not been partitioned accu-
and Blastoderm Formation
mulated in the center (not shown) of the mass of cells. (Stages
Zygotic nucleus divisions are influenced by the quantity of modified from Jura, 1972.)
yolk and cytoplasm. Division in eggs with little yolk parti-
tions the yolk in a few early divisions (Figure 1.3), such as in
the collembolan Tetrodontophora bielanensis (Apterygota),
but not after the 8-cell stage. In the great majority of insect
groups, the zygotic nuclei divide from the beginning with-
out cleavage of the yolk, and without formation of cell
membranes between nuclei. Repeated nuclear divisions
produce thousands of nuclei, each surrounded by a small
island of cytoplasm. Each nucleus with its island of cyto-
plasm is called an energid (Figure 1.4). Energids migrate
toward the periphery, and when a few thousand nuclei have
FIGURE 1.2 Maturation divisions of oocyte and sperm.

Oogonia in the germarial region of an ovary divide by meiosis to
produce an oocyte and a polar body. A second meiotic division,
which may not occur until the oocyte is united with the sperm, FIGURE 1.4 An example of an egg in which yolk is not par-
produces the final oocyte. The polar bodies are reabsorbed as titioned and cleavage nuclei (energids) are produced and sur-
food for the developing oocyte. Spermatocytes in the germarium rounded by a small amount of cytoplasm. Yolk remains in the
of the testes give rise to mature spermatozoa by meiotic divisions. interior of the egg. (Redrawn and modified from Johannsen and
Union of a sperm and egg produces the zygote. Butt, 1941.)
been formed, they distribute themselves in a single layer 1.2.2.1 Apterygota

around the perimeter. Some energids remain in the yolk Apterygotes are small, wingless insects with ametabolous
and become vitellophages that digest (liquify) the yolk development (no metamorphosis, and no major changes in
and make the nutrients available to the developing embryo. morphology between immature and adults), and include
Cytoplasmic strands extend from the blastomeres, as the the orders Protura (small insects in soil and leaf litter),
energids are now usually called, into the yolk as a route Collembola (commonly called springtails), Diplura (called
for nutrient uptake. Eventually, cell membranes become bristle tails), Archeognatha (also called bristletails), and
complete, the cytoplasmic strands disappear, and the layer Thysanura (some bristle tails, silverfish, and firebrats)
of cells is called the blastoderm (Figure 1.5). There are (Romoser and Stoffolano, 1998). Details and variations in
numerous differences in the way the blastoderm forms, and development of the Apterygota have been reviewed by Jura
in subsequent morphogenetic movements among the differ- (1972). Even in the Apterygota, the processes of division
ent groups of insects. A summary of major differences is and cleavage are not the same in all members of the group.
given below; the reviews and reference works cited in the In some, the yolk is cleaved at each division, but in others,
introduction should be consulted if more details about spe- nuclear division occurs without yolk cleavage. Division con-
cific groups are desired. tinues to make many small blastomeres that move toward
FIGURE 1.5 An illustration of the blastoderm stage in development. Energids gradually migrate to the periphery to form a single
layer of blastomeres around the periphery of the egg. Cell membranes are incomplete in an early blastoderm and cytoplasmic strands
from blastomeres extend into the yolk, but later the cell membranes are complete and junctions develop between cells to hold them
together. The dotted lines across the blastoderm indicate diagrammatically a fate map based on development of Drosophila melanogas-
ter, which has a determinate-type egg. Even at this early stage, blastoderm cells in Drosophila are known (from marking experiments)
to be committed to a specific path of development. The broken lines indicate regions developing into mouth parts, thorax, or abdomen.
This first evidence of developmental commitment marks the parasegments, developmental units within which genetic action leads to
the final segmentation pattern of the larva and adult.
Embryogenesis 5
the periphery of the egg and gradually align themselves in a superficial, and the yolk is not cleaved. Synchrony is lost
single layer around the perimeter of the egg to form the blas- after a few divisions. Some cleavage nuclei migrate to the
toderm. At one pole of the blastoderm, blastomeres become periphery while some remain in the yolk, functioning as
increasingly columnar as the dorsal organ forms. At the yolk nuclei, later to become vitellophages. The germ anlage
other pole (usually the ventral side), they are smaller but rep- or germ band forms at the posterior pole of the blastoderm.
resent the cells that will form the future embryonic rudiment A few blastomeres at the anterior pole of the blastoderm
(= germ band) and embryonic membranes (Figure 1.6). may form a dorsal organ, but some workers have ques-
The exact function of the dorsal organ is not clear; it tioned whether a dorsal organ is present. After gastrula-
may be secretory. If the cells that form it are damaged or tion, a part of the serosal membrane sinks into the yolk to
destroyed, the embryo does not develop normally and does form a secondary dorsal organ, but it soon degenerates and
not hatch. The dorsal organ cells invaginate into the under- its function is unknown. The yolk cells in Thysanura are
lying yolk and take the shape of a mushroom with a stalk, true vitellophages that digest the yolk; some yolk cells later
and tendrils grow out and contact the developing germ disintegrate and contribute to the formation of the midgut
band (the embryo) after gastrulation has occurred. A dorsal epithelium. The blastoderm stage exists only briefly in
organ does not develop in a recognizable form in Hemi-and Apterygota and is followed by gastrulation.
Holometabola.
In Japyx solifugus (Diplura), cleavage is superficial from 1.2.2.2 Hemimetabola
the start. The blastomeres migrate toward the periphery Embryogenesis of the Hemimetabola has been reviewed
of the egg at about the 64-cell stage, and after additional by Anderson (1972a). In general, eggs of hemimetabolous
divisions, the blastoderm is formed. A dorsal organ is pres- insects develop slowly, taking weeks or months to hatch.
ent. Cleavages of the zygote of Thysanura (silverfish) are When the egg is released from the ovary, the oocyte is in
FIGURE 1.6 A late blastoderm stage with germ band formed on ventral side of egg and dorsal organ on the dorsal side (modified from
Johannsen and Butt, 1941). The germ band will subsequently grow into the embryo. The function of the dorsal organ, not present in the
blastoderm of some species, is not known in detail.
metaphase of the first maturation division. The nucleus with In D. melanogaster, the morphogenetic events, as well
a small amount of cytoplasm lies at the periphery of the as their genetic control, have been extensively studied,
egg, where it stays as maturation divisions produce 3 polar and there typically are 13 synchronous division cycles
nuclei and 1 haploid female pronucleus. The female pro- before cell boundaries are established between nuclei.
nucleus migrates to the interior while the polar nuclei stay After the first seven synchronous divisions, there are 128
at the periphery. The union with the male pronucleus occurs nuclei arranged in an ellipsoid shape around the central
near the middle of the egg. The 3 polar nuclei and any yolk (Zalokar and Erk, 1976). Most of the nuclei begin to
unsuccessful male pronuclei are reabsorbed during early migrate to the periphery of the embryo, but about 26 nuclei
cleavage. The eggs are relatively rich in yolk. The zygotic stay near the yolk in the center of the egg after the sev-
nucleus undergoes divisions without yolk cleavage and enth division and become vitellophages. The vitellophages
energids are formed. Division is usually synchronous until and all the other nuclei undergo the eighth nuclear division
the blastoderm is formed. The rate of division varies a great together. Soon the first cells become determined (commit-
deal among the Hemimetabola, but none divides as fast as ted to a particular developmental fate), and a few nuclei
in the Holometabola. Energids gradually move toward the are incorporated into the posterior pole plasma to become
periphery of the egg and form the blastoderm. The number the polar buds or future germ cells. These will give rise
of nuclear divisions and the number of energids that form to the gametes (reproductive cells) of the adult insect. The
the blastoderm vary with species. remaining energids are destined to become somatic cells of
Energids that remain in the yolk mass become primary the embryo.
vitellophages and continue to divide and produce more The vitellophages, polar buds, and somatic nuclei divide
vitellophages. In Dictyoptera (cockroaches), Plecoptera in synchrony two more times, making a total of ten divi-
(stoneflies), and Gryllotalpidae (mole crickets), there are no sions for the somatic nuclei. In the eighth, ninth, and tenth
primary vitellophages, but some secondary ones develop divisions, the somatic nuclei progressively move toward the
from energids that migrate from the periphery back into the surface of the egg, forming a single layer of nuclei around
yolk. The final position of the germ band is ventral and usu- the perimeter of the egg, the syncytial blastoderm (syncytial
ally posterior, but the position along the anterior/posterior denotes the lack of cell boundaries) (Foe and Alberts, 1983).
axis is somewhat variable in different species. The germ After 13 divisions of the somatic nuclei during the
band may lie on the surface of the yolk mass, or it may grow first 3 hours of embryo life in D. melanogaster, there are
into the interior of the yolk in some groups. about 5000 syncytial blastoderm nuclei layered around the
periphery of the egg (Chan and Gehring, 1971). Cell mem-
1.2.2.3 Holometabola branes begin to form, and desmosomes form between cells
The eggs of the Holometabola have only a small amount to hold them together (Mahowald, 1963). The cytoplasmic
of yolk, and a relatively large peripheral periplasm (=cyto- strands that reach into the yolk gradually disappear as cell
plasm). The outermost part of the periplasm is called the membranes are completed. The time at which cells become
egg cortex. Eggs typically are small, 1 mm or less in length. committed to the formation of specific structures is vari-
Eggs of Lepidoptera tend to be round to ovoid in shape, while able in different insects, but in D. melanogaster formerly
those of Diptera and Hymenoptera are usually elongated. totipotent energids become determined in the blastoderm
Typically, the egg is in the metaphase of the first maturation stage, after which they can only develop into certain body
division when released from the ovary. Maturation division segments (Simcox and Sang, 1983; Gehring, 1987). The
results in 3 polar nuclei and the female pronucleus, which ultimate development of blastoderm cells in Drosophila has
migrates into the interior of the egg. The yolk is not cleaved been ascertained by marking cells to note their future fate,
and zygotic nuclear divisions produce energids. Divisions and the representation of the commitment of blastoderm
are typically synchronous through 8–10 or even more divi- cells as done diagrammatically in Figure 1.5 is called a fate
sions, but synchrony is lost in various Holometabola at map (Campos-Ortega and Hartenstein, 1985).
different times after about the eighth division. The rate of
division is variable, with higher Diptera (Drosophila, teph-
1.2.3 Formation of the Germ Band
ritid fruit flies, mosquitoes, other Cyclorrhapha) having the
fastest division rate. The number of cells in the blastoderm Initially, the cells of the blastula are uniform in size and
varies in the Holometabola from about 500 to 8000. Some shape, but along the ventral side of the blastula, the cells
of the blastoderm cells may migrate back into the yolk as rapidly thicken and enlarge into the germ band, the cells
secondary vitellophages. Although the nuclei of the vitel- destined to give rise to the embryo. In D. melanogaster and
lophages cease dividing and remain in the central yolk other Diptera with long germ patterns with large amounts
region, their DNA replicates and they become polyploid. of cytoplasm, nearly the entire cell number of the blasto-
The pole buds and syncytial blastoderm nuclei continue to derm becomes the germ band, leaving only a few cells to
divide independently of each other. The zygote usually lies build the extraembryonic membranes. In other insects typi-
centrally but may be displaced toward either end. Cell divi- cal of those with short or intermediate germ patterns (e.g.,
sion and growth of the embryo are rapid, and eggs usually the cricket Gryllus bimaculatus, Donoughe and Extavour,
hatch in a few days in most cases. 2016) a variable number of cells along the ventral side of
Embryogenesis 7
the blastoderm enlarge and become more columnar in to a specific developmental fate. In determinate eggs, the
shape, while lateral and dorsal to the ventral region the cells blastoderm cells become committed very early to a specific
become more flattened and squamous and are destined to developmental pathway. Regardless of the size of the berm
form the extraembryonic membranes called the amnion band initially, elongation and growth occur as development
and serosa. continues. Short germ eggs tend to be characteristic of the
The initial size of the germ band varies in different Orthoptera and Odonata (insects with panoistic ovaries),
groups of insects, and three major types occur, character- while long germ eggs tend to be produced by Lepidoptera,
ized as short germ band, long germ band, and interme- Coleoptera, Diptera, and Hymenoptera. However, there
diate germ band (reviewed by Sander et al., 1985). Short are some groups that do not fit easily into one category, so
germ band eggs tend to be indeterminate, large eggs from the correlation between taxon and egg type is not strong
panoistic ovaries, contain a large yolk with relatively lit- (Sander et al., 1985). Evolutionary selection may have led
tle cytoplasm, have a relatively small portion of the blas- to long germ eggs as an adaptation to use rapidly decaying
toderm that becomes the germ band, and develop slowly vegetable, fruit, or dead animal hosts, as well as reduced
over days, weeks, or months. Long germ band eggs usu- exposure of a relatively immobile stage (Sander et al.,
ally are smaller eggs that come from meroistic ovaries. 1985). Some insects have an intermediate germ band egg
They tend to have a relatively large amount of cytoplasm in which segmentation in the gnathocephalon and thorax
and a small amount of yolk. The germ band initially cov- occurs relatively rapidly, but the abdominal portion of the
ers a large portion of the blastoderm, and development to germ band grows slowly and segmentation takes longer to
hatching is rapid, often hours to days. Long germ band eggs occur. Eggs of the cricket Acheta domesticus are intermedi-
tend to be determinate. Indeterminate and determinate ate germ band type (Sander et al., 1985).
refer to how soon the blastoderm cells become committed
1.2.4 Gastrulation
During gastrulation part of the germ band sinks into the
ball of blastoderm cells (Figure 1.7a), and germ layers are
formed that will give rise to different organs and tissues.
Immediately after gastrulation occurs, the structure is
sometimes referred to as a gastrula.
Gastrulation is highly variable, and so different in some
insects from the process in other animals that some embryolo-
gists have questioned whether the events occurring are really
gastrulation in the classical sense. Deep invagination of the
germ band, so characteristic of many other types of organ-
isms, does not occur in insects (Johannsen and Butt, 1941).
In other organisms gastrulation results in an outer layer (the
ectoderm), an inner layer (the endoderm), and a middle layer
(the mesoderm). Typically, in insects at the end of gastrula-
FIGURE 1.7A Schematic representation of an early stage in tion, there is an outer ectodermal layer of cells and an inner
gastrulation during which the germ band invaginates. layer of cells termed the mesentodermal layer (Figure 1.7b).
FIGURE 1.7B A later stage in which germ layers have formed. (Redrawn and modified from Johannsen and Butt, 1941).
Most of the controversy about gastrulation has been focused Holometabola, body appendages soon appear as bilateral
on the formation, or some argue the lack of the formation, evaginations or small cellular buds from the ectoderm.
of a classical endoderm (Johannsen and Butt, 1941). The Buds from the protocephalon form the antenna and mouth
only structure formed from the endoderm, providing it is parts, and buds from the thoracic segments give rise to the
accepted as a germ layer, is the midgut. The outer layer legs and wings. Bilateral outgrowths of buds appear on the
of ectoderm gives rise to the nervous system, the tra- abdominal segments but are later reabsorbed in segments
cheal system, the fore- and hindgut, and the integument. 1–7 and 10. In some, abdominal buds on segments 8 and
Formation of the mesentoderm layer varies with different 9 continue to develop into the external genitalia and those
insect groups. In Coleoptera, invaginated cells along the on segment 11 form cerci. The exact form that the abdomi-
ventral midline fold into a tube that subsequently unfolds nal limb buds might take, if they were not reabsorbed, is
to become an irregular inner layer of cells. In honeybees, unknown, but some have interpreted them as gill flaps in an
Apis mellifera, a ventral plate of cells sinks inward and is ancient insect ancestor (Wigglesworth, 1972).
overgrown by the remaining lateral plates of germ band,
and a somewhat similar formation of an inner layer of cells
1.2.6 Blastokinesis and Extraembryonic Membranes
occurs in Orthoptera. The mesentoderm gives rise to mus-
cles, circulatory system, fat body, hemocytes, and the mid- Blastokinesis refers to movements and rotations of the
gut (but see the note above on controversy about separate embryo, processes that are variable in different insect
endoderm and origin of midgut). In Drosophila, the gene groups. Sometimes blastokinesis is divided into two phases,
tinman must be active for subsequent development of the anatrepsis and katatrepsis. Various degrees of anatrepsis
dorsal heart (Howard et al., 2021). and katatrepsis occur in different insects. Embryological
During gastrulation, the ectoderm and mesentoderm development in D. melanogaster has been well studied,
become overgrown by some of the remaining surface cells, but it is not typical of most other insects. In Drosophila,
eventually enclosing the developing embryo, an amnionic the gene zerknüllt (zen) specifies a single extraembryonic
cavity, and the remaining yolk. The layer of squamous cells membrane, the amnioserosa. Zen encodes a homeobox
lining the ventral portion of the amnionic cavity is called transcription factor and is one of the genes influenced by
the amnion, and a thin layer of cells on the outside of the maternal and zygotic dorsoventral (DV) morphogen gra-
gastrula becomes the serosa, the two extraembryonic dients. Maternal NF-k B/Dorsal protein gradient represses
membranes of the embryo. In Drosophila, the two mem- zen in the ventral half of the embryo, resulting in zen tran-
branes fuse into the amnioserosa. scription to a broad dorsal region.
Most of the Hemimetabola insects, those with incom-
plete metamorphosis, have eggs with a large amount of
1.2.5 Germ Band Elongation
central yolk, and blastokinesis is divided into two phases,
The germ band grows and elongates in all insects regard- anatrepsis and katatrepsis, with two extraembryonic mem-
less of its initial size. The anterior part of the germ band, branes being formed, the serosa and the amnion. Panfilio
the protocephalon, includes the antennal segments, inter- et al. (2006) and Panfilio (2008) described blastokinesis in
calary segments (which give rise to the tritocerebrum and the milkweed bug, Oncopeltus fasciatus, as an example for
parts of the head capsule), and three gnathal segments many insects, particularly the Hemimetabola. Oncopeltus
(primordia of the mandible, maxilla, and labium). The pro- has a short germ band, in which a relatively small por-
tocephalon is bilaterally widened at the anterior end (like tion of the single layer of cells in the blastoderm gives rise
a double-headed hammer), with a “finger-like” tail. In D. to the embryo. Blastokinesis means, as the term implies,
melanogaster, the posterior tail of the germ band, as well as that movements of the blastoderm cells take place. Briefly
the protocephalon, is fully formed at the blastoderm stage, stated, the embryo first invaginates into the large amount
and segmentation can proceed at once, usually occurring of yolk typical of eggs of many Hemimetabola, grows in
within hours of formation of the blastoderm and while gas- length, and then emerges from the yolk and comes to rest
trulation is in progress. on the ventral side of the egg where subsequent develop-
The tail portion of the germ band grows at variable rates ment occurs. The following description of blastokine-
in different groups. Dorso-ventral furrows rapidly appear sis in O. fasciatus is based on Panfilio’s (2008) review
behind the protocephalon in Drosophila embryos as seg- (Figures 1.8 and 1.9).
mentation is initiated. These first segments are called para- At about 22% into the embryological development, the
segments, and they are slightly out of register with the first blastokinetic movement, anatrepsis, occurs as the germ
final segmentation pattern that will develop. Nevertheless, rudiment invaginates into and becomes immersed in the yolk
they represent the first evidence of metamerization in the at the posterior pole of the egg, illustrated in Figure 1.8a.
embryo. Panfilio (2008) described the process like a “the toe of a
Six segments fuse into the head. The thorax consists of sock being pulled through its own opening”. It is important
three segments. The number of abdominal segments is vari- to note that the part of the germ rudiment that will eventually
able in different insects, but 11, or 12 if the terminal telson give rise to the head of the insect remains oriented near the
is counted, is the primitive number. In rapidly developing posterior pole of the egg (see Figures 1.8b, 1.9a, and 1.9b).
Embryogenesis 9
FIGURE 1.8 Blastokinesis during Oncopeltus fasciatus development illustrated in drawings at the left and light micrographs of
nuclear staining of dechorionated eggs on the right. (a) immersion anatrepsis with the embryo invaginating into the yolk; (b) extended
germband stage (see Figure 1.8a for labeling); (c) early stage with head region emerging from the yolk; (d) mid katatrepsis, with embryo
about half out of the yolk; and (e) late katatrepsis with embryo fully out of the yolk and now lying on the ventral side of the egg. The
serosa was mostly removed in the light micrograph (a) so that the yolk nuclei and germ rudiment are visible. The embryo is partially
visible in micrograph panels (b) and (c) in places where it is not so deep in the yolk. Egg orientation is anterior to the left and dorsal
up. Color coding: serosa (blue); amnion (orange); embryo (gray). Black arrows in the drawings indicate the direction of movement;
white arrowheads in the micrographs indicate the amnion-serosa boundary. Abbreviations: A, P, D, and V, anterior, posterior, dorsal,
and ventral axes of the egg, respectively; A’, P’, and V’, sides of the germband stage embryo; a, antennae; pr. ser, presumptive serosa;
t1, thoracic segment/leg 1. (From Panfilio, 2008, With Permission.)
Some blastoderm cells separate from the germ rudiment embryo proper, and a second extraembryonic membrane,
as it invaginates and remains on the surface to become the the amnion that covers the ventral side of the embryo. The
serosa, an extraembryonic membrane that spreads to fully embryo is upside down at this time with its ventral surface
enclose the yolk and the germ rudiment. While immersed directed upward toward the dorsal side of the egg, and the
in the yolk, the germ rudiment differentiates into the cells that will become the head oriented toward the posterior
FIGURE 1.9 Illustrations of a germ band stage embryo modeled on the milkweed bug Oncopeltus fasciatus with the extraembry-
onic membranes of serosa (blue) and amnion (orange), embryo (gray), and yolk (yellow). The amnionic cavity (white) lies between
the amnion and the ventral surface of the embryo. (a) Mid-sagittal section view. (b) Transverse-section view approximately across the
middle of (a) showing that the germband has spread laterally over the ventral side of the egg. The portion that will become the abdo-
men extends around the anterior end of the egg (behind the plane of the paper), and just the tip shows on the dorsal side of the egg
in this cross-section. The posterior pole of the egg is facing the viewer in the cross-section. The anterior end of the egg is at the left
in the sagittal section, and the egg-dorsal is up in both views. Abbreviations: a, antennae; am, amnion; ab, abdominal region; gn,
gnathal (mouthpart) region; h, head; ser, serosa; t1-3, thoracic segments/legs 1-3. The sagittal section is a labeled view of Figure 1.8b.
(From Panfilio, 2008, With Permission.)
pole of the egg (Figures 1.8 and 1.9). The embryo stays in blastokinesis movements. The blastokinetic events in most
this orientation for an additional 25% of the development holometabolous insects are typically reduced, although
time as it grows in length, undergoes some segmentation, some do have distinct movements and extraembryonic
and begins development of appendages. membranes. For example, the red flour beetle, Tribolium
About halfway through embryological development of castaneum, has complete development, like Drosophila,
the milkweed bug embryo the second blastokinetic move- but it has a short germ band type development in which it
ment, katatrepsis, begins as the germ rudiment starts to produces the main body segments in succession – head first,
evert or turn outward. The amnion turns inside out and then thoracic segments, and finally abdominal segments,
begins to fuse with the serosa over the future head of the and it has well developed extraembryonic membranes – the
embryo, but the two subsequently rupture as the embryo amnion and serosa (Handel et al., 2000). Tribolium has two
continues to evert and emerge from the yolk, resulting in zen homologs – Tc-zen1 and Tc-zen2 (Tc in the name comes
the freeing of the head and antennal region from the mem- from the first letters of the scientific name, T. castaneum,
branes as it pushes out of the yolk (Figure 1.8c). The serosa of the beetle). The serosa is specified by Tc-zen1 in early
contracts toward the anterior pole of the egg, contracting to development. The amnion covers the embryo at the dor-
a small anterior-pole cap, and eventually, when katatrep- sal side, and later Tc-zen2 promotes fusion of the amnion
sis is over, forming the dorsal organ which then disappears and serosa required for dorsal closure. Certain Lepidoptera
completely. The internal amnion and embryo continue to (some moths and butterflies) also have well-defined anat-
emerge from the yolk, with the head out first, then the tho- repsis and katatrepsis. Dorsal closure is characteristic of all
rax, and last the abdominal region. As these actions occur, insects. The review of Panfilio (2008) should be consulted
the emerging embryo bends backward over the posterior for more detailed descriptions of variations in blastokinesis
pole of the egg (somewhat like a “U” lying to the left on in various insect groups.
its side, as in Figure 1.8d as it emerges from the yolk) and Various functions have been suggested (Box 1.1) for the
migrates toward the ventral surface of the egg, coming to serosa and amnion, but few of the suggestions have been
rest with the head oriented toward the anterior pole of the substantiated with experimental evidence. The main evi-
egg and with the ventral surface of the developing embryo dence for the possible role of the serosa in forming a protec-
oriented to the ventral surface of the egg (Figure 1.8e). The tive cuticle, in water regulation, and in aiding in mounting
embryo grows dorsally and laterally until it replaces the an immune response to challenge comes from work with
amnion and dorsal closure occurs forming a cavity with all mosquitoes and the red flour beetle.
the yolk confined within the embryo. The embryonic gut
forms around the yolk and organogenesis continues.
BOX 1.1 SUGGESTED FUNCTIONS
Blastokinesis varies widely among insect groups, and
FOR THE SEROSA AND/OR
the two extraembryonic membranes are not always dis-
AMNION (PANFILIO, 2008)
tinct (Panfilio, 2008). Anatrepsis and katatrepsis are espe-
cially prominent in those insects without a pupal stage, the 1. General protective function
Hemimetabola, that have gradual metamorphosis, although 2. Cushioning of embryo from physical shock
variations exist in these groups. Some Hemimetabola, spe- 3. The serosa may be a source of innate
cifically ovoviparous Blattaria, Mantodea, and some species immune response
of Hemiptera (Hemiptera are now classified as Heteroptera) 4. Detoxification of environmental poisons
lack anatrepsis and katatrepsis or have no definable
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§ 11
In spite of the non-committal attitude of his solicitors, Sir John
Alard had been sure that to defend the suit would be to vindicate
Mary and her family against the outrageous Julian. He would not
believe that judgment could go against his daughter except by
default, and now that this incredible thing had happened, and Mary
had been publicly and argumentatively stripped of her own and
Alard’s good name, while Julian, with innocence and virtue
proclaimed by law, was set free to marry his new choice, he felt
uncertain whether to blame most his daughter’s counsel or his
daughter herself.
Counsel had failed to make what he might out of Julian’s cross-
examination ... what a fruitful field was there! If only Sir John could
have cross-examined Julian himself! There would have been an end
of that mirage of the Deceived and Deserted Husband which had so
impressed the court.... But Mary was to blame as well as counsel. She
really had been appallingly indiscreet ... her cross-examination—
Lord! what an affair! What a damn fool she had made of herself!—
Hang it all, he’d really have thought better of her if she’d gone the
whole hog ... the fellow wasn’t much good in the witness-box either ...
but he’d behaved like a gentleman afterwards. He had made Mary a
formal proposal of marriage the morning after the decree was given.
The only thing to do now was for her to marry him.
Lady Alard marked her daughter’s disgrace by sending for Dr.
Mount in the middle of the night, and “nearly dying on his hands” as
she reproachfully told Mary when she returned to Conster the next
afternoon. Mary looked a great deal more ill than her mother—dazed
and blank she sat by Lady Alard’s sofa, listening to the tale of her
sorrows and symptoms, only a slow occasional trembling of her lip
showing that her heart was alive and in torment under the dead
weight of her body’s stupefaction. All her mind and being was
withdrawn into herself, and during the afternoon was in retreat,
seeking strength for the last desperate stand that she must make.
After tea, Peter arrived, looking awkward and unhappy—then
George, looking scared and pompous. Mary knew that a family
conclave had been summoned, and her heart sank. What a farce and
a sham these parliaments were, seeing that Alard was ruled by the
absolute monarchy of Sir John. No one would take her part, unless
perhaps it was Gervase—Uranus in the Alard system—but he would
not be there today; she must stand alone. She gripped her hands
together under the little bag on her lap, and in her dry heart there
was a prayer at last—“Oh, God, I have never been able to be quite
true to myself—now don’t let me be quite untrue.”
As soon as the servants had cleared away the last of the tea things
—there had been a pretence of offering tea to Peter and George, as if
they had casually dropped in—Sir John cast aside all convention of
accident, and opened the attack.
“Well,” he said to his assembled family—“it’s been a dreadful
business—unexpectedly dreadful. Shows what the Divorce Court is
under all this talk about justice. There’s been only one saving clause
to the whole business, and that’s Smith’s behaviour. He might have
done better in the witness-box, but he’s stuck by Mary all through,
and made her a formal offer of marriage directly the decree was
given.”
“That was the least he could do,” said Peter.
“Of course; you needn’t tell me that. But I’ve seen such shocking
examples of bad faith during the last three days.... It’s a comfort to
find one man behaving decently. I’m convinced that the only thing
Mary can do is to marry him as soon as the decree is made absolute.”
George gave a choking sound, and his father’s eye turned fiercely
upon him.
“Well, sir—what have you to say?”
“I—I—er—only that Mary can’t marry again now—er—under these
new circumstances ... only the innocent partner....”
“You dare, Sir! Damn it all—I’ll believe in my own daughter’s
innocence in spite of all the courts in the country.”
“I don’t mean that she isn’t innocent—er—in fact—but the decree
has been given against her.”
“What difference does that make?—if she was innocent before the
decree she’s innocent after it, no matter which way it goes. Damn you
and your humbug, Sir. But it doesn’t matter in the least—she can
marry again, whatever you say; the law allows it, so you can’t stop it.
She shall be married in Leasan church.”
“She shall not, Sir.”
A deep bluish flush was on George’s cheek-bones as he rose to his
feet. Sir John was for a moment taken aback by defiance from such
an unexpected quarter, but he soon recovered himself.
“I tell you she shall. Leasan belongs to me.”
“The living is in your gift, Sir, but at present I hold it, and as priest
of this parish, I refuse to lend my church for the marriage of the guil
—er—in fact, for—the marriage.”
“Bunkum! ‘Priest of this parish’—you’ll be calling yourself Pope
next. If you can’t talk sense you can clear out.”
George was already at the door, and the hand he laid upon it
trembled violently.
“Don’t go!”—it was Mary who cried after him—“there’s no need for
you to upset yourself about my marriage. I haven’t the slightest
thought of getting married.”
But George had gone out.
§ 12
There was an uneasy shuffle of relief throughout the room. The
situation, though still painful, had been cleared of an exasperating
side-issue. But at the same time Mary was uncomfortably aware that
she had changed the focus of her father’s anger from her brother to
herself.
“What do you mean?” he rapped out, when the sound of George’s
protesting retreat had died away.
“I mean that you and George have been arguing for nothing. As I
told you some time ago, I haven’t the slightest intention of marrying
Charles.”
“And why not, may I ask?”
“Because I’ve had enough of marriage.”
“But Mary, think of us—think of your family,” wailed Lady Alard
—“what are we going to do if you don’t marry?”
“I can’t see what difference it will make.”
“It will make all the difference in the world. If you marry Charles
and go abroad for a bit, you’ll find that after a time people will
receive you—I don’t say here, but in London. If you don’t marry, you
will always be looked upon with suspicion.”
“Why?”
“Married women without husbands always are.”
“Then in spite of all the judges and juries and courts and decrees,
I’m still a married woman?”
“I don’t see what else you’re to call yourself, dear. You’re certainly
not a spinster, and you can’t say you’re a widow.”
“Then if I marry again I shall have two husbands, and in six
months Julian will have two wives.”
Lady Alard began to weep.
“For God’s sake! let’s stop talking this nonsense,” cried Sir John.
“Mary’s marriage has been dissolved, and her one chance of
reinstating herself—and us—is by marrying this man who’s been the
cause of all the trouble. I say it’s her duty—she’s brought us all into
disgrace, so I don’t think it’s asking too much of her to take the only
possible way of getting us out, even at the sacrifice of her personal
inclinations.”
“Father—I never asked you to defend the case. I begged you not to
—all this horror we have been through is due to your defence.”
“If you’d behaved properly there would have been no case at all,
and if you had behaved with only ordinary discretion the defence
could have been proved. When I decided that we must, for the
honour of the family, defend the case, I had no idea what an utter
fool you had been. Your cross-examination was a revelation to me as
well as to the court. You’ve simply played Old Harry with your
reputation, and now the only decent thing for you to do is to marry
this man and get out.”
“I can get out without marrying this man.”
“And where will you go?”
“I shall go abroad. I have enough money of my own to live on
quietly, and I needn’t be a disgrace to anyone. If I marry Charles I
shall only bring unhappiness to both of us.”
“Oh, Mary, do be reasonable!” cried Lady Alard—“do think of the
girls”—with a wave that included both twenty-two and thirty-eight
—“and do think how all this is your own fault. When you first left
Julian, you should have come here and lived at home, then no one
would ever have imagined anything. But you would go off and live by
yourself, and think you could do just the same as if you weren’t
married—though I’m sure I’d be sorry to see Jenny going about with
anyone as you went about with Charles Smith. When I was engaged
to your father, we were hardly ever so much as left alone in a room
together——”
“Your reminiscences are interesting, my dear,” said Sir John, “but
cast no light on the situation. The point is that Mary refuses to pay
the price of her folly, even though by doing so she could buy out her
family as well as herself.”
“I fail to see how.”
“Then you must be blind.”
“It seems to me it would be much better if I went right away. I’ve
made a hideous mess of my life, and brought trouble upon you all—I
acknowledge that; but at least there’s one thing I will not do—and
that is walk with my eyes open into the trap I walked into ten years
ago with my eyes shut.”
“Then you need expect nothing more from your family.”
“I won’t.”
“Father,” said Peter—“if she isn’t fond of the chap....”
Mary interrupted him.
“Don’t—it isn’t quite that. I am fond of him. I’m not in love with
him or anything romantic, but I’m fond of him, and for that very
reason I won’t take this way out. He’s twenty years older than I am,
and set in his bachelor ways—and I firmly believe that only chivalry
has made him stand by me as he has done. He doesn’t in his heart
want to marry a woman who’s ruined and spoiled ... and I won’t let
him throw himself away. If I leave him alone, he can live things down
—men always can; but if I marry him, he’ll sink with me. And I’ve
nothing to give him that will make up to him for what he will suffer. I
won’t let him pay such a price for ... for being ... kind to me.”
Nobody spoke a word. Perhaps the introduction of Charles Smith’s
future as a motive for refusing to use him to patch up the situation
struck the Alards as slightly indecent. And Mary suddenly knew that
if the argument were resumed she would yield—that she was at the
end of her resources and could stand out no longer. Her only chance
of saving Charles’s happiness and her own soul now lay in the
humiliation of flight. There is only one salvation for the weak and
that is to realise their weakness. She rose unsteadily to her feet. A
dozen miles seemed to yawn between her and the door....
“Where are you going, Mary?” asked Sir John—“we haven’t nearly
finished talking yet.”
Would anybody help her?—yes—here was Jenny unexpectedly
opening the door for her and pushing her out. And in the hall was
Gervase, his Ford lorry throbbing outside in the drive.
“Gervase!” cried Mary faintly—“if I pack in ten minutes, will you
take me to the station?”
§ 13
It was a very different packing from that before Mary’s departure
eighteen months ago. There was no soft-treading Gisèle, and her
clothes, though she had been at Leasan six months, were fewer than
when she had come for a Christmas visit. They were still beautiful,
however, and Mary still loved them—it hurt her to see Jenny
tumbling and squeezing them into the trunk. But she must not be
critical, it was as well perhaps that she had someone to pack for her
who did not really care for clothes and did not waste time in
smoothing and folding ... because she must get out of the house
quickly, before the rest of the family had time to find out what she
was about. It was undignified, she knew, but her many defeats had
brought her a bitter carelessness.
The sisters did not talk much during the packing. But Mary knew
that Jenny approved of what she was doing. Perhaps Jenny herself
would like to be starting out on a flight from Alard. She wondered a
little how Jenny’s own affair was going—that unacknowledged yet
obsessing affair. She realised rather sadly that she had lost her
sister’s confidence—or perhaps had never quite had it. Her own
detachment, her own passion for aloofness and independence had
grown up like a mist between them. And now when her aloofness was
destroyed, when some million citizens of England were acquainted
with her heart, when all the golden web she had spun round herself
was torn, soiled and scattered, her sister was gone. She stood alone—
no longer set apart, no longer veiled from her fellows by delicate self-
spun webs—but just alone.
“Shall I ring for Pollock?” said Jenny.
“No, I’d much rather you didn’t.”
“Then how shall we manage about your trunk?—it’s too heavy for
us to carry down ourselves.”
“Can’t Gervase carry it?”
“Yes—I expect he could.”
She called her brother up from the hall, and he easily swung up the
trunk on his shoulder. As he did so, and Mary saw his hands with
their broken nails and the grime of the shop worked into the skin,
she realised that they symbolised a freedom which was more actual
than any she had made. Gervase was the only one of the family who
was really free, though he worked ten hours a day for ten shillings a
week. Doris was not free, for she had accepted the position of idle
daughter, and was bound by all the ropes of a convention which had
no substance in fact. Peter was not free because he had, Mary knew,
married away from his real choice, and was now bound to justify his
new choice to his heart—George was not free, he was least free of all,
because individual members of the family had power over him as
well as the collective fetish. Jenny was not free, because she must
love according to opportunity. Slaves ... all the Alards were slaves ...
to Alard—to the convention of the old county family with its
prosperity of income and acres, its house, its servants, its ancient
name and reputation—a convention the foundations of which were
rotten right through, which was bound to topple sooner or later,
crushing all those who tried to shelter under it. So far only two had
broken away, herself and Gervase—herself so feebly, so painfully, in
such haste and humiliation, he so calmly and carelessly and
sufficiently. He would be happy and prosperous in his freedom, but
she ... she dared not think.
However, Jenny was thinking for her.
“What will you do, Mary?” she asked, as they crossed the hall
—“where are you going?”
“I’m going back to London. I don’t know yet what I’ll do.”
“Have you enough money? I can easily lend you something—I
cashed a cheque yesterday.”
“Oh, I’m quite all right, thanks.”
“Do you think you’ll go abroad?”
“I’ll try to. Meg is going again next month. I expect I could go with
her.”
They were outside. Mary’s box was on the back of the lorry, and
Gervase already on the driver’s seat. It was rather a lowly way of
leaving the house of one’s fathers. Mary had never been on the lorry
before, and had some difficulty in climbing over the wheel.
Jenny steadied her, and for a moment kept her hand after she was
seated.
“Of course you know I think you’re doing the only possible thing.”
“Yes ... thank you, Jenny; but I wish I’d done it earlier.”
“How could you?”
“Refused to defend the case—spared myself and everybody all this
muck.”
“It’s very difficult, standing up to the family. But you’ve done it
now. I wish I could.... Goodbye, Mary dear, and I expect we’ll meet in
town before very long.”
“Goodbye.”
The Ford gargled, and they ran round the flower-bed in the middle
of Conster’s gravel sweep. Jenny waved farewell from the doorstep
and went indoors. Gervase began to whistle; he seemed happy—“I
wonder,” thought Mary, “if it’s true that he’s in love.”
§ 14
During the upheaval which followed Mary’s departure, George
Alard kept away from Conster. He wouldn’t go any more, he said,
where he wasn’t wanted. What was the good of asking his advice if he
was to be insulted—publicly insulted when he gave it? He brooded
tenaciously over the scene between him and his father. Sir John had
insulted him not only as a man but as a priest, and he had a right to
be offended.
Rose supported him at first—she was glad to find that there were
occasions on which he would stand up to his father. George had been
abominably treated, she told Doris—really one was nearly driven to
say that Sir John had no sense of decency.
“He speaks to him exactly as if he were a child.”
“He speaks to us all like that.”
“Then it’s high time somebody stood up to him, and I’m very glad
George did so.”
“My dear Rose—if you think George stood up....”
After a time Rose grew a little weary of her husband’s attitude, also
though she was always willing to take up arms against the family at
Conster, she had too practical an idea of her own and her children’s
interests to remain in a state of war. George had made his protest—
let him now be content.
But George was nursing his injury with inconceivable
perseverance. Hitherto she had often had to reproach him for his
subservience to his father, for the meekness with which he accepted
his direction and swallowed his affronts.
“If you can put up with his swearing in church, you can put up with
what he said to you about Mary.”
“He has insulted me as a priest.”
“He probably doesn’t realise you are one.”
“That’s just it.”
She seemed to have given him fresh cause for brooding. He sulked
and grieved, and lost interest in his parish organisations—his Sunday
School and Mothers’ Union, his Sewing Club and Coal Club, his
Parochial Church Council—now established in all its glory, though
without Peter’s name upon the roll, his branches of the S.P.G., the
C.E.M.S., all those activities which used to fill his days, which had
thrilled him with such pride when he enumerated them in his
advertisements for a locum in the Guardian.
He developed disquieting eccentricities, such as going into the
church to pray. Rose would not have minded this if he had not
fretted and upset himself because he never found anyone else
praying there.
“Why should they?” she asked, a little exasperated—“They can say
their prayers just as well at home.”
“I’ve never been into Vinehall church and found it empty.”
“Oh, you’re still worrying about Gervase going to Vinehall?”
“I’m not talking about Gervase. I’m talking about people in
general. Vinehall church is used for prayer—mine is always empty
except on Sundays.”
“Indeed it’s not—I’ve often seen people in it, looking at the old
glass, and the carving in the South Aisle.”
“But they don’t pray.”
“Of course not. We English don’t do that sort of thing in public.
They may at Vinehall; but you know what I think of Vinehall—it’s un-
English.”
“I expect it’s what the whole of England was like before the
Reformation.”
“George!” cried Rose—“you must be ill.”
Only a physical cause could account for such mental
disintegration. She decided to send for Dr. Mount, who confirmed
her diagnosis rather disconcertingly. George’s heart was diseased—
had been diseased for some time. His case was the exact contrast of
Lady Alard’s—those qualms and stabs and suffocations which for so
long both he and his wife had insisted were indigestion, were in
reality symptoms of the dread angina.
He must be very careful not to overstrain himself in any way. No,
Dr. Mount did not think a parish like Leasan too heavy a burden—
but of course a complete rest and holiday would do him good.
This, however, George refused to take—his new obstinacy
persisted, and though the treatment prescribed by Dr. Mount did
much to improve his general condition, mental as well as physical, he
evidently still brooded over his grievances. There were moments
when he tried to emphasise his sacerdotal dignity by a new solemnity
of manner which the family at Conster found humorous, and the
family at Leasan found irritating. At other times he was
extraordinarily severe, threatening such discipline as the deprivation
of blankets and petticoats to old women who would not come to
church—the most irreproachable Innocent Partner could not have
cajoled the marriage service out of him then. He also started reading
his office in church every day, though Rose pointed out to him that it
was sheer waste of time, since nobody came to hear it.
§ 15
Social engagements of various kinds had always filled a good deal
of George Alard’s life—he and Rose received invitations to most of
the tea-parties, tennis-parties and garden-parties of the
neighbourhood. He had always considered it part of his duty as a
clergyman to attend these functions, just as he had considered it his
duty to sit on every committee formed within ten miles and to
introduce a branch of every episcopally-blessed Society into his own
parish. Now with the decline of his interest in clubs and committees
came a decline of his enthusiasm for tennis and tea. Rose deplored it
all equally——
“If you won’t go to people’s parties you can’t expect them to come
to your church.”
“I can and I do.”
“But they won’t.”
“Then let them stop away. The Church’s services aren’t a social
return for hospitality received.”
“George, I wish you wouldn’t twist everything I say into some
ridiculous meaning which I never intended—and I do think you
might come with me to the Parishes this afternoon. You know they’re
a sort of connection—at least everyone hopes Jim won’t marry
Jenny.”
“I don’t feel well enough,” said George, taking a coward’s refuge
—“not even to visit such close relations,” he added with one of those
stray gleams of humour which were lost on Rose.
“Well, this is the second time I’ve been out by myself this week,
and I must say.... However, if you don’t feel well enough.... But I
think you’re making a great mistake—apart from my feelings....”
She went out, and George was left to the solitude and peace of his
study. It was a comfortable room, looking out across the green,
cedared lawn to the little church like a sitting hen. The walls were
lined with books, the armchairs were engulfing wells of ease—there
was a big writing-table by the window, and a rich, softly-coloured
carpet on the floor. Rose’s work-bag on a side-table gave one rather
agreeable feminine touch to the otherwise masculine scene. The
room was typical of hundreds in the more prosperous parsonages of
England, and George had up till quite recently felt an extraordinarily
calm and soothing glow in its contemplation. It was ridiculous to
think that a few words from his father—his father who was always
speaking sharp, disparaging words—could have smashed all his self-
satisfaction, all his pride of himself as Vicar of Leasan, all his
comfortable possession of Leasan Vicarage and Leasan Church.... But
now he seemed to remember that the dawn of that dissatisfaction
had been in Leasan Church itself, before his father had spoken—
while he was kneeling there alone among all those empty, shining
pews....
He would go out for a walk. If he stopped at home he would only
brood—it would be worse than going to the Parishes. He would go
over and see Dr. Mount—it would save the doctor coming to the
Vicarage, perhaps—there must be a visit about due—and they could
have a chat and some tea. He liked Dr. Mount—a pleasant, happy,
kind-hearted man.
The day was good for walking. The last of Autumn lay in ruddy
veils over the woods of Leasan and Brede Eye. The smell of hops and
apples was not all gone from the lanes. George walked through his
parish with a professional eye on the cottages he passed. Most of the
doors were shut in the afternoon stillness, but here and there a child
swinging on a gate would smile at him shyly as he waved a Vicarial
hand, or a woman would say “Good afternoon, Sir.” The cottages
nearly all looked dilapidated and in want of paint and repair. George
had done his duty and encouraged thrift among his parishioners, and
the interiors of the cottages were many of them furnished with some
degree of comfort, but the exterior structures were in bad condition
owing to the poverty of the Manor. He cleared his throat distressfully
once or twice—had one the right to own property when one could not
afford to keep it in repair?... His philanthropic soul, bred in the
corporal works of mercy, was in conflict with his racial instinct, bred
in the tradition of the Squires.
When he came to Vinehall, he found to his disappointment that
Dr. Mount was out, and not expected to be home till late that
evening. George felt disheartened, for he had walked three miles in
very poor condition. He would have enjoyed a cup of tea.... However,
there was nothing to be done for it, unless indeed he went and called
on Luce. But the idea did not appeal to him—he and the Rector of
Vinehall were little more than acquaintances, and Luce was a shy,
dull fellow who made conversation difficult. He had better start off
home at once—he would be home in time for a late tea.
Then he remembered that the carrier’s cart would probably soon
be passing through Vinehall and Leasan on its way from
Robertsbridge station to Rye. If he went into the village he might be
able to pick it up at the Eight Bells. Unfortunately he had walked the
extra half-mile to the inn before he remembered that the cart went
only on Tuesdays, Thursdays and Saturdays, and today was
Wednesday. He would have to walk home, more tired than ever.
However, as he passed through the village, he thought of the church,
partly because he was tired and wanted to rest, partly because
Vinehall church always had a perverse fascination for him—he never
could pass it without wanting to look in ... perhaps he had a secret,
shameful hope that he would find it empty.
He crossed the farmyard, wondering why Luce did not at all costs
provide a more decent approach, a wonder which was increased
when, on entering the church, he found he had admitted not only
himself but a large turkey, which in the chase that followed managed
somehow to achieve more dignity than his pursuer. After three laps
round the font it finally disappeared through the open door, and
George collapsed on a chair, breathing hard, and not in the least
devout.
The church had none of the swept, shiny look of Leasan, nor had it
Leasan’s perfume of scrubbing and brass-polish; instead it smelt of
stale incense, lamp-oil and old stones—partly a good smell and partly
an exceedingly bad one. It was seated with rather dilapidated chairs,
and at the east end was a huge white altar like a Christmas cake.
There were two more altars at the end of the two side aisles and one
of them was furnished with what looked suspiciously like two pairs of
kitchen candlesticks. But what upset George most of all were the
images, of which, counting crucifixes, there must have been about a
dozen. His objections were not religious but aesthetic—it revolted his
artistic taste to see the Christ pointing to His Sacred Heart, which He
carried externally under His chin, to see St. Anthony of Padua
looking like a girl in a monk’s dress, to see the Blessed Virgin with
her rosary painted on her blue skirt—and his sense of reverence and
decency to see the grubby daisy-chain with which some village child
had adorned her. Luce must have bought his church furniture
wholesale at a third-rate image shop....
George wished he could have stopped here, but he was bound to
look further, towards the white star which hung in the east Yes ... it
was just as usual ... a young man in working clothes was kneeling
there ... and an immensely stout old woman in an apron was sitting
not far off. Certainly the spectacle need not have inspired great
devotional envy, but George knew that in his own parish the young
man would probably have been lounging against the wall opposite
the Four Oaks, while the old woman would have been having a nap
before her kitchen fire. Certainly neither would have been found
inside the church.
There was a murmur of voices at the back of the south aisle, and
looking round George saw one or two children squirming in the
pews, while behind a rather frivolous blue curtain showed the top of
a biretta. Luce was hearing confessions—the confessions of
children.... George stiffened—he felt scandalised at the idea of
anyone under twelve having any religious needs beyond instruction.
This squandering of the sacraments on the young ... as if they were
capable of understanding them....
He turned to go out, feeling that after all the scales had dropped on
the debit side of Vinehall’s godliness, when he heard behind him a
heavy tread and the flutter of a cassock. Luce had come out of his
confessional.
“Why—Mr. Alard.”
George was a little shocked to hear him speak out loud, and not in
the solemn whisper he considered appropriate for church. The
Rector seemed surprised to see him—did he want to speak to him
about anything?
“Oh, no—I only looked in as I was passing.”
“Seen our new picture?” asked Luce.
“Which one?” The church must have contained at least a dozen
pictures besides the Stations of the Cross.
“In the Sacrament Chapel.”
They went down to the east end, where Luce genuflected, and
George, wavering between politeness and the Bishop of Exeter’s
definition of the Real Presence, made a sort of curtsey. There was a
very dark oil painting behind the Altar—doubtful as to subject, but
the only thing in the church, George told himself, which had any
pretence to artistic value.
“Mrs. Hurst gave us that,” said Luce—“it used to hang in her
dining-room, but considering the subject she thought it better for it
to be here.”
He had dropped his voice to a whisper—George thought it must be
out of respect to the Tabernacle, but the next minute was
enlightened.
“She’s asleep,” he said, pointing to the stout old woman.
“Oh,” said George.
“Poor old soul,” said Luce—“I hope the chair won’t give way—they
sometimes do.”
He genuflected again, and this time the decision went in favour of
the Bishop of Exeter, and George bowed as to an empty throne. On
their way out his stick caught in the daisy-chain which the Mother of
God was wearing, and pulled it off.
§ 16
He and Luce walked out of the church together and through the
farmyard without speaking a word. The silence oppressed George
and he made a remark about the weather.
“Oh, yes, I expect it will,” said Luce vaguely.
He was a tall, white-faced, red-headed young man, who spoke with
a slight stutter, and altogether, in his seedy cassock which the unkind
sun showed less black than green, seemed to George an uninspiring
figure, whose power it was difficult to account for. How was it that
Luce could make his church a house of prayer and George could not?
How was it that people thought and talked of Luce as a priest,
consulted him in the affairs of their souls and resorted to him for the
sacraments—whereas they thought of George only as a parson, paid
him subscriptions and asked him to tea?
He was still wondering when they came to the cottage where the
Rector lived—instead of in the twenty-five-roomed Rectory which the
Parish provided, with an endowment of a hundred and fifty pounds a
year. They paused awkwardly at the door, and the awkwardness was
increased rather than diminished by Luce inviting him to come in.
George’s first impulse was to decline—he felt he would rather not
have any more of the other’s constraining company—but the next
minute he realised that he now had the chance of a rest and tea
without the preliminary endurance of a long and dusty walk. So he
followed him in at the door, which opened disconcertingly into the
kitchen, and through the kitchen into the little study-living-room
beyond it.
It was not at all like George’s study at Leasan—the floor had many
more books on it than the wall, the little leaded window looked out
into a kitchen garden, and the two armchairs both appeared so
doubtful as possible supports for George’s substantial figure that he
preferred, in spite of his fatigue, to sit down on the kitchen chair that
stood by the writing-table. He realised for the first time what he had
always known—that Luce was desperately poor, having nothing but
what he could get out of the living. Probably the whole did not
amount to two hundred pounds ... and with post-war prices ...
George decided to double his subscription to the Diocesan Fund.
Meantime he accepted a cigarette which was only just not a
Woodbine, and tried to look as if he saw nothing extraordinary in the
poverty-stricken room. He thought it would be only charitable to put
the other at his ease.
“Convenient little place you’ve got here,” he remarked—“better for
a single man than that barrack of a Rectory.”
“Oh, I could never have lived in the Rectory. I wonder you manage
to live in yours.”
George muttered something indistinct about private means.
“It’s difficult enough to live here,” continued Luce—“I couldn’t do
it if it wasn’t for what people give me.”
“Are your parishioners generous?”
“I think they are, considering they’re mostly poor people. The
Pannells across the road often send me over some of their Sunday
dinner in a covered dish.”
George was speechless.
“And I once found a hamper in the road outside the gate. But after
I’d thanked God and eaten half a fowl and drunk a bottle of claret, I
found it had dropped off the carrier’s cart and there was no end of a
fuss.”
“Er—er—hum.”
There was a knock at the outer door, and before Luce could say
“Come in,” the door of the study opened and a small boy stuck his
head in.
“Please, Father, could you lend us your ink?—Mother wants to
write a letter.”
“Oh, certainly, Tom—take it—there it is; but don’t forget to bring it
back.”
The small boy said nothing, but snatched his booty and went out.
“Are your people—er—responsive?” asked George.
“Responsive to what?”
“Well—er—to you.”
“Oh, not at all.”
“Then how do you get them to come to church?”
“I don’t—Our Lord does.”
George coughed.
“They come to church because they know they’ll always find Him
there—in spite of me.”
George could not keep back the remark that Reservation was
theologically indefensible.
“Is it?” Luce did not seem much interested. “But I don’t keep the
Blessed Sacrament in my church for purposes of theology, but for
practical use. Suppose you were to die tonight—where would you get
your last Communion from if not from my tabernacle?”
George winced.
“This is the only church in the rural deanery where the Blessed
Sacrament is reserved and the holy oils are kept. The number of
people who die without the sacraments must be appalling.”
George had never been appalled by it.
“But why do you reserve publicly?” he asked—“that’s not primitive
or catholic—to reserve for purposes of worship.”
“I don’t reserve for purposes of worship—I reserve for
Communion. But I can’t prevent people from worshipping Our Lord.
Nobody could—not all the Deans of all the cathedrals in England. Oh,
I know you think my church dreadful—everybody does. Those
statues ... well, I own they’re hideous. But so are all the best parlours
in Vinehall. And I want the people to feel that the church is their Best
Parlour—which they’ll never do if I decorate it in Anglican good taste,
supposing always I could afford to do so. I want them to feel at
home.”
“Do you find all this helps to make them regular communicants?”
“Not as I’d like, of course; but we’re only beginning. Most of them
come once a month—though a few come every week. I’ve only one
daily communicant—a boy who works on Ellenwhorne Farm and
comes here every evening to cook my supper and have it with me.”
George was beginning to feel uncomfortable in this strange
atmosphere—also he was most horribly wanting his tea. Possibly, as
Luce had supper instead of dinner, he took tea later than usual.

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Insect Physiology and Biochemistry 4th

Edition James L. Nation

Costanzo Physiology 7th Edition Costanzo Phd

Rhetoric And Marxism 1st Edition James Arnt Aune

Revision Exercises Based on Textbook of Biochemistry

Die beweinte Nation Peter Ihring

L analyse des films 4th Edition Jacques Aumont

Fastening the Grave Kali James Book 1 1st Edition L A

Threading the Bones Kali James Book 2 1st Edition L A

Fastening the Grave Kali James Book 1 1st Edition L A

James L. Nation, Sr.

and by CRC Press

CRC Press is an imprint of Taylor & Francis Group, LLC

© 2022 James L. Nation, Sr.

ISBN: 978-1-032-24704-5 (hbk)

Chapter 1 Embryogenesis .................................................................................................................................................1

2.4 Midgut Cell Types ............................................................................................................................... 31

Chapter 3 Nutrition ......................................................................................................................................................... 57

Chapter 4 Integument and Molting ................................................................................................................................. 77

Chapter 5 Hormones and Development ........................................................................................................................ 107

5.5.1 Glandular Source and Chemistry of Juvenile Hormones ..................................................... 121

Chapter 6 Biological Rhythms ...................................................................................................................................... 143

Chapter 7 Diapause ....................................................................................................................................................... 165

7.8 Molecular Studies of Diapause .......................................................................................................... 173

Chapter 8 Intermediary Metabolism............................................................................................................................. 181

Chapter 9 The Nervous System: Anatomy and Physiology ..........................................................................................207

9.10.4 Sodium Inactivation and Repolarization .............................................................................. 221

Chapter 10 The Nervous System: Selected Roles in Behavior ....................................................................................... 231

Chapter 11 Muscles Physiology and Kinematics ............................................................................................................ 247

References Added to 4th Edition .................................................................................................................. 262

Chapter 12 Insect Flight.................................................................................................................................................. 267

Chapter 13 Sensory Systems ........................................................................................................................................... 283

Chapter 14 Vision ........................................................................................................................................................... 301

14.5 Retinula Cells .................................................................................................................................... 305

Chapter 15 Circulatory System ....................................................................................................................................... 321

Chapter 16 Immunity ...................................................................................................................................................... 345

16.5 Synthesis of Antifungal and Antibacterial Peptides ......................................................................... 349

Chapter 17 Respiration ................................................................................................................................................... 365

Chapter 18 Excretion ...................................................................................................................................................... 391

18.3 Malpighian Tubule Cells.................................................................................................................... 393

Chapter 19 Semiochemicals............................................................................................................................................. 415

Chapter 20 Reproduction................................................................................................................................................. 447

20.2.1.4 Oviposition............................................................................................................ 450

Chapter 21 Insect Symbioses .......................................................................................................................................... 475

22.3 Acclimation of Insects to Lower Thermal Limits: Their Response to

Chapter 23 The Genomics Revolution in Entomology.................................................................................................... 521

1.1 INTRODUCTION silkworm, Bombyx mori, has been published (Miya, 1985),

Morphological Events (25°C) Hoursa

Source: Data from Campos-­Ortega and Hartenstein (1985).

FIGURE 1.1 Diagram of egg structure.

nucleus may lie at the periphery of the egg, on top of the

FIGURE 1.2 Maturation divisions of oocyte and sperm.

been formed, they distribute themselves in a single layer 1.2.2.1 Apterygota

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1.1 INTRODUCTION silkworm, Bombyx mori, has been published (Miya, 1985),

Source: Data from Campos-Ortega and Hartenstein (1985).

been formed, they distribute themselves in a single layer 1.2.2.1 Apterygota