Metamorphosis: A Problem in Developmental Biology

"The old order changeth, yielding place to new. " When Tennyson wrote this, he was unfamiliar with the pace of modem science else he would have said the new is displaced by the newer. When Gilbert and I gathered the papers for the first edition of this overview of metamorphosis, we aimed to provide a broad basis upon which the experimental analysis of the developmental changes called metamorphosis could proceed. We were both aware then that with the new techniques of biochemistry and with the revolutionary breakthrough to the nature of the gene, countless new possibilities were being opened for the exploration of the molecular basis of development. The resources offered by metamorphic changes offered unique opportunities to trace the path from gene to phenotype. Our expectations were high. I visited Larry Gilbert and Earl Frieden in their laboratories and saw with envy how far advanced they were then in the use of molecular methods of analysis. I had started on a different approach to develop an in vitro test for thyroid action on amphibian tissue. But circumstances limited my own progress to the initial delim­ itation of the technical possibilities of the in vitro system. Only from the sidelines could I watch the steady if slow progress of biology in penetrating the maze of molecular events by which animal tissues re­ spond to hormonal and other developmental factors.

1 Metamorphosis: An Overview.- 1. Introduction.- 2. Primacy of the Spawning Environment.- 3. Internal or External Salinity—Which Determines the Visual Pattern?.- 4. Euryhaline Fishes and Amphibians.- 5. Biochemistry of Metamorphosis.- 6. Second Metamorphosis.- 7. Deep-Sea Fishes; Eels.- 8. Land Vertebrates.- 9. Conclusion.- 10. Epilogue.- References.- I: Insects.- 2 A Survey of Invertebrate Metamorphosis.- 1. Introduction.- 2. Invertebrate Metamorphoses.- 2.1. Porifera.- 2.2. Cnidaria.- 2.3. Ctenophora.- 2.4. Platyhelminthes.- 2.5. Nemertinea.- 2.6. Acanthocephala.- 2.7. Aschelminthes.- 2.8. Rotifera.- 2.9. Kinorhyncha.- 2.10. Priapulida.- 2.11. Entoprocta.- 2.12. Polyzoa.- 2.13. Brachiopoda.- 2.14. Annelida.- 2.15. Sipunculida.- 2.16. Echiurida.- 2.17. Arthropoda.- 2.18. Mollusca.- 2.19. Echinodermata.- 2.20. Phoronidea.- 2.21. Chaetognatha.- 2.22. Hemichordata.- 3. Comparison of Insect Metamorphosis with That of Other Invertebrates.- 3.1. Ametabolous Development.- 3.2. Hemimetabolous Development.- 3.3. Holometabolous Development.- 3.4. Hypermetamorphosis.- 4. Control of Metamorphosis.- 4.1. Larval Settlement and Metamorphosis.- 4.2. The Timing of Metamorphosis.- 5. Conclusions.- References.- 3 Cell Structure during Insect Metamorphosis.- 1. Introduction.- 1.1. The Nature of Metamorphosis.- 1.2. Definition of Terms.- 2. Tissue Reorganization.- 2.1. Metamorphic Changes in the Arrangement of Cells in Lepidopteran Fat Body.- 2.2. Changes in the Location of Cells—Epidermal and Muscle Rearrangement.- 2.3. Changes in Composition and the Distribution of Reserves.- 3. Cell Remodeling.- 3.1. The General Mechanism of Autophagy.- 3.2. Repopulation with New Organelles.- 3.3. Membrane Changes and Membrane Turnover.- 3.4. The Cytoskelton and Changes in Shape and Organelle Distribution.- 3.5. Cell Coupling and Junctions.- 3.6. The Control of Remodeling.- 4. Changes in the Numbers and Kinds of Cells in Remodeling to Make New Tissues.- 4.1. Cell Division.- 4.2. Cell Death.- 4.3. Polyploidy and Polyteny.- 5. The Morphology Needed to Explain Some Aspects of Metamorphosis.- 5.1. Hormonal Signals and the Response of the Nucleus.- 5.2. Positional Signals and the Kind and Amount of Growth.- 5.3. The Reception and Use of Nutritional and Precursor Molecules: Pinocytosis and Transepithelial Transport.- 6. Discussion.- 6.1. The Onset of Metamorphosis.- 6.2. Comparisons between Insects and Vertebrates.- References.- 4 Hormonal Control of Insect Metamorphosis.- 1. Introduction.- 2. Classical Methods for the Study of the Endocrinology of Insect Metamorphosis.- 3. The Insect Endocrine System: Structural Components of the Classical Scheme.- 3.1. The Brain—Neurosecretory Cells.- 3.2. Neurohemal Organs.- 3.3. Prothoracic Glands.- 3.4. Corpora Allata.- 4. Studies Leading to the Elaboration of the Classical Scheme.- 5. Chemistry and Endocrinology of the Metamorphic Hormones.- 5.1. Brain Hormone.- 5.2. Molting Hormones (Ecdysteroids).- 5.3. Juvenile Hormones.- 6. Control of Endocrine Glands.- 6.1. Cerebral NSC.- 6.2. The PG.- 6.3. The CA.- 7. Summary.- References.- 5 Chemistry, Metabolism, and Transport of Hormones Controlling Insect Metamorphosis.- 1. Introduction.- 2. Prothoracicotropic Hormone.- 3. Molting Hormone.- 3.1. Ecdysteroids—Chemistry and Occurrence.- 3.2. Biosynthesis of Ecdysone and 20-Hydroxyecdysone.- 3.3. Ecdysteroid Transport.- 3.4. Ecdysteroid Degradation.- 4. Juvenile Hormones.- 4.1. Chemistry and Occurrence.- 4.2. Structure-Activity Relationships.- 4.3. Transport.- 4.4. Biosynthesis.- 4.5. Degradation.- References.- 6 Macromolecular Changes during Insect Metamorphosis.- 1. Introduction.- 2. Changes in Protein and RNA during Larval-Pupal-Adult Metamorphosis.- 2.1. Breakdown of Macromolecular Components.- 2.2. Synthesis of Macromolecular Components.- 2.3. Cuticular Proteins.- 3. Pupal-Adult Metamorphosis: Wing Development.- 4. Larval-Pupal Metamorphosis.- 4.1. Epidermis.- 4.2. Fat Body.- Conclusions.- References.- 7 Drosophila Imaginal Discs as a Model System for the Study of Metamorphosis.- 1. Introduction and Background.- 1.1 General Characteristics of Mass-Isolated Imaginal Discs.- 2. Characteristics of Disc Metamorphosis.- 2.1. Late-Larval and Prepupal Development.- 2.2. Specificity of Ecdysteroid Induction of Disc Metamorphosis.- 2.3. Ecdysteroid Receptors in Imaginal Discs.- 2.4. Effects of Ecdysteroids on Discs.- 3. Discussion.- 3.1. Direct Nuclear Action of Hormones.- 3.2. Instability of Hormone-Receptor Complex.- 3.3. Multiplicity of Target Tissues.- 3.4. Evolutionary Origin of Metamorphic Hormone Responsiveness.- References.- 8 Cell Lines as a Model for the Study of Metamorphosis.- 1. Introduction.- 1.1. Advantages of Cell Lines.- 1.2. Cell Types Present in Established Cell Lines.- 2. Responses of Established Cell Lines to Ecdysteroids.- 2.1. Morphological Alterations.- 2.2. Enzyme Induction.- 2.3. Cell-Surface Changes.- 2.4. Cell-Cycle Changes.- 2.5. Ecdysteroid Receptors.- 3. Responses of Established Cell Lines to Juvenile Hormones.- 3.1. Proliferation and Morphological Effects.- 3.2. Macromolecular Synthesis.- 3.3. Juvenile Hormone Metabolism.- 3.4. Juvenile Hormone Receptors.- 4. Conclusions.- References.- II: Vertebrates.- 9 Survey of Chordate Metamorphosis.- 1. Introduction.- 2. Urochordates.- 2.1. Appendicularia.- 2.2. Thaliacea.- 2.3. Ascidians.- 2.4. Triggers of Metamorphic Climax.- 2.5. Unresolved Questions in Urochordate Metamorphosis.- 3. Cephalochordates.- 3.1. Cephalochordate Feeding Behavior.- 3.2. Triggers for Metamorphosis.- 3.3. Unresolved Questions in Cephalochordate Metamorphosis.- 4. Fish.- 4.1 Agnatha.- 4.2. Chondrichthyes.- 4.3. Osteichthyes.- 5. Amphibians.- 5.1. Parental Care.- 5.2. Larval Morphology and Staging.- 5.3. Larval Life Span and Survival Rates.- 5.4. Amphibian Larval Behavior.- 5.5. Triggers for Amphibian Metamorphosis.- 5.6. Problem Areas in Amphibian Metamorphosis.- 6. Future Work in Chordate Metamorphosis.- References.- 10 Cytological and Morphological Changes during Amphibian Metamorphosis.- 1. Introduction.- 2. The Thyroid.- 3. The Central Nervous System and Associated Notochord.- 3.1. General Development of the CNS.- 3.2. The Mauthner Cells.- 3.3. Lateral Motor Column Cells.- 3.4. Fine Structure of LMC Cells and Their Degeneration.- 3.5. Tail Nerve Cord.- 3.6. General Structure and Development of the Notochord.- 3.7. Notochordal Fine Structure and Its Degeneration.- 4. The Alimentary Canal.- 5. The Pancreas.- 6. The Liver.- 7. The Pronephros.- 7.1. Structure and Development.- 7.2. Fine Structure.- 7.3. Degeneration.- 8. The Skin.- 8.1. Early Epidermal Cellular Differentiation.- 8.2. General Structure of Larval Skin.- 8.3. Degeneration of Larval Tail and Body Skin.- 8.4. Thyroid Hormones and Larval Skin.- References.- 11 Hormonal Control of Amphibian Metamorphosis.- 1. Introduction.- 2. The Thyroid.- 2.1. Thyroid Function during Premetamorphosis.- 2.2. Thyroid Function during Prometamorphosis and Climax.- 2.3. Thyroid Function in Larval Urodeles.- 2.4. Metabolism of Thyroid Hormones.- 2.5. Tissue Sensitivity to T3 and T4.- 2.6. Pituitary Regulation of Thyroid Function.- 2.7. Control of Thyrotropic Function by Thyroid Hormonesm.- 2.8. Control of Thyrotropic Function by the Brain.- 2.9. Effects of Thyroid Hormones on Hypothalamo- Hypophysial Development and Function.- 3. Prolactin.- 3.1. PRL, GH, and Growth.- 3.2. Antimetamorphic Actions of PRL.- 3.3. PRL-Thyroid Interactions in “Second Metamorphosis”.- 3.4. Control of PRL Secretion and PRL Levels during Metamorphosis.- 4. Adrenocortical Hormones.- 5. Osmoregulation and Metamorphosis.- 6. Control of Anuran Development and Activation of Metamorphic Climax.- 7. Conclusions.- References.- 12 Biological Basis of Tissue Regression and Synthesis.- 1. Introduction.- 2. Spontaneous and Thyroid-Hormone-Induced Differentiation and Development of Anuran Tadpole Limbs and Lungs.- 2.1. Introduction.- 2.2. Tadpole Limbs.- 2.3. Tadpole Lungs.- 2.4. Conclusion.- 3. Spontaneous and Thyroid-Hormone-Induced Degeneration of Anuran Tadpole Tail and Gills.- 3.1. Introduction.- 3.2. Tadpole Tail.- 3.3. Tadpole Gills.- 3.4. Conclusion: Model for Hormone-Modulated Degeneration.- References.- 13 Transitions in the Nervous System during Amphibian Metamorphosis.- 1. Introduction.- 2. Gross Changes.- 3. Mesencephalic Fifth Nucleus.- 4. Mauthner’s Neuron.- 5. Lateral Motor Column.- 6. Dorsal Root Ganglia.- 7. Rohon-Beard Cells.- 8. Cerebellum.- 9. Sense Organs.- 10. Mitotic Activity.- 11. Behavioral Changes.- 12. Median Eminence.- 13. Conclusion.- References.- 14 Changes in the Blood during Amphibian Metamorphosis.- 1. Introduction.- 2. An Overview of Changes in Serum Proteins and Iron Metabolism.- 2.1. Changes in Blood Osmolarity, Serum Protein Concentration, and Serum Albumin.- 2.2. Changes in the Circulating Levels of Thyroid Hormones and Binding Proteins.- 2.3. Changes in Iron Transport, Metabolism, and Storage.- 3. Changes in the Hemoglobins and Red Blood Cells.- 3.1. Changes in Hb Structure and Function.- 3.2. Developmental Timing of the Hb Transition in Various Amphibians.- 3.3. Changes in Morphology and in Other Properties of the RBCs.- 4. Central Questions Pertaining to the RBC-Hb Transition in Bullfrogs.- 4.1. Do Adult and Larval Hbs Share Any Globin Chains?.- 4.2. Are Adult and Larval Hbs Contained in the Same RBCs during Metamorphosis?.- 4.3. Is the RBC-Hb Transition Mediated by a Change in Erythropoietic Sites?.- 4.4. Does the Life Span of RBCs Change during Metamorphosis?.- 4.5. Do Thyroid Hormones Have a Direct Effect on the Switch from Larval to Adult Globin Gene Expression?.- 4.6. What Is the Origin of the Stem Cells That Give Rise to Larval and Adult RBCs?.- 5. Summary.- References.- 15 Biochemical Characterization of Organ Differentiation and Maturation.- 1. Introduction.- 2. The Liver.- 2.1. DNA Synthesis, Cell Division, and Nuclear Morphology.- 2.2. Protein Synthesis, RNA Metabolism, and Cytoplasmic Morphology during Metamorphosis.- 2.3. Liver Glycogen.- 2.4. Mitochondrial Structure and Function during Metamorphosis.- 2.5. Temperature Effects on Liver Metamorphosis.- 2.6. Summary.- 3. The Kidney.- 4. The Intestine.- 4.1. Loss of Primary Epithelium and Shortening of the Gut.- 4.2. Proliferation of Secondary Epithelium and Development of Extraepithelial Tissues.- 4.3. Summary.- 5. The Integument.- 5.1. The Pigmentary System.- 5.2. Nonpigmentary Changes.- 6. The Eye.- 6.1. The Lens.- 6.2. The Retina.- 7. Summary and Conclusions.- References.- 16 The Dual Role of Thyroid Hormones in Vertebrate Development and Calorigenesis.- 1. Introduction.- 2. The Role of Iodine in Invertebrates.- 2.1. The Mystique of Iodine.- 3. Thyroid Hormone Dose-Response Relationships.- 4. Thyroid Hormone Receptors.- 5. Thyroid Hormone Effects in Poilcilothermic Vertebrates.- 6. Metamorphic Hormones in Amphibians.- 7. Thyroid Hormone Action in Birds.- 8. Metabolism and Calorigenesis.- 8.1. Hypo- and Hyperthyroidism.- 9. Thyroid Hormones and Differentiation.- 10. Mechanism of Action of Thyroid Hormones.- 10.1. Control of Nuclear Transcription and Protein Synthesis.- 10.2. Alternative Mechanisms of Thyroid Hormone Action.- References.