Fundamentals of Comparative Vertebrate Endocrinology

Fundamentals of Comparative Vertebrate Endocrinology

Edited by

I. Chester-Jones and

P. M. lngleton Sheffield University Sheffield, United Kingdom

and

J. G. Phillips Loughborough University of Technology Loughborough, United Kingdom

Springer Science+Business Media, LLC

Library of Congress Cataloging in Publication Data

Fundamentals of comparative vertebrate endocrinology.

Includes bibliographies and index. l. Endocrinology, Comparative. 2. Vertebrates-Physiology. I. Chester-Jones, I. II.

lngleton, P. M. III. Phillips, J. G. (John Guest) QP187.F795 1986 596'.0142 86-22703

ISBN 978-1-4899-3619-6 ISBN 978-1-4899-3617-2 (eBook) DOI 10.1007/978-1-4899-3617-2

© 1987 Springer Science+Business Media New York Originally published by Plenum Press, New York in 1987. Softcover reprint of the hardcover lst edition 1987

All rights reserved

No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher

Contributors

R. J. Balment • Department of Zoology, University of Manchester, Manchester M 13 9PL, England

T. F. C. Batten • Department of Cardiovascular Studies, Medical School, Univer­sity of Leeds, Leeds LS2 9JT, England

Ian P. Callard • Department of Biology, Biological Science Center, Boston Uni­versity, Boston, Massachusetts 02215

I. Chester-Jones • Department of Zoology, Sheffield University, Sheffield S 10 2TN, England

D. A. Gapp • Biology Department, Hamilton College, Clinton, New York 13323

S. Harvey • Wolfson Institute, University of Hull, Hull HU6 7RK, England

I. W. Henderson • Department of Zoology, University of Sheffield, Sheffield S 10 2TN, England

S-m. Ho • Department of Biology, Tufts University, Boston, Massachusetts 02155

P. M. Ingleton • Department of Pathology, Medical School, University of Sheffield, Sheffield S 10 2RX, England

D. E. Kime • Department of Zoology, Sheffield University, Sheffield S 10 2TN, England

S.M. Kleis • Department of Biology, Biological Science Center, Boston Univer­sity, Boston, Massachusetts 02215

v

vi Contributors

Frank L. Moore • Department of Zoology, Oregon State University, Corvallis, Oregon 97331

j. G. Phillips • Wolfson Institute, University of Hull, Hull HU6 7RK, England

J. A. Pudney • Biological Science Center, Boston University, Boston, Mas­sachusetts 02215

C. G. Scanes • Department of Animal Science, Rutgers University, New Brunswick, New Jersey 08903

A. P. Scott • Ministry of Agriculture, Fisheries and Food, Directorate of Fisheries Research, Fisheries Laboratory, Lowestoft, Suffolk NR33 OHT, England

Preface

Endocrinology, as a discipline, was a late arrival in the corpus of established subjects. Its growth in recent years has been prodigious, extending from mor­phology to molecular levels. Most of the major endocrine glands were noted by the early anatomists, although the adrenal glands were not described until 1563 by Bartholomaeus Eustachius (1520-1574). On the other hand, elucidation of the function of these glands was extremely slow. Key work by A. A. Berthold (1849), although overlooked at the time, showed that comb atrophy in castrated fowl was prevented by testis transplantation. The idea that glands produced substances reach­ing the bloodstream directly and not via excretory ducts stemmed from Claude Bernard, who first used the term internal secretion in 1855. The clinical observa­tions of Thomas Addison at Guy's Hospital-published as a monograph in 1855 entitled The Constitutional and Local Effects of Disease of the Suprarenal Capsules -were seminal. However, the stimulus of this early research did not bring imme­diate widespread further investigations.

Upon the discovery of secretin in 1902, Bayliss and Starling considered the term "internal secretion" to be clumsy, and the term "hormone" was coined (from OQ[!UW-1 excite or arouse) and it was first used by Starling in his Croonian Lecture of 1905. The relatively simple statement that endocrine glands secrete hormones, chemical agents circulating in the bloodstream through which an event in one part of the body influences or initiates an event in another part, now involves more complicated definitions. Indeed they become blurred, as in the case of cellular "inductors" and growth factors with local actions. Nevertheless the study of glands of internal secretion demanded a general term for the subject. This became endocrinology (£voov-within; xg[vw-separate), first used in 1909 by the Italian physician Pen de and established in England by Crookshank in 1914.

Endocrinology in its origins placed predominant emphasis on medical condi-

vii

viii Preface

tions and paramedical experiments. The term general endocrinology was introduced to indicate that endocrine examination of any member of the animal kingdom, both vertebrate and invertebrate, was legitimate in its own right. Such an approach gave rise to textbooks which included general endocrinology in the title. The subject of the present volume is comparative endocrinology. Comparative is an adjective derived from comparison, and the examination of organs in the light of correspond­ing features in another was practiced in the earliest days of comparative anatomy, for example by Aristotle (384-322 B.C.) and Galen (130-200 B.C.). However, these early studies were concerned only with descriptive anatomy (zootomy) and the comparison of one species with another. It was the theory of evolution which gave conceptual substance to comparative anatomy. Comparative could then be applied, in the modem sense, to various disciplines such as comparative phys­iology. Now comparative endocrinology is an established part of the corpus of knowledge comprising endocrinology and relates to the evolutionary status of the animals considered. In practical terms, comparative endocrinology is concerned with control, at all levels from molecule to social group, and may be expected to provide some interesting insights into the evolution of intercellular ''paracrine'' control. For example, in the typical mammalian mosaic of pituitary cells, adjacent, but different, cells appear to influence the activity of each other; in fishes, cell types are not all intermingled and perhaps the only "paracrine" influence is via a nerve axon.

Comparative vertebrate endocrinology is an expanding area of knowledge, and the five parts of this book provide the essential building blocks of information and understanding upon which further study must be based. For this reason the editors have brought together specialist authors to present the fundamental facts, so that each chapter is designed for the clearest presentation of the particular subject area.

Steroids are very ancient molecules which have been utilized throughout the evolution of living forms. Here, in Part I, we describe the anatomy and morphology of steroid-secreting tissues in vertebrates, as well as the metabolism of steroid molecules. The physiological roles of steroids have evolved into many systems, as described particularly in Part II: Reproduction in Nonmammalian Vertebrates, Part IV: Secretion of Endocrine Glands and Their Relationship to Osmoregulation, and Part V: Endocrine and Related Factors in the Control of Metabolism in Nonmam­malian Vertebrates. Modem evolutionary theories suggest that persistence of the genome into subsequent generations provides the fundamental reproductive drive. Part II describes the endocrine control of reproductive functions and mechanisms in nonmammalian vertebrates, which have evolved to ensure successful inheritance of genotype. Living organisms must consistently respond to changes in their environ­ment to maintain their own integrity. The hypothalamus and pituitary gland together form the major integrative endocrine system which coordinates signals from the environment, principally via the brain, integument, and gastrointestinal tract, with internal stimuli from peripheral endocrine organs; the structure, functions, and secretions of this system are described in Part III. The role of hormones in maintain­ing internal water and ion balance in vertebrates faced with hostile hypertonic or

Preface ix

hypotonic media is described in Part IV, while in Part V the evolution of mecha­nisms of action of the gut hormones is presented. The gut forms a major interface between an animal and its environment and is the site of uptake of essential amino acids, lipids, and sugars needed to maintain somal integrity; thus, hormones in this system play a truly vital role.

The level of presentation throughout is that required for undergraduate and graduate students pursuing courses in endocrinology. Thus, while further reading lists are provided, all statements and opinions are not documented as they would be in research papers and reviews. Apart from the three editors, thirteen authors of these chapters have provided the student with the necessary background from which to move forward to greater understanding of the patterns of life.

The style of this book has been prepared to accord with American usage based on Webster's Third New International Dictionary and Dorland's Medical Diction­ary. Thus, for example, "hypophyseal" is the preferred spelling although "hypo­physial" is correct: The authoritative statement and explanation of the error were given by David McRioch, George B. Wislocki, and James L. O'Leary in 1940 in Res. Publ. Assoc. Nerv. Ment. Dis. 20:3.

We thank Dr. David J. Groves for the original drawings in Part I, Chapters 2 and 3, which are not otherwise acknowledged.

I. Chester-Jones P. M. lngleton J. G. Phillips

Contents

I. STRUCTURE OF STEROIDOGENIC TISSUES AND THEIR MODES OF SECRETION

1. The Steroids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 D. E. Kime

l. General Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 2. Steroid Structure and Biosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 3. Steroids of the Testis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19 4. Steroids of the Ovary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30 5. Steroids of the Adrenal and Interrenal Glands . . . . . . . . . . . . . . . . . . 38 6. The Liver and Steroid Catabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . 50 7. General Conclusions and Comments . . . . . . . . . . . . . . . . . . . . . . . . . . 53 8. Selected Readings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56

2. Overall View of the Organization of the Vertebrate Gonad and the Structure of Steroidogenic Cells. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57 J. A. Pudney

l. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57 2. Morphology of Steroid-Producing Cells . . . . . . . . . . . . . . . . . . . . . . . 57 3. Correlation of Structure with Function . . . . . . . . . . . . . . . . . . . . . . . . 67 4. Steroid Secretion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69 5. Organization of the Gonads . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70 6. Selected Readings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94

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xii Contents

3. Structure of the Adrenal and Interrenal Glands . . . . . . . . . . . . . . . . . . 95 I. Chester-Jones

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95 2. Mammalia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96 3. Aves (Birds) ............................................. 106 4. Reptilia ................................................. 108 5. Amphibia ............................................... Ill 6. Pisces (Fish) ............................................. 113 7. General Observations ...................................... 118 8. Selected Readings ......................................... 120

II. REPRODUCTION IN NONMAMMALIAN VERTEBRATES

4. Avian Reproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125 S. Harvey, C. G. Scanes, and J. G. Phillips

1. Introduction .............................................. 125 2. Maturation and Development ................................ 126 3. Male Reproductive System ................................. 132 4. Female Reproductive System ................................ 136 5. Environmental Interactions ................................. 153 6. Reproductive Behavior ..................................... 159 7. Selected Readings ......................................... 185

5. Reproduction in Reptiles. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187 Ian P. Callard and S. M. Kleis

1. Introduction .............................................. 187 2. Female Reproduction ...................................... 190 3. Male Reproduction ........................................ 195 4. Regulation of Reptilian Gonadal Cycles ....................... 198 5. Hormone-Oviductal Interactions ............................. 202 6. Regulation of Egg Laying and Parturition ..................... 203

6. Reproductive Endocrinology of Amphibians . . . . . . . . . . . . . . . . . . . . . 207 Frank L. Moore

l. General Introduction ....................................... 207 2. Amphibian Neuroendocrinology ............................. 208 3. Gonad Structure and Function ............................... 212 4. Gonadotropins and Gonadal Steroid Hormones ................. 216 5. Prolactin and Corticosterone in Amphibian Reproduction ......... 220

Contents xiii

6. Hormonal Control of Amphibian Reproductive Behavior ......... 220 7. Selected Readings ......................................... 221

7. Reproductive Endocrinology of Fish . . . . . . . . . . . . . . . . . . . . . . . . . . . . 223 A. P. Scott

1. Introduction .............................................. 223 2. Class Osteichthyes: Superorder Teleostei ...................... 223 3. Class Osteichthyes: Superorder Chondrostei .................... 252 4. Class Chondrichthyes (Cartilaginous Fishes) ................... 252 5. Class Cyclostomes ........................................ 254 6. Conclusions .............................................. 255 7. Selected Readings ......................................... 256

8. Vitellogenesis and Viviparity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257 Jan P. Callard and S-m. Ho

1. General Introduction ....................................... 257 2. Viviparity and Placentation in Nonmammalian Species ........... 258 3. Evolutionary Aspects of Viviparity and Vitellogenesis: The

Reptilian-Therian Transition ................................ 267 4. Comparison of Reptilian and Mammalian Viviparity: Egg

Membranes and Trophoblast ................................ 267 5. The Vertebrate Egg in Relation to Vitellogenesis and Viviparity ... 268 6. Structure, Biochemistry, and Molecular Biology of Vitellogenin

(Yolk) .................................................. 269 7. Vitellogenin Genes and Vitellogenin Messenger mRNA Synthesis . 272 8. Posttranslational Modification of the Vitellogenin Polypeptide ..... 274 9. Plasma Vitellogenin Levels ................................. 275

10. Hormonal Requirements of Vitellogenesis ..................... 276 11. Uptake of Vitellogenin by the Growing Oocytes ................ 279 12. Conclusion .............................................. 280 13. Selected Readings ......................................... 281

III. THE HYPOTHALAMUS AND PITUITARY GLAND T. F. C. Batten and P. M. lngleton

9. The Structure and Function of the Hypothalamus and Pituitary Gland . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 285

1. General Introduction ....................................... 285 2. Anatomical Relationships of Brain and Pituitary ................ 286 3. Protochordates ........................................... 305

xiv Contents

4. Agnatha ................................................. 306 5. Elasmobranchs ........................................... 312 6. Primitive Bony Fishes ..................................... 316 7. Teleosts ................................................. 320 8. Crossopterygian Fishes ..................................... 329 9. Amphibians .............................................. 333

10. Reptiles ................................................. 338 11. Birds ................................................... 345 12. Mammals ............................................... 349 13. Chemistry of Pituitary and Hypothalamic Hormones ............. 355 14. Hypothalamic Control of Pituitary Functions ................... 374 15. Actions of Pituitary Hormones .............................. 391 16. Techniques for Identifying Pituitary and Hypothalamic Cells ...... 399 17. Selected Readings ......................................... 408

IV. SECRETION OF ENDOCRINE GLANDS AND THEIR RELATIONSHIP TO OSMOREGULATION R. J. Balment and I. W. Henderson

10. Environmental Constraints and Adaptive Mechanisms ............ 413

1. Introduction .............................................. 413 2. The Osmoregulatory Process ................................ 417 3. The Vertebrate Series ...................................... 419

11. Endocrine Glands and Their Secretions ......................... 445

1. Introduction .............................................. 445 2. Pituitary Hormones ........................................ 447

12. Integration of Hormonal Actions to Regulate Extracellular Fluid Volume and Composition ..................................... 481

I . Introduction .............................................. 481 2. Calcium ................................................. 482 3. Water ................................................... 488 4. Sodium ................................................. 491 5. General Conclusions ....................................... 493

Contents XV

13. A Phylogenetic Perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 497

1. Introduction .............................................. 497 2. The Renal Apparatus ...................................... 498 3. The Radiation of Vertebrates ................................ 501 4. Endocrine Controls ........................................ 503 5. Selected Readings ......................................... 507

V. ENDOCRINE AND RELATED FACTORS IN THE CONTROL OF METABOLISM IN NONMAMMALIAN VERTEBRATES D. A. Gapp

14. Introduction ................................................ 511

15. Gastroenteropancreatic Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 515

1. Characteristics and Origins ................................. 515 2. The GEP Hormones ....................................... 528 3. Modes of GEP Hormone Delivery ........................... 539

16. The Gastrointestinal Endocrine System . . . . . . . . . . . . . . . . . . . . . . . . . 541

1. Introduction .............................................. 541 2. Hormones of the Mammalian Gastrointestinal Tract ............. 542 3. Possible Gut Hormones in Invertebrates and Protochordates ....... 551 4. Gut Hormones in Nonmammalian Vertebrates .................. 554 5. Hormonal Control of Gastrointestinal Function ................. 561 6. Conclusions .............................................. 577

17. The Endocrine Pancreas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 579

1 . Introduction .............................................. 579 2. Organization of the Pancreatic Islets .......................... 579 3. Comparative Aspects of Islet Morphology ..................... 584 4. Evolutionary Considerations of Morphology ................... 599 5. Control of Synthesis and Release of Pancreatic Hormones ........ 604 6. Comparative Aspects of Pancreatic Endocrine Secretion .......... 610 7. Summary and Conclusions .................................. 620

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18. Hormonal Control of Metabolism 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 623

1 0 Metabolic Pathways 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 623

20 Regulation of Metabolic Pathways 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 630

3 0 Hormonal Control of Intermediary Metabolism in Vertebrates 0 0 0 0 0 634

40 Cyclostomes 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 636

50 Elasmobranchs 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 637

60 Teleosts 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 639

7 0 Amphibia 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 645

80 Reptiles 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 648

90 Birds 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 652

100 Appendix: Classification of Chordata 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 658

110 Selected Readings 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 660

Index 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 661