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252 Pages·1988·7.36 MB·English
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c. H. Tyndale-Biscoe and P. A. Janssens (Eds.) The Developing Marsupial Models for Biomedical Research With 102 Illustrations Springer-Verlag Berlin Heidelberg New York London Paris Tokyo Dr. C.Hugh Tyndale-Biscoe Division of Wtldlife and Ecology CSIRO, P.O. Box 84 Lyneham, ACT 2602 Australia Dr. Peter A.Janssens Department of Zoology Australian National University GPO Box 4 Canberra City, ACT 2601 Australia Cover motif: Macropus eugenii at weaning. Drawing F. Knight ISBN 978-3-642-88404-7 ISBN 978-3-642-88402-3 (eBook) DOI 10.1007/978-3-642-88402-3 Library of Congress Cataloging-in-Publication Data. The Developing marsupial: models for biomedical research 1 C.H. Tyndale-Biscoe and P.A.Janssens (eds.). p. cm. Based on papers presented at a conference of the Australian Academy of Science, held in Feb. 1986; sponsored by the Australian Society for Reproductive Biology and the Australian Mammal Society. Bibliography: p. Includes index. ISBN 0-387-19047-3 (U.S.) 1. Marsupialia - Development - Congresses. 2. Mammals - Development - Congresses. I. Tyndale-Biscoe, C.H. (C. Hugh) II. Janssens, P.A. (Peter A.), 1938- . III. Australian Aca- demy of Science. IV. Australian Society for Reproductive Biology. V. Australian Mammal Society. [DNLM: 1. Marsupialia - growth & development - congresses. 2. Models, Biological - con- gresses. QL 737.M3 D4891986) QL 737.M3 D48 1988 599.2' 043 - dc19 DNLM/DLC This work is subject to copyright. All rights are reserved, whether the whole or part of the mate- rial is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recita- tion, broadcasting, reproduction on microfilms or in other ways, and storage in data banks. Duplication of this publication or parts thereof is only permitted under the provisions of the German Copyright Law of September 9, 1965, in its version of June 24, 1985, and a copyright fee must always be paid. Violations fall under the prosecution act of the German Copyright Law. © Springer-Verlag Berlin Heidelberg 1988 Softcover reprint of the hardcover 1st edition 1988 The use of registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. 2131/3130-543210 Preface The two most common perceptions of marsupials are that they are rare and unusual species to be conserved or that they are undesirable competitors with agriculture and should be destroyed; consequently most research on marsupials has hitherto been designed to assist in their conservation or control. However, a third perception is now emerging; marsupials provide new and unusual models for biomedi- cal research, which can complement studies done with conventional laboratory and domestic species of mammal. This new perception has in part arisen from the growing body of knowledge about marsupials and in part from the establishment of self-sustaining laboratory colo- nies of several species. Biomedical problems can now be investigated, using marsupials, with the same rigour as in research with conven- tional species. Some aspects of this new perception of marsupial research were explored in February 1986 at a Boden Research Conference of the Australian Academy of Science (reported in Search 19: 267-269, 1986). The conference was sponsored by the Australian Society for Reproductive Biology and the Australian Mammal Society and had financial support from the Academy and the Faculty of Science of the Australian National University. About 50 mammalogists, reproductive physiologists and perinatal physiologists from Australia, New Zea- land, England and the United States came together to discuss "Lacta- tion and the physiological development of the young marsupial". This aspect of marsupial biology provides the greatest potential for contri- buting to problems of general significance; the young of marsupials are born at a very immature stage of development, before differentia- tion of the nervous system or the major physiological systems, and are thereafter accessible for direct investigation. The composition of the milk that sustains the immature young through its long period of dependence changes in all its constituents; this offers the opportunity to investigate the role of particular substances in the development of the young mammal and to investigate the regulation of mammary gland function. At the end of the conference it was decided that the time was opportune for the publication of a book on the subject. Subsequently, through correspondence with Dr. Dieter Czeschlik, Life Sciences Edi- tor, Springer-Verlag agreed to commission a book on this topic and VI Preface contributions were invited from active practitioners in the field of marsupial development and the lactation that sustains the young. The book addresses four main themes: the neonatal marsupial, marsupial lactation, growth and development of the suckling young, and the mutual interaction of the young and its mother. The book was commissioned in November 1986, with manuscripts to be submitted to the publisher in November 1987. We thank all the contributors for their cooperation in enabling us to meet this time- table. In preparing the book we had the full use of the resources of our respective institutions. We thank Chris Collet, Mandy Giuliano, Jenny Grigg, Lyn Hinds, Helen Mason and Ralph Ogden for their help with the preparation of the manuscript. We and the authors owe a special debt of gratitude to Helen Blain, who prepared disc files and hard copies of the whole manuscript for direct transmission to the Publishers, and by her timely help appreciably advanced the date of publication. Finally we wish to express our appreciation of the excellent co- operation and help that we have received from the staff at Springer. C. Hugh Tyndale-Biscoe Peter A. Janssens Contents Chapter 1 Introduction C. H. Tyndale-Biscoe and P. A Janssens (With 1 Figure) 1 Chapter 2 Structural Adaptations of the Newborn Marsupial RL.Hughes and L.S.Hall (With 29 Figures) . . . . . . . . . . . 8 Chapter 3 Patterns of Growth A Cockburn and C. N.Johnson (With 6 Figures) . 28 Chapter 4 The Composition of Marsupial Milk B. Green and J. C. Merchant (With 6 Figures) . 41 Chapter 5 Hormonal Control of Lactation L. A Hinds (With 5 Figures) ........ . 55 Chapter 6 Control of Milk Protein Synthesis in the Marsupial Macropus eugenii: a Model System to Study Prolactin- Dependent Development K. R Nicholas (With 8 Figures). . . . . . . . . . . . . . 68 Chapter 7 Growth of the Brain J. E. Nelson (With 3 Figures) ... 86 Chapter 8 Differentiation of the Neocortex M.L.Reynolds and N.RSaunders (With 5 Figures) 101 Chapter 9 Development of the Marsupial Primary Visual Pathway S. A Dunlop, L.-A Coleman, A M. Harman, and L. D. Beazley (With 7 Figures) . . . . . . . . . . . . . . . . . . . . . . . . . .. 117 Chapter 10 Development of the Marsupial Cardiorespiratory System R V. Baudinette, S.1. C. Runciman, P. F. Frappell, and B.J.Gannon (With 8 Figures) ........ . 132 Chapter 11 Metabolism and the Development of Endothermy AJ.Hulbert (With 6 Figures) . . . . . . . . . . . . . . . . . . .. 148 VIII Contents Chapter 12 Changes in Nutritional Metabolism During Weaning P.A.Janssens and M. Messer (With 7 Figures) .. ....... 162 Chapter 13 The Development of Renal Function G. E. Wilkes and P.A.Janssens (With 9 Figures) ......... 176 Chapter 14 Immunological Development in Pouch Young Marsupials E. M. Deane and D. W. Cooper . . . . . . . . 190 Chapter 15 Sexual Development in Marsupial Pouch Young R V.Short, M.B.Renfree, and G.Shaw (With 2 Figures) . . . .. 200 References . . 211 Subject Index 241 List of Contributors The addresses are given at the beginning of each contribution Baudinette, R. V. 132 Janssens, P. A 1 Beazley, L. D. 117 Johnson, C. N. 28 Cockburn, A 28 Merchant, J. C. 41 Coleman, L.-A 117 Messer, M. 162 Cooper, D. W. 190 Nelson, J. E. 86 Deane, E. M. 190 Nicholas, K. R. 68 Dunlop, S. A 117 Renfree, M. B. 200 Frappell, P. F. 132 Reynolds, M. L. 101 Gannon, B.J. 132 Runciman, S. I. C. 132 Green, B. 41 Saunders, N. R. 101 Hall, L.S. 8 Shaw, G. 200 Harman, AM. 117 Short, R. V. 200 Hinds, L. A 55 Tyndale-Biscoe, C.H. 1,162, Hughes, R. L. 8 176 Hulbert, AJ. 148 Wilkes, G. E. 176 CHAPTER 1 Introduction C. H. Tyndale-Biscoe1 and P. A. Janssens2 The feature that most clearly distinguishes marsupials from most other mammals is the immaturity of their young at birth. Only newly hatched monotremes are as immature, whereas even the most altricial young of eutherian mammals, such as insectivores and bears, are more advanced than any marsupial. Many reasons have been proposed for the immaturity of neonatal marsupials: inadequacy of the yolk sac placenta to provide nourishment or gaseous exchange sufficient for the accelerating demands of the growing fetus; insufficient size of the separate uteri or birth canal to accommodate an advanced fetus; lack of immunological protection by the trophoblast; and inability of the corpus luteum to prolong its secretory phase to sustain the luteal phase in the uterus. In the last two decades these several ideas have been examined experimentally and none has proved to be an adequate explanation. The yolk sac placenta of the tammar wallaby, Macropus eugenii, is capable of selective transport of monosac- charides, amino acids and proteins, including immunoglobulins (Renfree 1973) and therefore is a functional placenta. While marsupials have not evolved luteal or placental functions that compare in complexity to those of advanced eutherian species, the potential for such adaptations has been shown to exist (see Tyndale- Biscoe and Renfree 1987). In several macropodid marsupials the extended gesta- tion period is associated with an extended autonomous life of the corpus luteum, analogous to that of the corpus luteum of the Carnivora among eutherian mam- mals, while among the peramelid marsupials there is evidence that the corpora lutea respond to pituitary luteotrophin (Gemmell 1984). In M. eugenii there is evi- dence for a luteolytic effect at the end of pregnancy (Tyndale-Biscoe et al. 1983) and in Isoodon macrourus a luteolytic effect of prostaglandin in mid-lactation (Gemmell 1985). Likewise there is evidence for steroid secretion by the placenta in two species of macropodid (Bradshaw et al. 1975; Heap et al. 1980), and a local influence on the endometrium by the placenta of three species of macropodid (Renfree and Tyndale-Biscoe 1973; Shaw and Rose 1979; Wallace 1981), while the invasive chorio-allantoic placenta of the peramelids (Padykula and Taylor 1976) indicates a potential for the kind of placental adaptations that have evolved in the eutherian mammals. If we accept that marsupials possess the potential for extended gestation but, in an evolutionary sense, have not exploited it, we are drawn to conclude that the 1 Division of Wildlife and Ecology, CSIRO, P.O. Box 84, Lyneham, ACT 2602, Australia 2 Department of Zoology, Australian National University, GPO Box 4, Canberra City, ACT 2601, Australia C. H. Tyndale-Biscoe and P. A. Janssens (Eds.) The Developing Marsupial. Models for Biomedical Research ©Springer-Verlag Berlin Heidelberg 1988 2 C. H. Tyndale-Biscoe and P. A. Janssens emphasis on lactation in marsupial reproduction is an alternative rather than a more primitive form of mammalian reproduction. We may then view the develop- ment of the marsupial as fully equivalent to that of eutherian mammals, in which most early development occurs in the uterus of the mother. In eutherian mammals the intimate nature of the placenta, interposed for most of development between the embryo and its source of nourishment, makes it difficult to investigate the very early development of physiological and neurological function. This does not apply to marsupials, however, because the young are born at a much earlier stage of development (most weigh less than 0,01 % of the mother's weight at birth) and their physiological systems and biochemical pathways develop during the ensuing lengthy lactation (Fig. 1.1), throughout which they are fully accessible for study. Therefore, marsupials offer much more accessible models than the several euthe- rian species currently in use for the study of early development of mammalian organ systems and the differentiation of their physiological and biochemical func- tions. Despite the extreme immaturity of most of its systems, the neonatal marsupial, paradoxically, is as well-developed in certain respects as the much more mature neonatal eutherian (see Chapter2). For instance, in most species of marsupial the 2.0 Continuously attached Intermittently Eating Out o f· pouch ___to _teat_s _1 11111111a111t11t ached to te111a111 _t g_ras_s _ weaned 1.5 Ectothermic EndothermiC _______. I/IJI ___~ ~---- Weigh t (kg) Nephrogenesis complete 1.0 Eyes open ~ 6 layers in cerebra l co rtex j 0.5 laPchtastieosn 0c1y cle [:::;::::::J.~• •••••••~ ._ I ___~ __- 2a 2b 3 Fig. 1.1. Summary of events in the growth and development of Macropus eugenii and corre- sponding changes in the phases of the lactation cycle. Phase 1 is the period of lactogenesis during pregnancy; it is followed by Phase 2, which is divided into an early phase when the young is con- tinuously attached to one teat and a later phase when the young begins to relinquish the teat but is still wholly dependent upon milk for its nourishment; at the end of this phase it is physiologically mature and makes its first exit from the pouch. During Phase 3 it gradually shifts from a diet of milk to one of herbage. These changes in the young are matched by changes in the composition of the milk and the control of lactation

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