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Histology and Ultrastructure of Wing

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Histology and Ultrastructure of Wing 1 HISTOLOGY AND ULTRASTRUCTURE OF WING DEVELOPMENT IN ONCOPELTUS FASCIATUS DALLAS (HEMIPTERA: LYGAEIDAE) BY NIVEDITA MALLELA M. Sc, A thesis submitted for the degree of Doctor of Philosophy in the University of London Department of Zoology and Applied Entomology Imperial College of Science and Technology South Kensington LONDON SW 7. September, 1979. 2 ABSTRACT The postembryonic development of the fore and hind wings of Oncopeltus fasciatus has been studied by various methods. A morphological account is given of the adult wings, including their venation, basal attachment and axillary sclerites. The development of the tracheal supply to the larval wing pad is described in relation to the venation, with information on tracheal variation and the processes of tracheal retractiōn and degeneration in the adult insect. The bearing of these results on the venational homologies of the Heteroptera is discussed and a system of homologies and terminology is proposed. Light-microscope histological investigations provide a detailed account of the differentiation of the wing pad at selected intervals throughout the moulting cycle and the inter-moult period. The formation of lacunae is described and it is shown that their development (with which that of the veins is related) precedes the growth of the associated tracheal supply. Paranotal regions of cell proliferation have been discovered in the prothorax and are perhaps serially homologous with the wings, but they regress later in post- embryonic life. Parallel ultrastructural studies were made of the cuticle, epidermis, tracheae, tracheoles and innervation of the developing wing pads and the young adult wings. These supplement and extend the above histological observations and include detailed accounts of changes in cell organelles during apolysis, ecdysis and the inter- moult period from the earliest appearance of wing rudiments in the third larval instar. Haemocytes, epidermal glands, macrotrichia and microtrichia are also described. The collapse, retraction and 3 degeneration of the tracheal system, and the degeneration of the wing epidermis after the formation of veins and trabeculae occur in the adult wings within 48 hours of emergence and are described. The work is illustrated with numerous line drawings and electron micrographs. 4 ACKNOWLEDGEMENTS I am grateful to Professor T. R. E. Southwood. F. R. S. for providing me with a place in the department to undertake this work. I owe a debt of gratitude to my supervisor, Mr IL G. Davies for his invaluable guidance, constructive criticism, constant encouragement and support throughout the course of this study. I am also grateful to him for translating the relevant German literature, and for his care and patience when reading my manuscript. He has proved to be not only a guide but also a great teacher to me. I thank Mr C. L. Meredith, Departmental Superintendent, for providing me with all the necessary technical facilities and for his personal help. I am extremely grateful to all my colleagues, friends and members of the technical staff who provided me with technical and moral support. In particular I thank Dr R. E. Sinden for explaining the techniques of Electron microscopy; Mr N. L. Costa for providing me with facilities in the Life Sciences E.M. Unit; and Miss M. Singh for technical assistance. I also thank Mr I.J. French, Mrs A. Merry, Mr J. Harmer and Mrs J. Yeadon and the other library staff for their co-operation and help. I have also benefited from discussions with Dr T. Srihari and with my husband Dr Rao I am grateful to my husband for constant encouragement and financial support; and to my father and family for their encouragement and helps I am also pleased to thank Mrs A. Meredith for her great care and interest in typing my thesis. I am also grateful to Mr P. Jayasankar and C. K. M. College Committee for their encouragement and sanctioning leave. 5 TABLE OF CONTENTS Page ABSTRACT ... ... ... ... ... ... ... ... ... 2 ACKNOWLEDGMENTS ... ... ... ... ... ... 4 CONTENTS ... ... ... ... ... ... ... ... ... 5 GENERAL INTRODUCTION ... ... ... ... ... 7 I : MORPHOLOGICAL ASPECTS: 1. The adult wing venation of Oncopeltus fasciatus Dallas ... ... ... ... ... 15 2. The basal attachment and articular S dc rites ... ... ... ... .. 23 3. Tracheation of the larval wing pad ... ... 29 4. Variation of the cubital trachea , , , , , , 40 5. Tracheal retraction ... ... ... ... ... 48 II : HISTOLOGICAL OBSERVATIONS (Light Microscopy): 1. Materials and methods ... ... ... ... 54 2. Mesothoracic wing development ... ...... 55 3. Metathoracic wing development ... ... ... 110 4. Discussion ... ... ... ... ... ... ... 125 III: ULTRASTRUCTURAL OBSERVATIONS: 1. Materials and methods ... ... ... ... ... 142 2. Third larval instar wing pads .. , ... 145 3. Fourth larval instar wing pads ... ... ... 163 (a) cuticle ... ... ... ... ... ... ... 16 3 (b) epidermis 000 000 ... ... ... ... 179 6 Page (c) tracheae and tracheoles ... ... ... 216 (d) nerve supply ... ... ... ... ... 235 4. Fifth larval instar wing pads ... ... ... 240 (a) cuticle ... ... ... ... ... ... 243 (b) epidermis ... ... ... ... ... ... 248 (c) tracheae and tracheole s ... ... ... 278 (d) nerve supply 292 5. Adult wings ... ... ... ... ... ... ... 297 (a) Newly emerged adult wings ... ... 297 (b) 18-hour adult wings ... ... , ... ... 321 (c) 32-hour adult wings ... ... ... ... 341 (d) 48-hour adult wings ... ... ... ... 353 IV : GENERAL DISCUSSION AND CONCLUSIONS ... 366 V : SUMMARY ... ... ... ... ... ... ... ... ... 387 VI : LIST OF ABBREVIATIONS USED IN ILLUSTRATIONS 390 VII : REFERENCES ... ... ... ... ... ... ... ... 394 7 GENERAL INTRODUCTION The subject of the present study is the postembryonic development of the wings in the Large Milk-Weed Bug, Oncopeltus fasciatus (Dallas). This species is a member of the family Lygaeidae in the series Geocorisae (section Pentatomom'orpha) of the suborder Heteroptera. This, and closely allied families from the Lygaeoidea can be distinguished from the Coreoidea by the somewhat reduced venation of the hemelytral membrane. The species was named Lygaeus fasciatus by Dallas (1852). In 1868 Still transferred it to Oncopeltus, under which it has since stood. It is widely distributed in the Western Hemisphere and five of forty-one known species of Oncopeltus are found in the United States; some occur in South America and some in Australia. Oncopeltus fasciatus is a seed-sucking Heteroptera which feeds on various species of Milk Weed plants (Asclepiadaceae). Like most Heteroptera it passes through five larval instars in its growth to the adult, each instar being easily recognisable through its coloration, wing pad size and other features (Andre, 1934). In the third instar, the mesothoracic wing pads appear externally for the first time as small bag-like structures on the posterolateral angles of the meso- thorax. The general biology of Oncopeltus has been reviewed by Andre (1934), and the ease with which it can be reared indoors at room temperature has led to its wide use as an experimental animal (Feir, 1974). An extensive literature deals with the morphology and histol- ogy of wing development in insects, but previous studies have mostly dealt with the holometabolous insects and relatively little is known of the simpler and presumably more primitive processes of wing devel- opment in hemimetabolous species. The main aims of the present work are, therefore, as follows:- (1) To investigate by simple light-microscope study the venation and tracheation of the wings of Oncopeltus; (2) to re-examine the proposed homologies of the principal veins with the help of developmental data; (3) to compare histological details during the various stages of post- 8 embryonic development with published observations on holometabolous species and the much smaller body of information on hemimetabolous forms; (4) to establish the relationships between the tracheae of the wing pad and the developing venation; (5) to examine the differences between the corium and membrane of hemelytra and to suggest possible causes for the tracheal retraction observed in the membrane; (6) to provide new information on the ultrastructural organisation of the developing wing and the changes it undergoes during post embryonic life; and (7) to consider the findings in the light of other published interpretations of cell and tissue differentiation in the insects. The background of available information on these and allied subjects will be dealt with in detail in the course of the thesis, but it is convenient here to summarise some previous work in the fields most intensively studied by earlier workers. 1. Tracheal homologies: Since 1850 or before, taxonomists have tried to use venational characters in the classification of the Heteropteran. A systematic set of homologies applicable in all orders of insects was first proposed by Comstock & Needham (1898, 1918). This was based on the tracheation, in the belief that the wing tracheae, which precede the veins in ontogeny, also determine their paths. They found that the course of the tracheae in many wings was often more readily interpretable than the subsequent venation and therefore provided evidence of the homologies of the veins. They included a little work on the wing-venation of Pentatomidae, considering them to be a generalised type of Heteropteran wing. They found six principal tracheae, with corresponding veins, in each wing and designated them by the now familiar terms: Costa, Sub- costa, Radius, Media, Cubitus and Anal. Handlirsch (1908)
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