Some titles of related interest BERNHARD, C. G. Functional Organization of the Compound Eye BOYDEN, A. Perspectives in Zoology CAMPBELL, P. N. The Structure and Function of Animal Cell Components CLOUDSLEY-THOMPSON, J. L. Desert Life CLOUDSLEY-THOMPSON, J. L. Spiders, Scorpions, Centipedes and Mites COHEN, J. Living Embryos INGLIS, J. K. A Textbook of Human Biology MARSHALL, P. T. The Development of Modern Biology MUZZARELLI, R. Chitin PARSONS, T. R. & TAKAHASHI, M. Biological Oceanographic Processes ROGER, F. Onchocerciasis in Zaire WHITE, D. C. S. & THORSON, J. The Kinetics of Muscle Contraction Full details of all books listed will gladly been sent upon request Morphology and Evolution of the Insect Abdomen WITH SPECIAL REFERENCE TO DEVELOPMENTAL PATTERNS AND THEIR BEARINGS UPON SYSTEMATICS R Y U I C HI M A T S U DA Biosystematics Research Institute, Canada Department of Agriculture, Ottawa, Ontario PERGAMON PRESS OXFORD • NEW YORK • TORONTO SYDNEY • PARIS . FRANKFURT U. K. Pergamon Press Ltd., Headington Hill Hall, Oxford OX3 OBW, England U. S. A. Pergamon Press Inc., Maxwell House, Fairview Park, Elmsford, New York 10523, U.S.A. CANADA Pergamon of Canada, Ltd., P.O. Box 9600, Don Mills M3C 2T9, Ontario, Canada AUSTRALIA Pergamon Press (Aust.) Pty. Ltd., 19a Boundary Street, Rushcutters Bay, N.S.W. 2011, Australia FRANCE Pergamon Press SARL, 24 rue des Ecoles, 75240 Paris, Cedex 05, France WEST GERMANY Pergamon Press GmbH, 6242 Kron- berg/Taunus, Pferdstrasse I, Frankfurt- am-Main, West Germany Copyright © 1976 Pergamon Press Ltd. All Rights Reserved. No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means: electronic, electrostatic, magnetic tape, mechanical, photocopying, recording or otherwise, without permission in writing from the publishers First edition 1976 Library of Congress Cataloging in Publication Data Matsuda, Ryuichi. Morphology and evolution of the insect abdomen. (International series in pure and applied biology; v. 56: Zoology division) 1. Insects—Evolution. 2. Insects—Anatomy. 3. Abdomen. I. Title. QL468.7.M37 1975 595.7'04'9 75-22473 ISBN 0-08-018753-6 Printed in Hungary Introduction THIS is the third of a series of works in which the structural evolution of insects is studied. This volume deals primarily with the evolution and homologies of skeletal structures of the abdomen and the internal reproductive system. As in the previous works on the head (Matsuda, 1965) and thorax (Matsuda, 1970), the data for analysis and synthesis are derived almost exclusively from published works. Special attention has been paid to devel- opmental processes, with the initial intention of clarifying the developmental bases of homologies of the structures that occur in the insect abdomen. It soon became apparent, however, that the nature of insect development cannot be adequately understood without reference to modern concepts of developmental biology and evolution. Further, it became increasingly evident that analysis of the developmental data yielded ideas pertinent to systematic entomology and zoology; hence the discussion in Part I and the subtitle of this work. Part I is not to be read as an independent section, since the principles discussed there are applied in Part II (a general discussion on the insect abdomen) and in Part III (special discussions on the abdomen in individual orders), and the principles in turn could never have been discovered without knowing the facts presented in these parts. The whole work is therefore expected to be coherent, all parts being relevant to one another. Excuse for certain omissions is now in order. In this work musculature is not treated. My previous experiences (1965, 1970) now convince me that the homologies of the kinds of structures treated in this work can safely be established without reference to the associated musculature. As far as the genitalia are concerned, attention has been paid primarily to homologies of genitalic parts at the subordinal and ordinal levels, and the study of the genitalia will be extended along with the study of musculature in the future. The development of the gonad is not fully treated here since enough summaries and books pertinent to this subject have appeared in recent years. Most of the figures appearing in this work have been borrowed from published works; however, the terminologies used in explaining these figures are based primarily on my own interpretations and usage, and often differ from those originally used. This work was started in the summer 1969 and was completed in the summer 1974. yii Acknowledgements MY thanks goes to J. A. Dowries (Ottawa) for the discussions I had with him during the course of this study. He also edited, at one time or another, a substantial portion of the manuscript. I am also indebted to many of my colleagues here in Ottawa in completing this work. E. G. Munroe has often given me cogent suggestions and read portions of the manuscript. K. G. A. Hamilton, G. P. Holland, E. E. Lindquist, J. F. McAlpine, A. Mutuura, W. R. Richards, F. Schmid, A. Smetana and C. Yoshimoto have given me valuable infor- mation and criticism on the portions of the manuscript of their specialties (mainly Part III). A. R. Soponis has often been the first victim to hear about the "new ideas" that developed in this study. N. Sussmann and other library staff have been highly cooperative in litera- ture search. I have also benefited from occasional conversations with other colleagues in various ways, scientific as well as linguistic, and I now hope that I have a right amount of "the" in the manuscript. I have also received help from scientists outside Ottawa. S. J. Gould (Cambridge, Mass.), C. D. Michener (Lawrence, Kans.) and V. R. L. Vickery (Macdonald College, Que.) read Part I of the manuscript and gave valuable comments. D. K. McE. Kevan (Macdonald College, Que.) suggested improvements in the portion of the manuscript on Orthoptera, and C. W. Sabrosky (Washington, D.C) provided information on Diptera. viii 1. Morphogenetical regularities and anagenesis Anagenesis is a progressive evolution of structures and organs which lead to their improve- ment and perfection in functional and physiological terms. It is implicit that in anagenesis natural selection has been the directing force of this improvement. Huxley (1953) goes so far as to say "natural selection plus time produce biological improvement (or anagenesis). Rensch (1959) recognized 6 essential principles of anagenesis: (1) increased complexity, (2) rationalization of structures and function (including increased centralization), (3) special complexity and rationalization of the central nervous system, (4) increased plasticity of structures and functions, (5) improvement permitting further improvement (partly identical with (4)), and (6) increased independence from the environment and increased command of environmental factors (progression of autonomy). The question here is what kinds of morphogenetical regularities are involved in the struc- tural changes that accompany anagenesis. Of the above 6 principles of anagenesis, as Rensch's discussion shows, (1) involves differentiation of preexisting structures, which sometimes leads to production of new structures', (2) involves interiorization (inward shift) of structures and fusion of similar structures and thereby superfluous parts are eliminated; (3) involves differentiation of nervous parts, and purely quantitative increase (growth) of nerve cells; (4) to (6) refer to general improvement in physiology and adaptability, although such improvements cannot be independent of structural alteration. Remane (1956) recognized 4 regularities in alteration that bring the structural organiza- tion of animals and plants to perfection (Vervollkommnungsgesetze)* They are (1) decrease and increase in number of similar structures, (2) differentiation, (3) interiorization, and (4) concentration (fusion). Several morphogenetical regularities that are evident in the above analysis of principles of anagenesis and the law of perfection, are reduction which may lead to loss of structures (evident in the decrease in number of similar structures of Remane), fusion, differentiation, shift in position (interiorization) of structures, and production of new structures. These regularities are called here "morphogenetical regularities of anagenesis." The understanding of various principles of structural evolution is greatly facilitated if they are studied in terms ofthese regularities and anagenesis, as seen in the discussion in following chapters (hetero- chrony, substitution, homology). Apparent morphogenetical regularities are often the con- sequence of complex developmental processes and the relationships between various regularities are also complex, as discussed below. •The laws of perfection {Vervollkommnungsgesetze) conceived of by earlier zoologists implied the structural alteration, driven by inner autonomous force, from a lower to a higher level of organization in animals and plants. When the "inner autonomous force" is replaced by natural selection, the laws are roughly equivalent to anagenesis. 4 MORPHOLOGY AND EVOLUTION OF THE INSECT ABDOMEN Reduction and loss. Reduction and loss of simple structures are largely matters of growth, and they can be analyzed quantitatively. When a simple structure grows more slowly than the standard organ (e.g. the total body size), the growth is negatively allometric, and when it grows faster than the standard organ the growth is positively allometric. If the positive allometric growth rate of a structure remains unchanged during phylogeny and if the body size decreases in descendants, the size of the structure is bound to be relatively smaller in the descendants. The reduction of the sword-like extension of the tail of the fish Xiphophorus, cited by de Beer (1958), illustrates this type of reduction. Conversely, if a structure is nega- tively allometric, it may become reduced or even vestigial with the increase in body size in descendants. Rensch (1959) showed some examples of reduction due to negative allometry. In Gerridae (Heteroptera), as Matsuda (1960) showed, the hind leg and the body size have become reduced in evolution of most taxa, and the underlying growth patterns are more complex than in the above examples. Apart from the total loss of a structure due to loss of the genetic factor producing it, the apparent loss of structures seen in the adult is often due to regression during development, as seen in the degeneration of the female accessory glands in Orthoptera, some thoracic muscles (Matsuda, 1970), the embryonic abdominal appendages (p. 62), the stylus in the female Blattaria and Isoptera, etc. The degeneration of functional mouthparts in adult Ephemeroptera is also a well known case of regression, de Beer (1958) showed various similar examples in which structures occur only during developmental stages; all these cases of regression represent one aspect of heterochrony (p. 9). Sometimes regression of structures during development is incomplete and the structures are retained in the adult as nonfunctional vestigial organs; and their existence is, as is generally believed, apparently tolerated by natural selection. The left ejaculatory duct in the male of higher Dermaptera is such a nonfunctional vestigial organ. Sometimes, however, the vestigial organs are so modified as to be functional, as seen in the haltere in Diptera and ear bones of mammals, etc. Sometimes loss of structures occurs through nondifferentiation. In other words, some structures formed in other related species (groups) simply do not differentiate in some animals. Examples of nondifferentiation include fewer numbers of abdominal segments that differentiate in Collembola and sternorrhynchous Homoptera, many structures (characters) that do not differentiate in viviparous female Aphididae (Homoptera) and Isoptera, etc. All of these cases of nondifferentiation relate to neoteny which is to be dis- cussed later (p. 10). Fusion. Outstanding examples of fusion of structures in insects are segmental ganglia (p. 105), the incompletely fused abdominal appendages in Collembola, and the fused second maxillary appendages, the labium. Fusion of structures is a widespread phenomenon and does not require further explanation. Differentiation. In embryology (and hence in ontogeny) differentiation means formation of structures and organs from undifferentiated or less-differentiated tissues or rudiments in earlier stages of development. From the viewpoint of structural evolution, important aspects of differentiation are morphogenetical potencies of cells and rudiments and subse- MORPHOGENETICAL REGULARITIES AND ANAGENESIS 5 quent developmental processes, as will be repeatedly discussed in dealing with substitution (p.24), heterochrony (p. 9) and related concepts. The term "differentiation" as used by Remane (1956) refers primarily to the differentiation of parts of a complex structure seen in the adult. The differentiation in the sense of Remane therefore applies to the end-results of morphogenesis. Most differentiations of complex organs and structures in the adult are what Remane (1956) called "additive differentiation" which leads to functional differentiations of parts (division of labour). Heterodonty in mammals, heterochelae in the crab, and differentiation of appendage pairs in Crustacea are outstanding examples of additive differentiation. In the Insecta tagmosis or differentiation of body segments into discrete regions (head, thorax, and abdomen) is an example of additive differentiation that has occurred on the scale of a class. The modification of mouthparts into a sucking organ in various orders by differentiation of preexisting parts is another good example of additive differentiation that has occurred on the scale of an order. Clearly in these processes of differentiation, unequal growths of preexisting parts (reduction, loss, enlargement) and fusion of parts have taken place. The facultative differentiation (Verteilungsdifferenzierung of Remane, 1956) refers to the differentiation from the undifferentiated rudiment into one of the two alternative states in the adult. Differentiation of the undifferentiated gonad in the early developmental stage either into the ovary or the testis is a typical case of facultative (optional) differentiation. Other kinds of differentiation include polymorphism and alteration of biologically different generations (polyp and medusa in Cnidaria, bisexual and parthenogenetic generations in many animal groups). These differentiations are not treated in this work. Sometimes the dominant trend of the additive differentiation has been reversed, and the highly differentiated structures have reverted into former less-differentiated conditions of the structures (Entdifferenzierung of Remane). A case cited by Remane was the reversal of the vertebrae to a more normal condition as a result of reduction of appendages in the whale, snake, etc. A comparable case in insects is the reversal of the highly differentiated dipterous pterothorax to a more generalized pterothorax in Chionea, as a result of the loss of the wing (Matsuda, 1970). Shift in position of structures. In the insect abdomen the shift in position of posterior seg- ments (especially the 12th segment) occurs through fusion, loss, differentiation, and non- differentiation of neighboring segments, as seen in the discussion on pp. 51-62. The same applies to the shift of wing veins. Shift in position of structures occurs also through rotation of the structures during development. In many Diptera rotation of the genital and postgenital segments occurs either by 180° or 360° (seep. 347). In chalastogastrous Hymenoptera and some Coleoptera only the penis is rotated by 180°. In some Heteroptera mild degrees of rotation (less than 180°) of the male external genitalia occurs. Rotation of the anterior part of the head and the concomital displacement of the internal structures (hypopharynx and associated muscles) have occurred in Mallophaga. Interiorization refers to the condition of structures which become sunken into the body cavity from their originally superficial positions. In the Insecta an example is the tendency for posterior abdominal segments to be telescoped into cavities of preceding segments in 6 MORPHOLOGY AND EVOLUTION OF THE INSECT ABDOMEN higher orders, such as Hymenoptera (see Oeser, 1961). The spiracle of insects also shows a tendency of interiorization by forming the atrium into which the opening leads; the most generalized type of spiracle is little more than a simple crypt devoid of lips and closing apparatus as seen in Collembola. In insects internal structures such as muscles, nerves, gonads, etc., develop more or less independently of the external structures during ontogeny. Therefore, there is a marked tendency for these structures to differ in their positions relative to the associated external structures in different species (groups), as discussed later (p. 37). Production of new structures. Production of an entirely new organ or structure is generally believed to be rare by most modern evolutionists including Rensch (1959), who thought that new organs result from differentiation of the organ system that evolved a long time ago. Bock (1959), from his study of the basitemporal articulation in birds, thought that the concept of preadaptation and multiple evolutionary pathways can assist in the interpreta- tion of the evolution of new organs. Scudder (1964), among entomologists, accepted Bock's idea and pointed out that the paranota are such preadapted structures which gave rise to the wing in insects. Some caenogenetic structures such as the tracheal gills in nymphal Epheme- roptera and Plecoptera are also modifications of the paranota, and the latter may be con- strued as being preadapted for the production of the tracheal gills in these orders. Scudder (1964) further suggested a possibility that the ovipositor in insects has arisen from the embryonic abdominal appendages which were preadapted for the production of the ovi- positor. As discussed fully (p. 89), however, this concept holds good only for Acrididae (Orthoptera). The aedeagus formation in Homoptera and Heteroptera from the internal parameres present in the plesiomorphic related order Psocoptera may also be considered as an example of production of a new structure from a preadapted structure. The production of new structures in all of these cases involves mainly the modification of clearly defined preexisting structures or areas. Many of the presumed new structures in insects are, however, simply local differentiations of tissues and cells, without involving the modification of clearly defined preexisting struc- tures. Thus, for instance, the functional copulatory organ on the 2nd and 3rd abdominal sterna in Odonata is a quite unique, elaborate new organ, and there is no comparable organ known, either within the Insecta or in other arthropods. The pleural ridge, the basa- lare and subalare are also new developments that arose with acquisition of the wing in early insects. The origin of the anterior valvulae can be attributed only to the local cell differen- tiation on the 8th abdominal sternum in the ancestor of the Thysanura-Pterygota. Sperm- pumps evolved independently at least four times in evolution of higher insects, after the me- thod of the sperm-transfer by means of the spermatophore had been relinquished. The sperm pumps of 4 different origins are in fact structurally distinct. The vagina in the female efferent duct is also another example of new structure that developed independently in many taxa during the evolution of insects. An extra pair of genital appendages, the parameres, are also new structures that arose in some higher groups of insects. Many other abdominal structures considered to be new structures are those associated with the penis (p. 76) and with the gonocoxopodite (p. 80), many glands that occur in the male and female efferent systems (p. 97 and p. 103), the pseudocercus in Dermaptera, etc. MORPHOGENETICAL REGULARITIES AND ANAGENESIS 7 Many other new structures have arisen in other parts of the body. To cite a few, the ptilinal suture and the pseudotracheae are such new structures that arose in the head of the higher Diptera. The pheromone-producing organ in Lepidoptera (Birch, 1970) and many of the other pheromone-producing organs arose independently in different groups of insects. As is clear from the discussion on the increase in number of similar structures (antennal segments, ovarioles, etc., p. 8), production of new structures can occur also through splitting and fragmentation of preexisting structures. An example worthy of note here is the fragmented thoracic sclerites in Embioptera which have the terms of their own (new struc- tures). Some tergopleural muscles in the Pterygota are new muscles that arose mainly by splitting of the preexisting muscles (Matsuda, 1970). Some caenogenetic structures, which are to be discussed later, can also be considered as new structures that arose de novo in imma- ture insects (and other animals). The above examples of production of new structures lead us to believe that the insect tissue forming the external structures is highly plastic, and this plasticity has allowed the production of new structures over and over again, and hence the great diversity of forms in insects. If, as is generally believed, the production of new structures is rare in animals, the production of new structures in insects constitutes a conspicuous exception to the rule. Production of new structures and origin of Odonata and Embioptera. As the reduction of structures due to neoteny has sometimes been the cause of origin of higher taxa in the evolution of insects (p. 16), the production of new structures was also sometimes a major cause of the origin of new taxa. A conspicuous example is the Odonata, in which addition of some new structures has made this order quite distinct from the rest of the pterygote orders. Such new structures (confined to this order) include: the entirely different wing base structures, wing veins, and the wing movement mechanism (including new muscles), the secondary copulatory organs on the 2nd-3rd abdominal sterna, the antealar sinus of the mesothorax, some peculiar larval structures (e.g. lateral appendages), etc. The distally undivided endite lobe in the maxillary and labial segments, and the apparently 2-segmented trochanter also may represent the production of new structures. In Odonata the production of these new structures and the highly pronounced fusion of thoracic segments (synthorax) have been dominant features of structural evolution, and a series of these structural alter- ations has resulted in the origin of this order. In Odonata the opposing tendency of reduc- tion is not pronounced,* and many structures have remained highly plesiomorphic. The reduction or loss of wings, which is usually associated with neoteny, is nowhere evident in this order. The fragmented thoracic sclerites (new structures) in Embioptera represent highly autapomorphic features which separate this order from the related orders Plecoptera and Phasmida. Reduction in number of similar structures. Reduction in number of similar structures, with which Remane (1956) was concerned in dealing with the laws of perfection, occurs through regression, nondifferentiation, and fusion, and numerous examples were given by Dogel * Note the reduction of the penis and the trend of reduction of the ovipositor.