Table Of ContentZoophysiology Volume 3]
Editors
S. D. Bradshaw W. Burggren
H. C. Heller S. Ishii H. Langer
O. Neuweiler D. J. Randall
Zoophysiology
Volumes already published in the series:
Volume 1: P. J. Bentley Volume 17: R.J.F. Smith
Endocrines and Osmoregulation The Control of Fish Migration
(1971) (1985)
Volume 2: L. Irving Volume 18: E. Gwinner
Arctic Life of Birds and Mammals Circannual Rhythms (1986)
Including Man (1972) Volume 19: J. C RUegg
Volume 3: A. E. Needham Calcium in Muscle Activation
The Significance of Zoochromes (1986)
(1974) Volume 20: J.-R. Truchot
Comparative Aspects of Extra
Volume 4/5: A. C Neville
cellular Acid-Base Balance (1987)
Biology of the Arthropod Cuticle
(1975) Volume 21: A. Epple and J.E.
Brinn
Volume 6: K. Schmidt-Koenig
The Comparative Physiology of the
Migration and Homing in Animals
Pancreatic Islets (1987)
(1975)
Volume 22: W. H. Dantzler
Volume 7: E. Curio Comparative Physiology of the
The Ethology of Predation (1976) Vertebrate Kidney (1988)
Volume 8: W. Leuthold Volume 23: G. L. Kooyman
African Ungulates (1977) Diverse Divers (1989)
Volume 9: E. B. Edney Volume 24: S. S. Guraya
Water Balance in Land Arthropods Ovariant Follicles in Reptiles and
(1977) Birds (1989)
Volume 10: H.-U Thiele Volume 25: G. D. Pollak and
Carabid Beetles in J. H. Casseday
Their Environments (1977) The Neural Basis of Echolocation
in Bats (1989)
Volume 11: M.H.A. Keenleyside
Diversity and Adaptation in Volume 26: G. A. Manley
Peripheral Hearing Mechanisms in
Fish Behaviour (1979)
Reptiles and Birds (1989)
Volume 12: E. Skadhauge
Volume 27: U M. Norberg
Osmoregulation in Birds (1981)
Vertebrate Flight (1990)
Volume 13: S. Nilsson
Volume 28: M. Nikinmaa
Autonomic Nerve Function in the
Vertebrate Red Blood Cells (1990)
Vertebrates (1983)
Volume 29: B. Kramer
Volume 14: A.D. Hasler Electrocommunication in Teleost
Olfactory Imprinting and Homing Fishes (1990)
in Salmon (1983)
Volume 30: W. Peters
Volume 15: T. Mann Peritrophic Membranes
Spermatophores (1984) (1991)
Volume 16: P. Bouverot Volume 31: M. S. Kaulenas
Adaption of Altitude-Hypoxia Insect Accessory Reproductive
in Vertebrates (1985) Structures (1992)
M. S. Kaulenas
Insect
Accessory Reproductive
Structures
Function, Structure, and Development
With 30 Figures
Springer-Verlag
Berlin Heidelberg New York London
Paris Tokyo Hong Kong Barcelona
Budapest
Professor Dr. M. S. KAULENAS
University of Massachusetts at Amherst
Zoology Department
348 Morrill Science Center
Amherst, MA 01003, USA
ISBN-13:978-3-642-84082-1 e-ISBN- 13 :978-3 -642-84080-7
DOl: 10.1007/978-3-642-84080-7
Library of Congress Cataloging-in-Publication Data. Kaulenas, M. S. Insect accessory re
productive structures: function, structures, and development 1 M. S. Kaulenas. p. em. -
(Zoophysiology; v. 31) Includes bibliographycal references and index.ISBN-13:978-3-642-
84082-1 (U. S.) I.Insects-Generative organs.2.Insects-Reproduction. I. Title. II. Series.
QL494.K38 1992 91-27958 595.7'016-dc20
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© Springer-Verlag Berlin Heidelberg 1992
Softcover reprint of the hardcover 1st edition 1992
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Preface
In retrospect, the range of topics covered in this monograph,
although forming a coherent ensemble, is so extensive that a
detailed discussion could easily extend to three or four times the
current length. My approach has been to identify the critical
issues, summarize the major accomplishments, and to suggest
promising avenues for future research. To facilitate this sum
mary presentation, I have limited the literature review largely to
material published after 1970, extending to material appearing
late in 1990.
I gratefully acknowledge the advice of many colleagues,
particularly the valuable criticisms of Drs. Warren Burggren,
Joseph Kunkel, Randall Phillis, and John Stoffolano. I also
wish to thank Mrs. Elizabeth Brooks for secretarial assistance.
Finally, thanks are due to Dr. D. Czeschlik and his staff at
Springer Verlag for their patience and support.
Amherst, MA, October 1991 M. S. KAULENAS
V
Contents
Chapter 1 Introduction ........................... 1
Chapter 2 The Reproductive Elferent Duct Systems
and Associated Structures. Development and Genetic
Control of Differentiation ......................... 5
2.1 Origin of the Germ Cells and Associated Cells
and Tissues ................................ 5
2.2 Differentiation of the Efferent Duct System
and Associated Structures ................... 9
2.2.1 The Male System .. .. .. . . .. . .. . .. . .. . .. . . .. . 9
2.2.2 The Female System ......................... 13
2.3 Genetic Control of Sexual Differentiation ..... 16
2.3.1 Daughterless............................... 17
2.3.2 Sex Determination: Measurement
of the X:A Ratio.......................... 20
2.3.3 Sex Lethal ................................. 22
2.3.4 Genes Controlling Somatic Sexual
Differentiation ............................. 24
2.3.5 Dosage Compensation ...................... 29
Chapter 3 Structure and Function of the Female
Accessory Reproductive Systems . . . . . . . . . . . . . . . . . . . . 33
3.1 General Overview ......................... . 33
3.2 Accessory Systems Associated with the Ovary .. 38
3.2.1 Follicle Cells: General Observations .......... . 38
3.2.2 Yolk Protein Synthesis by Follicle Cells ...... . 43
3.2.3 The Vitelline Membrane ................... . 46
3.2.4 The Chorion ............................. . 50
3.2.5 Other Synthetic Activities of Follicle Cells .... . 75
3.2.6 Nurse Cells and Trophocytes ................ . 75
3.3 Duct-Associated Structures ................. . 82
3.4 The Ectadenia ............................. 84
3.4.1 Spermatheca and Spermathecal
Accessory Glands .......................... 84
VII
3.4.2 Other Accessory Glands .................... . 90
3.5 Fat Body ................................. . 96
3.5.1 General Description ....................... . 96
3.5.2 Development ............................. . 100
3.5.3 Vitellogenesis ............................. . 102
Chapter 4 Structure and Function of the Male
Accessory Reproductive Systems . . . . . . . . . . . . . . . . . . . . 123
4.1 Accessory Systems Associated with the Testis .. 123
4.2 Structures Associated with the Vasa Deferentia
and the Seminal Vesicles .................... 124
4.3 Male Accessory Glands and Ejaculatory
Duct-Associated Structures .................. 125
4.3.1 Orthoptera ................................ 126
4.3.2 Lepidoptera ............................... 142
4.3.3 Coleoptera ................................ 145
4.3.4 Diptera ................................... 150
Chapter 5 Concluding Remarks .................... 157
References ....................................... 159
Subject and Species Index ......................... 207
VIII
Chapter 1
1 Introduction
The last decade has been a very exciting one in developmental biology, as a combi
nation of new approaches in cell biology, embryology, genetics, and molecular biology
has allowed progress on a number of long-standing questions. Before this recent
explosion of information, it could be plausibly maintained that studies of develop
ment largely reformulated, in more up-to-date terms, questions originally posed by
workers of the late nineteenth and early twentieth centuries. Such reformulations
need not imply a deeper understanding ofthe problems. In fact, many developmental
biologists were pessimistic about the utility of adopting molecular approaches to
problems in cell differentiation. From this point of view, analyses of systems at more
detailed levels of structure do not contribute to the solution of problems, but rather,
as Davenport (1979) stated, lead to "a disappearance of the phenomena we are
concerned with and the reappearance of new problems of form in association with
new structural levels. Properties appear and disappear as each new structural level is
reached, but the formal problems associated with the emergence of physical systems
remain." Development, viewed as the successive emergence of progressively higher
levels of order, would be unanalyzable by reductionist approaches if there were no
possibility for interconnecting the different levels of complexity.
It seems now likely that such views are too pessimistic. For instance, analysis of
the genes which control early events of embryogenesis has revealed a cascade of
interactions between transcriptional regulators, leading to the positional specifica
tion of cells (Ingham 1988). Molecular mechanisms behind pattern formation, em
bryonic induction, and cell-cell interactions in general, as well as the nature of the
"determined" state are emerging (Dressler and Gruss 1988; Yarden and Ullrich 1988;
Harrison and Aggarwal 1990; Takeichi 1990). Such definitions begin to provide the
basis for interconnections between the various structural levels encountered in
development.
In these emerging molecular and genetic definitions of developmental problems,
such as the establishment of the embryonic axis and the specification of segmental
identity, insect systems, especially that ofthe fruit fly Drosophila, are playing a leading
role. While the focus is on the events taking place during actual development, a
number of accessory reproductive structures play vital roles in establishing the
background against which the differentiative processes take place. For example, none
of the dramatic events of embryogenesis would be possible without the provision of
adequate energy resources to the egg, or the supply of most of the components of the
protein synthetic machinery. Equally, systems that ensure the physical survival of the
egg, as well as those designed to deliver viable sperm, are essential. Accessory
reproductive systems which play out their roles away from the oocyte itself therefore
perform vital functions in enabling the complicated interplay of development to
occur. Such accessory systems also provide outstanding models for the analysis of a
1
variety of questions in cell biology, endocrinology, and genetics. These accessory
systems and their contribution to insect development are the subjects of the present
volume.
The scope of the coverage is illustrated and summarized in Fig. 1. From a
developmental perspective, the central site of action is the ovary. As documented in
Section 3.2, three basic types of ovary organization are found in insects: (1) the
panoistic ovary, in which most ofthe informationaUinstructive resources ofthe oocyte
are provided by the synthetic activity of the oocyte nucleus itself; (2) the meroistic
polytrophic ovary, in which a number of cells derived from the germinal tissue, termed
nurse cells, form a part of the egg chamber and supply the bulk of the nonyolk
cytoplasmic content of the mature oocyte; and (3) the meroistic telotrophic ovary, in
which a syncytium of trophocyte cells provides informational and other components
to growing oocytes via specialized organelles called trophic cords. In the vast majority
of species, in all three types of ovary, the nutritive, or yolk, contribution is supplied
largely by the fat body, a metabolically versatile and multifunctional tissue (Sect. 3.5).
In some cases, the follicle cells can serve as additional sources of yolk (Sect. 3.2.2).
Another follicle cell function is the formation of the protective layers ofthe egg. These
include the vitelline membrane and the chorion (Sects. 3.2.3, 3.2.4). Ovary and
oviduct-associated secretory cells can have important contributions to various aspects
of egg production. Possibly the most significant of such structures are the spermathe
cal accessory glands (Sect. 3.4.1), and the female accessory glands, such as the
collaterial glands (Sect. 3.4.2). Lastly, various secretory functions of the vagina may
playa role in egg production.
With regard to male accessory reproductive structures, the accessory glands are
of major significance; such glands enable the transfer of the sperm to the female (Sect.
4.3). In many cases this involves the production of a spermatophore, a packaging
device for sperm, which facilitates sperm transfer. Various ancillary functions, which
affect sperm survival or impinge on postmating female behavior, are often,associated
with spermatophore production. Other secretory activities of the male efferent
reproductive ducts, such as the products of the vas deferens or the ejaculatory duct,
also facilitate the mating process (Sects. 4.2, 4.3). The synthetic activities and the
definitive morphological characteristics of most of these structures are influenced by
either juvenile hormone and/or ecdysteroids, at some stage, and provide important
experimental systems for the investigation of the effects of hormones on develop
mental processes. Together, these various systems make important contributions,
whether direct or indirect, to the analysis of embryonic development.
2
o
~
FAT BODY
00 0 cJ
o 0
•
B
,
TESTIS-ASSOCIATED GLANDS
A VAS DEFERENS '-}
-..... F
I'
L•ATE RAL
~ SEMINAL VESICLE
C
O.
COLLATERAL GLANDS
ACCESSORY G..L.A NDS
E"
SPERMATHECAL GLANDS
, G
VAGINA ------to _ EJACULATORY ~UCT
H
Fig.l. Diagrammatic representation of the female (left) and male reproductive systems and associ
ated structures. The full range of complexity for the oviducts, accessory glands and vagina for the
female and the accessory glands for the male are not illustrated, but are discussed in detail under the
appropriate sections in the text. Thick lines ectodermally derived structures. Thin lines mesodermally
derived structures. A-HThe major products or activities of reproductive system-associated structures.
A Yolk protein, vitelline membrane, chorion. B rRNAs, mRNAs and other cytoplasmic components.
C Variable secretory contribution to egg-laying. D Trophic secretions; egg cases; glues. E Sperm
storage and maintenance. F Generally various nutritive secretions. G Formation of spermatophore
and various fecundity-enhancing and female receptivity limiting factors. H In cases where the duct is
secretory, generally the production of materials which influence the female's physiology; Vg
vitellogenin
3
Description:In retrospect, the range of topics covered in this monograph, although forming a coherent ensemble, is so extensive that a detailed discussion could easily extend to three or four times the current length. My approach has been to identify the critical issues, summarize the major accomplishments, and
