The Physiology of Insect Reproduction

313 Pages·1970·10.972 MB·English

by  Franz Engelmann and G. A. Kerkut (Auth.)

THE PHYSIOLOGY
OF INSECT REPRODUCTION
by
FRANZ ENGELMANN
DEPARTMENT OF ZOOLOGY
UNIVERSITY OF CALIFORNIA AT LOS ANGELES, CALIFORNIA
PERGAMON PRESS
Oxford · New York · Toronto
Sydney · Braunschweig
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First edition 1970
Library of Congress Catalog Card No. 70-114850
Printed in Great Britain by A. Wheat on & Co., Exeter
08 015559 6
PREFACE
THE present monograph is an outgrowth of this writer's interest in gaining for himself a
comprehensive understanding of the basic phenomena governing reproductive processes in
insects. During the several years of intensive reading, I became acutely aware of pertinent
published results contained in a great number of scattered journals and books. Many of
the original papers are not available to many scientists at various colleges, universities, and
research institutes throughout the world. The need to summarize the principle findings thus
became even more compelling. Topics of this monograph range from aspects of sex deter
mination to means of control in insect societies. The book is an attempt to cover all aspects
related to the propagation of the species; it is indeed a biology of the insects.
When a biologist finds a new book, he first looks through those chapters related to his
own research interests and often concludes that the material is covered inadequately. Then
by paging through the remainder of the book, he decides that, on the whole, the book might
not be as bad as he had thought; but he is misled since he does not know all pertinent litera
ture as thoroughly as he does that in his own research field. It is true, no author of today can
deal with all aspects of biology to the same depth with the same comprehension. He naturally
stresses the areas of his own research specialty a little more than the others. The reader will
find that this author is no exception. I tried to extract from the vast literature the essential
information on the topics treated.
This monograph in its present form would not have been possible without the invaluable
help, criticisms, and discussions by some of my colleagues and friends. Various chapters
were read by J. N. Belkin, C. W. C. Davis, and R. C. King and I am indebted to them for
their effort and willingness to spend their time in helping to improve the manuscript.
Furthermore, during the preparation of the manuscript, considerable help was received
from L. Andersen, P. Girard, and J. Malamud; their efforts are gratefully acknowledged.
It is my pleasure to thank Miss G. Beye and Mr. K. Pogany who prepared many of the
illustrations from drafts or originals. Permission to reproduce copyrighted materials was
given by the following publishers: Academic Press, New York; American Association of
Advancement of Sciences, Washington; Canadian Entomological Society; Centre National
de la Recherche Scientifique, Paris; Gauthier-Villars & Cie, Paris; Masson & Cie, Paris;
Museum d'Histoire Naturelle, Geneve; Springer-Verlag, Berlin-Heidelberg-New York;
The Thomas Say Foundation, The Entomological Society of America; Verlag für Recht
und Gesellschaft AG, Basel; Verlag Paul Parey, Berlin; Wistar Institute, Philadelphia.
IX
CHAPTER 1
THE GENITALIA
THE anatomy of the external and internal genitalia in males and females is of interest to
physiologists, morphologists, and taxonomists. While the taxonomist and morphologist
describe and use structural features for classification of the species and attempt to interpret
the structure in terms of ontogenetic and phylogenetic origins, the physiologist can fully
understand function only with a knowledge of the anatomy. Considerations of the functional
anatomy of ovarian development (Chap. 5) and egg maturation as well as those on oviposi-
tion mechanisms may exemplify this. It is neither feasible nor intended to give a full account
here of the genital structures in insect species of all orders. The diversity is enormous; yet
certain common elements are characteristic of nearly all the species (Snodgrass, 1935,
1957; Weber, 1954; Dupuis, 1955; Tuxen, 1956). Certain aspects have been more recently
reviewed by Gouin (1963), who showed how ontogenetic studies of the genitalia become
quite valuable in discerning homologous structures of the species of various orders. Attempts
to bring order to the confusing terminology have been made by Dupuis (1955), Tuxen (1956),
and Snodgrass (1957). In the following short description of the genitalia, basically the
outlines of Snodgrass (1935) and Weber (1954) have been followed.
Male internal genitalia usually consist of two testes, vasa deferentia with vesiculae semi-
nales and accessory glands, and an unpaired ductus ejaculatorius (Fig. 1). Only in the
Ephemeroptera are the original paired gonopores still present. The normally unpaired
ejaculatory duct arises from an invagination of ectoderm and is consequently lined with a
cuticular intima. However, the vasa deferentia can consist of both mesodermal and ecto-
dermal elements. Some variations are found in the genital structures, such as unpaired
seminal vesicles or unpaired accessory glands.
The external genitalia of a male are generally formed from the ninth sternite from an
originally unpaired invagination, the lobi phallici. During further development, this anläge
becomes paired and gives rise to paired mesomeri and parameri (Günther, 1961). The meso-
meri generally fuse to form an unpaired intromittent organ, or phallus, which may bear an
aedeagus; however, depending on the species, the parameres become phallomeres, claspers,
or harpagones which are functional during copula (Snodgrass, 1957; Günther, 1961;
Gouin, 1963). Parameres are considered by some investigators to be homologous to
abdominal appendages similar to the gonapophyses of the female. Some recent studies on
the musculature of the genitalia in a few species, however, do not support this view; these
muscles are of sternal origin and are homologous to those muscles of the pregenital segments
(Matsuda, 1958; Gouin, 1963); if the external genitalia were appendages, they would have
no metameric muscles. This conclusion is based on embryological investigations which
appear to offer reliable criteria since muscles rarely change their original positions or attach-
1
2 THE PHYSIOLOGY OF INSECT REPRODUCTION
ments. Unfortunately, practically no data are available on the details of either the innerva-
tion of the genital muscles or the origin of these nerves. Since the genitalia of the male arise
in the ninth abdominal segment, the gonopore generally comes to lie between the ninth and
tenth sternum, or occasionally, on the tenth sternum.
The female internal genitalia, consisting of paired ovaries and oviducts, a common
oviduct with accessory sex glands and spermatheca, can be shown to originate from abdominal
segments 7 through 9. During development ectodermal invaginations occur in all three
sterna, but later these can no longer be recognized as separate parts. In Ephemeroptera,
FIG. 1. Diagrammatic representation of male genitalia. (a) General structure, (b) Section
through testis. Ac = accessory sex glands. Aed = aedeagus. Dej = ductus ejaculatorius.
F = testis follicle. Go = gonopore. Par = paramer. Per = peritoneal sheath. Phb =
phallobase. Vd = vas deferens. Ves = vesiculum seminalis. Tit = titilator. (Modified from
Weber, 1954.)
paired gonopores are found on the seventh sternum and it is believed that phylogenetically
this is the original type (Palmen, 1884) (Fig. 2). In the most common type, the genital
opening is on the eighth sternum and joins the common oviduct (arising from the anläge of
the seventh sternum) leading anteriad. The opening may be located more anteriorly, due
to secondary modifications of the terminal segments. Accessory sex glands (arising from the
anläge of the ninth sternum) open into the genital atrium or vagina. This type is found in the
Orthoptera, Hymenoptera, Diptera, Neuroptera, and others (Heberdey, 1931; Weber, 1954;
Davies, 1961). While the common oviduct has an ectodermal lining, the paired oviducts
THE GENITALIA 3
FIG. 2. Schematic representation of the types of internal female genitalia. (a) A primitive
type found in Ephemeroptera. (b) Orthopteroid type; the genital opening is on the 8th
segment, (c) Further development to a type found in Lepidoptera. Numbers 1, 2, 3 indicate
the positions of the original genital openings. Ac = accessory sex glands. Go = gonopore.
Rec = receptaculum seminis or sphermatheca. Vag = Vagina. (Modified from Weber, 1954.)
often are composed of mesodermal and ectodermal parts. Ovipositors, which are of great
taxonomic value, are formed by the eighth and ninth sternum and probably in the female
can be considered as abdominal appendages (Scudder, 1961a, b, 1964; Oeser, 1961; Davies,
1961).
A further modification of the female genitalia is found in the Lepidoptera. With the
exception of the Microlepidoptera, all species have two genital openings (Weidner, 1934;
Snodgrass, 1935). The posterior opening constitutes the actual gonopore, while the anterior
one (eighth segment) forms a bursa copulatrix (Figs. 2, 3). The two openings are apparently
homologous to the corresponding embryonic anlagen. As the schematic drawings show,
the bursa has a connection to the common oviduct via the ductus seminalis through which
the sperm migrate to reach the receptaculum seminis. All these organs are lined with a
cuticular intima since they are of ectodermal origin.
4 THE PHYSIOLOGY OF INSECT REPRODUCTION
Very little is known concerning the details of innervation of the female genitalia although
such details could supply interesting information regarding the segmental origin of the
various parts and would supplement embryological investigations. The studies on Apis
mellifera (Ruttner, 1961) and Leucophaea maderae (Engelmann, 1963) generally confirm the
conclusions of earlier studies with respect to the segmental origin of the genitalia. Nerves
of certain ganglia innervate the corresponding genital portions. There is one noted exception
in Leucophaea. The spermatheca in this species are innervated by branches of the seventh
abdominal nerve, thus suggesting that they originate from the seventh sternum. Embryo-
logical studies in other species, however, ascribe the spermatheca to the eighth segment.
The paragenital system of the Cimicoidea, which is a peculiarity among insects, ought to
be mentioned here since its functional significance has been under investigation. Males of
many species of the Cimicoidea do not deposit their sperm mass into the genitalia of the
female but rather penetrate a meso-ectodermal structureon the female's abdomen anddeposit
FIG. 3. Schematic representation of female genitalia of Lepidoptera with two genital
openings. Ac = accessory sex glands. Ac rec = accessory glands of spermatheca, D sem =
ductus seminalis which connects the bursa copulatrix with the vagina. Ov = common
oviduct.
the sperm there. This organ, known as organ of Berlese or Ribaga or simply called sperma
lege (Fig. 41), can be located on nearly any abdominal segment but its location is species
specific (Carayon, 1966). Spermatozoa migrate through the haemocoel to the conceptacula
seminis where they are stored. Some species possess a structural connection from the
spermalege to the conceptacula. This connection appears to be a solid core of tissue within
which the spermatozoa migrate. Phylogenetically this system may have evolved from an
accidental penetration of a females abdomen by the male aedeagus during copula (Carayon,
1966).
Lastly, we have to consider the structural differences of the ovaries found in the various
species. Each ovary consists of a number of ovarioles which may range from 1, as in the
Coprinae (Coleoptera)—which also have only one ovary (Heymons, 1929; Robertson,
1961)—2 as in Gte/Vza (Saunders, 1961), 360 as in Apis (Dreischer, 1956), and up to 1200 in the
army ant Eciton (Hagan, 1954a). Naturally, the number of ovarioles determines to some
extent the reproductive capacity of a species. On the basis of structural differences, two basic
types of ovarioles are distinguished: the panoistic and the meroistic (Snodgrass, 1935;
THE GENITALIA 5
Panoistic Ov. Meroistic Ov. Adenotrophic Ov.
FIG. 4. The four types of ovarioles found in species of insects. The adenotrophic type is only
found in Steraspis. Nutr = nutritive cord. Tr = trophic tissues. (Modified from Weber,
1954 and Martoja, 1964.)
Weber, 1954; Bonhag, 1958). The meriostic type can be further subdivided into polytrophic
and telotrophic (acrotrophic) ovarioles (Fig. 4). In the most primitive type, the panoistic
ovariole, the germarium contains only oogonia which as they migrate down the ovariole,
are surrounded by mesodermal cells, thus forming follicles. This type is found in the
Odonata, Ephemeroptera, Dictyoptera, Orthoptera, Plecoptera, Embioptera, Thysanoptera,
and Siphanoptera. Polytrophic ovarioles are distinguished from panoistic ones in that each
follicle contains a number of nurse cells together with one oocyte. Generally the nurse cells
and oocyte of a follicle are derived from one oogonium (p. 45). Polytrophic ovarioles
are observed in the Anoplura, Psocoptera, Dermaptera, Mecoptera, Trichoptera, Lepidop-
tera, Diptera, and Hymenoptera. There is some controversy as to whether the Mallophaga
have panoistic or polytrophic ovarioles (Ries, 1932; Seguy, 1951).
Telotrophic ovarioles are characterized by their terminal nutritive tissue and its connection
6 THE PHYSIOLOGY OF INSECT REPRODUCTION
with the oocytes via a nutritive cord (Fig. 4). The Homoptera and Heteroptera typically
possess ovarioles of this type. Among the Coleoptera, various authors ascribe either
polytrophic or telotrophic ovarioles to the same species. The difficulty in classification of
these cases may arise from the fact that the nutritive cord breaks down early in development
in some species; the ovariole may then appear as a polytrophic or panoistic type. Indeed,
panoistic ovarioles are reported in Melolontha vulgar is (Vogel, 1950) and in Tenebrio
molitor (Huet and Lender, 1962); yet, in the latter species, Schlottman and Bonhag (1956)
describe a telotrophic ovariole. Bonhag (1958) expresses doubt whether panoistic ovarioles
exist in any coleopteran and suggests a reinvestigation of each report.
In one species of Coleoptera, namely Steraspis speciosa, a new type has been identified
(Martoja, 1964). The germarium and vitellarium of this ovariole are unusually short (Fig. 4).
FIG. 5. Relationship of accessory sex glands to ovarioles. Glandular tissues are indicated
by solid black. 1. Dictyopteran type. 2. Acrida type with pseudoaccessory glands. 3. Locusta
type. 4. Steraspis type in which the lower portions of the ovarioles furnish secretory materials
used in egg covering. Ac = Accessory sex glands. Ov = Ovariole. (Adapted from Martoja,
1964.)
Proximal to the short vitellarium, the epithelium of a long glandular section of the ovariole
is thrown into folds which unfolds as an egg passes down. This unique glandular portion of
the ovariole appears to secrete a covering for the egg; the material is presumably similar to
that of accessory sex glands. A sphincter at the posterior end of the long ovariole closes it
off from the oviduct. No nutritive cord has yet been found; Martoja, nevertheless, believed
that one is dealing here with a modified telotrophic ovariole and proposed the term adeno-
trophic for this type. No other species is known to have a similar ovariole. A certain difficulty
is encountered with this new classification, however. The distinction among the other three
types is based on the location of the nutritive tissues in relation to the growing oocytes. In
this new type, the oocytes apparently do not receive nutrients from the glandular portions
of the ovariole. From this viewpoint, the terminology is debatable.
On the basis of the anatomical relationship between the accessory sex glands, which furnish
the material for the oothecae or egg covering, and the ovarioles, Martoja (1964) distinguished
THE GENITALIA 7
four different types (Fig. 5). In the dictyopteran type, which is the most widely distributed
among insects, the accessory glands are clearly associated with the common oviduct or
vagina. In the next type, which is found in many Acrididae, the anterior portion of the
lateral oviduct bears the accessory sex gland. In Locusta (type 3), the entire lateral oviduct is
secretory (Lauverjat, 1964), the material of which is used in forming the plug for the egg pod.
In both of these latter types no accessory sex glands are associated with the common oviduct.
In type 4, which is found in Steraspis, materials from both the lateral oviducts and the
proximal portions of the ovarioles enwrap the eggs as they are laid. The secretory portion
of the ovarioles may be analogous to the secretory oviducts of Locusta, yet anatomically
it is part of the ovariole.