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OOGENESIS--OVISORPTION
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Classification of Hymenoptera by the
Female's Reproductive
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Variability in Ovisorption Process among Hymenoptera |
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History Biological control workers are thought to have been the
first to consider the phenomenon of ovisorption as a nutrient storage
mechanism in insects. Weyer (1927) working with ants was presumably the first
to recognize ovisorption at all; and later Flanders (1935) related
ovisorption to the effectiveness of parasitoids in controlling their hosts.
Insect physiologists also noted the phenomenon almost simultaneously in other
orders of insects (Pfeiffer 1939; Wigglesworth 1936, 1948a, 1948b; Highnam et
al. 1963). General Characteristics When certain parasitic Hymenoptera which ovulate
yolk-replete eggs are withheld from their hosts, the processes of oogenesis
and ovisorption occur synchronously and enable the female to deposit
newly formed viable eggs after a period of inhibited oviposition (usually 3-4
days). Parasitoid species that show this particularly well are Brachymeria
euploeae Westwood, Peridesmia phytonomi Gahan, Pteromalus
puparum L., Encyrtus fuliginosus Compere, and Metaphycus
helvolus (Compere) and Nasonia vitripennis (Walker) (Flanders
1935, 1942b,e; Schneider 1941, Medler 1962, Hopkins & King 1964, 1966;
King & Richards 1968a, King & Ratcliffe 1969). Non-viable eggs in the process of disintegration may be
deposited, as well as viable, partially-collapsed eggs (Flanders 1942b,e),
whose deposition in the host appears to be indiscriminate (Gerling &
Legner 1968 ). Such deposition of partially absorbed viable eggs may
produce the diploid males in Bracon hebetor (Flanders 1943); or
embryonic starvation and thence deposition of defective eggs in the honeybee
(Flanders 1957, 1959b). They may be prerequisites to worker caste
determination in ants, bees and wasps (Flanders 1945b, 1952, 1956). They may
also change the normal sex ratio in Nasonia vitripennis (King
1962). Ovisorption occurs when conditions are unfavorable for the deposition
of any mature (ripe) eggs (Flanders 1942e, Edwards 1954b, LaBergrie 1959,
Phipps 1966). It may occur following parasitism as in Bombus terrestris
(Palm 1948). The processes of host-feeding, oviposition and
ovisorption are closely related and affect the fecundity, longevity and host
killing capacity of the parasitoid (Legner & Gerling 1967, Legner &
Thompson 1977). Physiology of
Ovigenesis-Ovisorption Classic work has been conducted on other orders by
physiologists (Wigglesworth 1936, 1948a,b; Ito 1942, Pfeiffer 1945),
emphasizing the role of the corpus allatum in
oogenesis and resorption. The neurosecretory cells
were recognized as a source of stimulation of the corpus allatum and the
ovaries (Wigglesworth 1936, 1948a,b). The role of the corpus cardiacum was also recognized
(Pfeiffer 1945). In Calliphora, allatectomy experiments showed effects
on ovary development and yolk deposition (Thomsen 1952). The medial
neurosecretory cells of the brain, when cauterized, have the same effect
(Thomsen 1952). Histological, biochemical and histochemical work on
Coleoptera (Schlottman & Bonhag 1956), on Orthoptera (Highnam 1962,
Highnam et al. 1963, Lusis 1963; Pfeiffer 1945), and studies on diapause of Leptinotarsa
decemlineata (de Wilde 1962, deWilde & de Boer 1961) suggested
that the nervous system controls the amount of protein in the haemolymph,
stimulating the corpora allata / ovary system for the deposition and
ovisorption of eggs. The protein uptake by the oocytes is controlled by the
corpus allatum (Strong 1965, Telfer 1965). Ovisorption is, therefore, an
integrated process in which the brain, corpora allata, corpus cardiaca, plus
physical and chemical environmental factors complement their actions. The
role played by the different parts of the system varies with the insect
species (Englemann 1968). Ovisorption was defined by deWilde (1964) as "the
capacity of the follicle cells to dissolve and absorb the oocyte."
Several factors can contribute to the production of this phenomenon in which
vitellogenesis is interrupted and the oocyte, wholly enveloped in its
follicle, may die. Follicle cells cease to participate in alimentary egg
formation; they may divide amitotically, and absorb the dead oocyte. Their
nuclei become pycnocytic, the cells breaking down and being absorbed through
the ovarian sheaths (King 1963, Richards & King 1967). Thomsen (1952) showed
that ovisorption is brought about by the integration of several
neurosecretory, physical and chemical factors. Doutt (1964) maintained that
from a biological control viewpoint, this physiological characteristic is a
very important one in parasitoids where effectiveness as natural enemies of
pests will depend in part on their conservation of reproductive material
which is correlated with a high host searching capacity. Vitellogenesis (Yolk
Formation) Bonhag (1958) reviewed the process of vitellogenesis,
followed by another review by Telfer (1965) in light of rapid developmental
progress in this aspect of insect physiology. In the process, apparently
blood proteins are transferred directly to the developing yolk in the
oocytes. There is a large number of different kinds of blood proteins
synthesized in insects, the site of any single one not being definite. In all
insect ovaries, the chain of follicles comprising an ovariole is continuously
surrounded by a cellular sheath (the ovariole wall) and a basement lamella,
the so-called tunica propria (Bonhag 1958,
Bier 1967, King & Ratcliffe 1968). During yolk formation the individual
oocyte is directly enveloped by a single layer of follicle cells whose outer surface
adheres to the inner side of the basement lamella. In some insects there is,
in addition, a vitelline membrane lying between the oocyte surface and the
follicle cells (King & DeVine 1958). All membranes are thought to be
permeable to blood proteins. Intercellular spaces form in the follicle cells
synchronous with the onset of blood protein penetration. There is also some
evidence that nurse cells atrophy before the onset of chorion formation and
much of their cytoplasm literally flows tho=rough the connectives into the
oocyte. Some portion of the nurse cells remains outside the chorion, however,
after its formation (see Telfer 1965). A role of the nurse cells in yolk
formation is indicated in some insects, but seems to be rather insignificant
in others (Telfer 1965). When the individual follicle has reached the stage
where yolk formation should commence, its further development in many insects
requires the presence of the corpus allatum (secreting a juvenile hormone).
Another hormone is produced later which activates the final stages of oocyte
formation (see Telfer 1965 for an extensive treatment of hormonal control of
yolk formation). In a number of insects which form eggs prior to the
emergence of the adults, the fat body in addition to the blood is one of the
primary storage sites of yolk precursors (Telfer 1965). Classification of
Parasitic Hymenoptera Using the
Female Reproductive System Parasitic Hymenoptera may be divided into two general
types: (1) proovigenic and (2) synovigenic. In proovigenic
species oogenesis is largely, if not entirely, completed prior to egg
deposition. Most of the eggs are laid shortly after eclosion from the pupa,
and the oviposition period is usually so short that relatively large numbers
of females are needed to search a given area effectively. The maintenance of
such a parasitoid population requires a relatively large population of hosts.
Synovigenic species, on the other hand, generally synchronize oogenesis with
egg-deposition. They possess a prolonged oviposition period, and they are
thought to be more effective in biological control because they are longer
lived and, consequently, can reproduce at lower densities of the host
population. Synovigenic species may be further divided into two
sub-groups: (1) where ovulation is internally induced and (2) where
ovulation is externally induced. In the group where ovulation is
internally induced there are additionally two types: (a) the Ophion-type where the oviducts are
almost as long as the ovary. This includes ectoparasitic species with uterine
incubation as well as some endoparasitoids. Most of the Ophion-type
species do not have oviducts modified for egg storage; (b) the Apanteles-type, which has oviducts that
are shorter than the ovary and are modified for egg storage. All of these
species are endoparasitic (e.g., Chelonus), with no ectoparasitoids
known. In the group of synovigenic species where ovulation is
externally induced, the oviducts are not adapted to storage of ovulated eggs.
One subgroup of this type is the Monootene-type,
where only one ripe egg at a time occurs in each ovariole (e.g., Signiphora).
A second sub-group, the Polyootene-type,
has several ripe eggs at a time in each ovariole (e.g., Nasonia, Spalangia).
In these species ovisorption sets in when the pressure of accumulated eggs
reaches a certain point (Schneider 1941). Polyootene-type species may deposit
partially absorbed eggs (e.g., Spalangia cameroni). Such eggs
may be laid in the absence of hosts, as shown in Phaeogenes nigridens
(Wesmael) (Smith 1932); or they may be laid on the hosts, as in Spalangia
cameroni (Gerling & Legner 1968 ). Hymenoptera may also be classified according to the amount
of yolk contained in the ripe eggs. Thus, we have yolk-deficient hydropic species and yolk-replete anhydropic species. It is necessary for
anhydropic eggs to be eliminated from the oviduct, for if not, in some
species the larvae will hatch and perforate the oviduct wall, killing the
parent female (Chewyreuv 1911, 1912). In some species with hydropic eggs,
ripe eggs may be stored in the enlarged oviducts pending conditions suitable
for oviposition (Flanders 1942). Because development is stimulated only by
substances present in the host, the hydropic eggs in the oviducts remain in a
quiescent condition during the life of the female. When hosts are lacking, a
portion of the eggs of hydropic species of Ascogaster is stored in the
oviduct. Then, ovulation ceases and ovisorption takes place in the ovarioles. Variability in
Ovisorption Process Among Hymenoptera In ectoparasitic species, ovisorption probably proceeds
with greater rapidity than oogenesis (Flanders 1942). Delayed ovulation may
result in the deposition of slightly absorbed eggs of low viability. A
decrease in oviposition rate may account for the observation by Whiting
(1940) that the percentage of non-hatching eggs deposited by Bracon hebetor
increases with the age of the ovipositing female. Whiting also pointed out
that in Bracon hebetor embryonic development occurs in almost
every nonhatching egg. Consequently, it seems probable that eggs which have
not regressed beyond a certain point may hatch, and the larvae by feeding
avidly on the host, may complete their development. In worker ants, the honeybee and certain wasps, the
resorption of developing eggs has been described by Weyer (1927). In some
parasitic Hymenoptera a temporary withdrawal of hosts will allow ovisorption
and oogenesis to occur synchronously, thus enabling a female after a period
of inhibited oviposition to deposit viable eggs as if no interruption had
occurred (Flanders 1942). If the absence of hosts is prolonged, such species
may maintain their reproductive capacity by complete ovisorption and
cessation of oogenesis, a state that Flanders (1935) considered phasic castration or imaginal
diapause. Withdrawal from hosts for even a limited period of time (3
days) does have a pronounced significant effect on the fecundity and
longevity of the female thereafter, however (Legner & Gerling 1967). This work
involved three genera of parasitic Hymenoptera and was conclusive beyond a
doubt. Nevertheless, Lloyd (1940) reported that the daily fecundity of the
ichneumonid Diadromus collaris was unaffected by periods of
inhibited oviposition; and Flanders (1942) maintained that in several
chalcidoids parasitic on black scale the substitution of ovisorption for
ovulation during periods of isolation apparently maintained the normal
oviposition curve. In certain pteromalids, ovisorption may be followed by a
long period of castration, five months or more at 26.7BC,
which begins and ends spontaneously (e.g., Dibrachoides). The fate of the chorion in ovisorption has sometimes been
questioned. In no species is it known that the chorions, or remnants of an
absorbed egg, are discharged either into the oviduct or through either the
ovipositor or the copulatory opening. The accumulation of egg remnants in the
ovarioles, which often occurs, seems not to interfere with ovulation. In the Encyrtidae, Flanders (1942) observed that the
remains of an aeroscopic plate indicated that
ovisorption has occurred. In one species, Encyrtus fuliginosus
Compere, the exochorion of each disintegrated eggs appeared to have been
extruded into the body cavity. In this species the longevity of ovipositing
adults is longer than that of adults that do not oviposit. Apparently,
internal organs such as the heart, auxiliary pumps, etc., become clogged
with chorions! Partial
ovisorption occurs in Spalangia cameroni after 10 days without
hosts (Gerling & Legner 1968 ). Such
partially-resorbed eggs were deposited. Complete resorption apparently occurs
only in individuals that were given an opportunity to oviposit and host feed
early in life. Ovisorption Rate.--In Signiphora only one mature egg and one
developing egg occur in any given ovariole, the rest of the structure being composed
of germarium (Quezada 1967). It was reasoned that this was logical since the
species had an extremely rapid rate of egg development and resorption (two
hours!). If Signiphora females were not provided with hosts for five
days, ovisorption was complete and the germarium was no longer capable of
generating more eggs. Two days are usually required for resorption and three
days for oogenesis in most species. In the honeybee, with an excess of 300
ovarioles, the process of ovisorption must be continuous since there are
usually never more than about 1000 eggs deposited each day. Each ovariole in
the honeybee contains several (4-6) ripe eggs at any given time. Evidence for
the tremendous amount of ovisorption in the honeybee is given by the yellow ring present in ovarioles of older queens. Effect of
Ovisorption on Longevity.--Ovisorption may enable a starved female to outlive a
male (King & Hopkins 1963). It may enable hymenopterous parasitoids with
anhydropic eggs to retain their reproductive potential during periods of
unfavorable environmental conditions, although fecundity is sometimes lowered
after ovisorption has occurred, and the sex ratio of the offspring may be
affected by partial resorption (King 1962: work with Nasonia vitripennis). Research on
Nasonia vitripennis.--In Hymenoptera, ovisorption usually occurs before the
formation of either the vitelline membrane or the chorion, but may be either
before or after yolk formation (King 1968a). However, Nasonia is
exceptional in that the oldest eggs with developed chorions are the first to
be resorbed (King 1968a). The egg membranes are removed by enzymes which are
apparently released from the follicle cells (enzymes = Leucine amino
peptidase and esterase) (Richards & King 1967). The earlier onset of ovisorption
in older individuals probably results from the reduction in reserve food
materials stored in the fat body so that under conditions of starvation the
protein in the haemolymph is depleted more rapidly in older starved
individuals (King 1968a). King also restated the fact that the speed of
ovisorption is not affected by the age of the individual (Edwards 1954, King
1963). Exercise 18.1--Discuss ways in which ovisorption might influence the
sex ratio of a parasitic species. Exercise 18.2--Distinguish synovigenic from proovigenic species. Exercise 18.3--Recognize the difference between Ophion-type and Apanteles-type
species. Exercise 18.4--How quick is the ovisorption process? Exercise 18.5--How does ovisorption affect the longevity of the organism? REFERENCES: [Additional references
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