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OOGENESIS--OVISORPTION
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Classification of Hymenoptera by the
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Variability in Ovisorption Process among
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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
may be found at MELVYL Library ] Bellows,
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K. 1967b. Origin and sites of synthesis of macromolecular reserve substances
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R. L. 1954a. The effect of diet on egg maturation and resorption in Mormoniella vitripennis (Hymenoptera,
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S. E. 1935. An apparent correlation between the feeding habits of certain
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