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Classification of Hymenoptera by the Female's Reproduction
Variability in Ovisorption Process among Hymenoptera
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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).
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?
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