EMBRYOLOGY / ONTOGENY / ANATOMY
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Prenatal Development in Hymenoptera Specifically
Common Egg Shapes in Parasitoids
[ Please refer also to Selected Reviews
Embryology concerns the origin and development of the definitive individual organism. Development here is characterized by cumulative progressiveness in which the significance of each component process and result is viewed against what precedes and what follows.
The embryo is a forming individual which at all stages of development is adequately provided as to its needs and environment. Most advances achieved at any period anticipate functions that appear later. Developmental stages, therefore, contrast with the recurring, non-progressive, physiological changes that are concerned solely with the maintenance of life.
Embryological development is often divided into two parts by the incident of birth or hatching: (1) the prenatal part and the post-natal part. Earlier work in embryology characteristically focused on prenatal development. Modern concepts consider post-natal development, although not usually as dynamic, of equal importance. The embryology of the individual and all subsequent developmental events is called ontogeny.
Early Stages of Ontogeny
Organization of the Ripe Egg.--The ripe egg possesses polarity or axiation in which there are two poles: the animal and vegetal, and a main axis connecting them. The animal pole is that end of the egg which was most active in physiological exchange during oogenesis.
The ripe egg is bilaterally symmetrical. Among the innumerable planes that could divide the egg into physiological halves, only one finally dominates. Such planes are not equivalent, however.
Eggs are not homogenous, there being a greater concentration of pure protoplasm at the animal pole. Reserve materials (yolk) favor the vegetal pole. The internal portion differs from the gelatinous surface in being semi fluid; and ligaturing the newly deposited egg so that one-third of the protoplasm is not used can reduce the size of the mature embryo.
Development of the Egg.--Ripe eggs undergo aging among some species, resorption in others, and a combination of both in others. In the Hymenoptera aged eggs may be deposited prior to resorption and develop either into male or female progeny depending on the kind of parthenogenesis. In some cases eggs may hatch within the mother, which kills her. The sate of meiosis at oviposition will vary.
Cleavage.--Cleavage is the subdivision of the one-celled egg into smaller building units called blastomeres. Such subdivisions are always mitotic. Each division results in a reduction in size of ensuing blastomeres. The total mass of living substance available at the start is not increased appreciably when cleavage is finished.
Among most arthropods, the ova are centrolecithal where the yolk is massed centrally and surrounded by a peripheral shell of cytoplasm. Cleavage occurs only in the peripheral region and is termed superficial. Some endoparasitic Hymenoptera and the Collembola that have little yolk (isolecithal) show total cleavage.
Gastrulation.--Gastrulation is the process through which the three germ layers are formed: the ectoderm, mesoderm and entoderm. The various germ layers produce the body organs and other specialized parts.
Segmentation.--is also characteristic among insects.
Prenatal Development in Hymenoptera Specifically
Egg orientation is similar among all Hymenoptera studied. It follows Hallez' law of orientation (Hallez 1886) within the polytrophic ovariole. The anterior pole is directed toward the head of the parent female. However, during oviposition, the posterior pole emerges first, which permits regulation of fertilization. The dorsal, ventral and lateral sides vary within the same individual. The embryo remains in the original cephalocaudal axis during the entire development, but just before eclosion it rotates 180B on the longitudinal axis.
The yolk components are called deutoplasm. Included are protein yolk bodies, lipid yolk bodies and glycogen particles. Some Chalcidoidea lack yolk altogether.
Cleavage usually begins one or two hours after the egg is laid. Some exceptions are cases where eggs even hatch inside the mother. The duration of cleavage varies, but generally it is finished after six to eight hours at room temperature (23BC).
Gastrulation occurs in diverse ways among the Hymenoptera, and differs in different species of the same family. The duration appears to range from seven to twelve hours.
Segmentation occurs early in development in some Hymenoptera, and later in other species. The duration is variable.
Embryonic envelopes: there are two membranes, the serosa and amnion, that usually envelop insect embryos. However, in the Hymenoptera, one or both may be rudimentary or entirely lacking. Embryonic envelopes function both in protection and nutrition, and usually occur well developed in species with little yolk. Eggs with little yolk are usually minute when deposited in the host. Then, probably by osmosis or active absorption of host fluid, they gradually become larger (Imms 1931, Simmonds 1947). Expanding eggs of this type have been called hydropic eggs (Flanders 1942a). Flanders (1942d) found in Coccophagus capensis Compere, that only the fertilized egg produced a trophic membrane.
Membranes are known by various names. Hagen (1964) stated that during eclosion when the trophamnion is broken and cells of the membrane float free in the host's haemolymph, these cells increase in size proportional to the growth of the larval parasite; they become greatly enlarged while retaining their trophic function because the larva feeds upon these cells (Jackson 1928, O. J. Smith 1952). Host nutrition influences the development of these cells and in turn influences the parasitoid larva. Some membranes persist, covering the larva. For example, the chorion may remain intact until after first larval ecdysis (Flanders 1964).
Formation of entoderm, mid-gut, stomodaeum, proctodaeum, gonads, head, abdominal and thoracic appendages, dorsal closure, mesoderm and ectoderm, is discussed by Bronskill (1959).
Hatching of the egg usually occurs when histogenesis is complete. Exceptions are cited by Ivanova-Kazas (1948-58). First-instar larvae of many endoparasitoids are precociously emerged embryos (protopod larvae) such as Platygaster (Imms 1931).
Eggs with embryos can be deposited when partially or completely incubated only through the copulatory pore. The larvae, upon hatching, commence to feed. Completely incubated eggs do not always hatch immediately and may overwinter in the completely incubated condition. Hatching in ectoparasitoids may require a relative humidity of over 90% and under 100% at the egg site (Gerling & Legner 1968 ). Specific host organs may serve as oviposition sites, and egg chorions may be variously coated to avoid encapsulation in the host (Flanders 1934).
Egg Size and Shape
Eggs can reveal important information about the taxonomic groups of the organism which develop them. A survey of eggs within the Insecta shows they are variable in terms of number and size and plastic in terms of shape (Hinton 1981). Nevertheless, these characteristics are typically stable at the species level and frequently constant at the family level. This constancy at one taxonomic level pitted against variability at another creates an interesting blend of features which can be informative in terms of classifying insects and understanding their biologies. Parasitic insect eggs express variation in terms of size and shape. This variability is in part a consequential artifact of the enormous number of taxa involved and in part generated by the biology and developmental requirements of the insect embryos contained in these eggs. The variability in size and shape partially reflects a compromise between needs of the developing embryo and problems associated with oviposition.
The primitive nomenclature and early literature associated with the shapes of parasitoid eggs was characterized by Clausen (1948), reviewed by Hagen (1964), and summarized here. That schema is briefly discussed here, but research on egg morphology of the Insect during the past 20 years has shown that shape of the egg alone is not diagnostic and unrelated taxa share identical shapes. With the application of scanning electron microscopy it is now apparent that chorion morphology, eggshell complexity and micropylar position, number and configuration are all equally important features which must be described, studied and understood. Collection of this kind of information is tedious, time consuming and expensive. Moreover, the number of taxa for which egg anatomy must be collected is very large if we are to obtain an accurate picture of parasitoid biology. Egg biology and morphology has obviously lagged considerably behind other pursuits involving parasitic insects.
Common Egg Shapes in Parasitoids
Most of the names for egg shapes used by Pantel (1910) for his study of the Tachinidae were subsequently adopted for other groups of insects. These are briefly reviewed:
Acuminate eggs are characteristically long, narrow and generally adapted for extrusion from the long ovipositor of parasitic Hymenoptera which attack insects that form galls or live in galleries and tunnels. This kind of egg has been described for some Ichneumonoidea and Chalcidoidea.
Encyrtiform eggs are unusual in that they change shape after oviposition. Inside the ovary they are typically shaped as two spheres connected by a stalk. After oviposition one bulb collapses and the egg appears stalked. All encyrtiform eggs are deposited internally with the collapsed sphere projecting from the stalk outside the body of the host. An aeroscopic plate, used for embryonic and larval respiration, usually is found on the stalk and sometimes projects onto the body of the gg. This type of egg is characteristic of the Encyrtidae, but more recently has been reported in the Tanaostigmatidae (LaSalle & LeBeck 1983). It has not been found in the Eupelmidae, a family considered close to the Encyrtidae.
The Hymenopteriform egg may be viewed as the hypothetical ancestral form or the generalized type. Its shape is typically sausage-like with rounded poles and whose body is several times longer than wode. This is the generalized egg form expressed by Hymenoptera and it is also found in some Diptera (Nemestrinidae, Bombyliidae, Cecidomyiidae).
A Macrotype egg was proposed by Pantel (1910) for large eggs with a thick, opaque dorsal surface and thin, flat and transparent ventral surface. Macrotype eggs are oblong in dorsal aspect and semicircular in lateral aspect. Surface features which may be present include a flange margin for the ventral surface, and spumaline for adhesion to the host. Macrotype eggs typically have an extensive chorionic respiratory system. Macrotype eggs are restricted to the Tachinidae and were subdivided into dehiscent and indehiscent forms.
The Membranous egg is variable in size but the chorion is thin, transparent and appears membraous. The surface reticulation pattern and pliancy provide an impression of membrane. This is an egg typically ejected from the female which contains a mature embryo which is ready to emerge. Eclosion occurs soon after oviposition. Eggs are often glued to the host and site specificity has been suggested. The distinction between macrotype and membranous eggs is sometimes lost. This egg shape is representative of Diptera (Tachinidae, Sarcophagidae).
Microtype eggs are typically minute, variable in shape, with dorsal and lateral surfaces thick and dark, ventral surface thin and membraneous. Embryonic development occurs in the uterus. This egg type must be consumed by the host if development is to proceed, but the stimulus for hatching is unknown. Microtype eggs are widely distributed among the Tachinidae.
The Pedicellate egg is an apparent variation of the stalked egg in which one end is modified to anchor the egg to the integument or seta of the host. Most pedicellate eggs are deposited externally on the host, but a few are internal and attached to the host via the ventral surface of the egg. The pedicel may originate from the stalk, from the body of the egg or from a modified micropylar structure. This form of egg is widely distributed among parasitic Hymenoptera, including Chalcidoidea, Ichneumonoidea and Diptera (Cecidomyiidae, Conopidae, Tachinidae).
Stalked eggs are elongate with a constricted stalk-like projection from the one or both of the poles of the body of the egg. The stalk is of variable length, sometimes corkscrew shaped, and often several times longer than the remainder of the egg. This type of egg is found in some Diptera (Pyrgotidae) and most of the major superfamilies of parasitic Hymenoptera, including the Chalcidoidea (most families), Chrysidoidea, Cynipoidea, Evaniioidea, Ichneumonoidea and Proctotrupoidea (most families).
Polyembryony in Entomophages
Polyembryony representes a form of asexual reproduction in which many embryos develop from repeated division of an egg or zygote. The phenomenon has been reported in several groups of insects, including the Coleoptera and Hymenoptera. Among the parasitic Hymenoptera, polyembryony is known in the Braconidae, Platygasteridae, Dryinidae and Encyrtidae. Cruz (1986b) described in detail the development of Copidosomopsis tanytnemus Caltagirone, and egg-larval parasitoid of the Mediterranean flour moth, Anagasta kuehniella (Zeller).
Because of its curiosity, polyembryony has been extensively studied. It was first described by Marchal (1898, 1904) and Martin (1914). Other examples are Daniel (1932), Doutt (1947, 1952), Imms (1931), Kornhauser (1919), Leiby (1922, 1929), Leiby & Hill (1923, 1924), Marchal (1898, 1904, 1906), Martin (1914), Paillot (1937), Parker (1931), Patterson (1915, 1917), Silvestri (1906, 1923, 1937).
The generation time in polyembryony varies from several weeks to almost a year. Embryo development begins just as in monoembryony. Polar nuclei, however, do not enter directly into the blastula stage, but produce an embryonic membrane called the trophamnion which surrounds the developing embryo-like area. The trophamnion extracts nutrients from the host haemolymph. The embryo then divides into small groups of cells called morulae enclosed by the trophamnion. The trophamnion then changes into a chain-like structure with the morulae arranged in a row or branching cluster. This finally breaks up and separate embryos are formed. The number of embryos from a haploid egg equals one-half that from a diploid egg. Examples are reported from Litomastix (Copidosoma) koehleri (Blanchard) (Doutt 1947, Flanders 1942).
Polyembryony has been considered a process which restores a nucleocytoplasmic balance which is upset by osmosis of the host cytoplasm through the chorion. Perhaps more interesting from the viewpoint of parasitoid bioloty is the examination of polymorphic larvae within C. Tanytnemus by Cruz (1981, 1986a). It was shown that precocious larvae represent a so-called "defender morph." The defender morph is characterized by a well developed head, mouthparts and high motility. This morph attacks and kills or injures the larvae of competing internal parasitoids.
The number of larval instars found in Hymenoptera is variable, but five seems to be most common. The Aphelinidae, however, possess three instars and the Encyrtidae are variable. The number of mandible sets are the best evidence for instars.
Larval dimorphism may occur within the same instar, and sexual dimorphism is often striking. The most distinctive parasitic stage in the life cycle is the primary or first-instar larva (protopod larva).
Various methods of locomotion are found from slug-like to jumping. The fastest locomotion is characteristic of those species which lay their eggs apart from the host (Clausen 1976).
Larvae are also variously protected, the greatest protection being in the form of spines, plates, etc., which are characteristic of the more exposed larvae. Strong mandibles are found in species that show aggressiveness between the larvae (Salt 1961). These care characteristically endophagous forms. Other species protect themselves by producing a cytolytic enzyme (Thompson & Parker 1930, O. J. Smith 1952, Salt 1961, Gerling & Legner 1968 ). [e.g., Lounsburgia on black scale ].
Larval Feeding.--Egg parasitoids and other endophagous species are thought to absorb much of their food through the cuticle. Observations on ectophagous parasitoids (Gerling & Legner 1968 ) show a peculiar type of lacerating-like feeding in which the mandibles are used only for rasping followed by an imbibing of oozing fluids from the host. Such feeding wounds heal rapidly, causing the parasitoid larva to move to other feeding sites. Different instars prefer to congregate on different body regions (Gerling & Legner 1968 ). Similar feeding marks are also found on synthetic parasitoid diets (S. N. Thompson, pers. comm.).
Larval Respiration.--First-instar larvae exhibit the greatest diversity in respiration (Clausen 1950). Endophagous larvae either respirate through the integument or obtain air from the outside of the host through tube-like mechanisms (a membranous cocoon attached to the host's tracheae). The final instar may possess a completely different spiracle arrangement and number (Hagen 1964), while early instars may lack spiracles altogether.
Larval Anatomy.--Several distinctive larval forms are found in parasitic insects:
Eruciform larvae are shaped like a caterpillar. Anatomically they are characterized by a well developed head capsule, thoracic legs and abdominal prolegs. The eruciform larva is seen in Lepidoptera and Symphyta. It represents the ancestral type for Hymenoptera larvae, and presumably the form from which other types evolved.
The Hymenopteriform larva represents the generalized larval form seen in apocritous Hymenoptera. Characteristically the body is spindle-shaped, without thoracic legs, featureless with pale to translucent integument and the head capsule is weakly developed of absent.
Caudate apocritous larvae have a specialized body characteristically segmented, with long flexible caudal appendages. The function of caudal appendages has not been established, but sometimes they are progressively reduced in later instars and lost in the last instar. The caudate form is displayed by some endoparasitic ichneumonid larvae.
The Vesiculate apocritous larva has the proctodaeum everted, and displays short caudal appendagtes with vesicles at the bases. It is found in some endoparasitic Braconidae and some Ichneuumonidae.
Mymariform apocritous larvae display a head and caudal end each bearing a conical process anterad. The abdomen of some species is segmented. The larval form is found in Mymaridae and Trichogrammatidae.
The Sacciform apocritous larva is ovoid, featureless and without segmentation. It is found in Dryinidae, Mymaridae and Trichogrammatidae.
The Polypodeiform (cf. vesiculate) apocritous larva is endoparasitic, segmented with paired, short flexible projections from thoracic and abdominal segments. It occurs in Cynipoidea and Proctotrupoidea.
Hypermetamorphosis is found in some endopterygote insects whose larvae change form, shape or substance during successive instars as a normal consequence of development. Examples are found in, but not restricted to, Coleoptera (Meloidae), Strepsiptera, Diptera (Acroceridae, Bombyliidae), Lepidoptera (Epipyropidae), and Hymenoptera (Eucharitidae, Perilampidae).
The Teleaform apocritous larva is hypermetamorphic (e.g., Scelionidae: Proctotrupoidea) and unsegmented, weakly cephalized with prominent protuberances or curved hooks at the cephalic extremity. The body is posteriorly prolonged into a caudal process which has one or more girdles or rings of setae around the abdomen.
Cyclopoid larvae are hypermetamorphic, endophagous Hymenoptera, (e.g., some Proctotrupoidea). It is characterized by a large swollen cephalothorax, very large sickle-like mandibles and a pair of bifurcate caudal processes. The larva resembles the nauplius larva of crustaceans.
Planidium is the hypermetamorphic, migratory, first-instar larva of some parasitic insects. Morphologically it is characterized by a legless condition and somewhat flattened body which often displays strongly sclerotized, imbricated integumental sclerites and spine-like locomotoray processes. The term most appropriately is restricted to Hymenoptera (Euchartiidae, Perilampidae and some Ichneumonidae) and Diptera (Tachinidae). It is incorrectly used interchangeably with Triungulin (Heraty & Darling 1984).
Eucoiliform larvae are found in apocritous Hymenoptera which are hypermetamorphic (e.g., Eucoilidae). The primary larval form displays three pairs of long thoracic appendages but lacks the cephalic process and girdle of setae of the teleaform larva. Subsequent instars display a polypodeiform larval form. It has also been found in Charipidae and Figitidae.
Prepupa.--This stage begins when the last larval instar ceases to feed, voids meconium and shows scarcely any external movement. Rapid changes take place throughout the body. Although this is often referred to as a resting stage, it is by no means a physiological resting time! The length of time that it takes prepupae to form differs within the same species or can occur simultaneously for eggs deposited in a 24-hr period (Gerling & Legner 1968 , Legner 1969). The linking of the mid- and hind guts begins when the last larval instar is fully-fed, and is completed at the prepupal stage. Prepupae usually remain for less than 24 hrs, and the meconium is shed either freely in pellets, or encased in a peritrophic sac (Gerling & Legner 1968 ). In some species the meconium is discharged only when adult (e.g., Trichogramma). Meconia may serve to identify the species (Flanders 1942b).
Pupa.--Most hymenopterous parasitoids that pupate in the relatively dry remains of the host do not spin cocoons; the fully-fed endophagous larvae while immersed in host fluids can, however, construct membranous cocoons. Similar cocoon-like structures are found between gregarious (polyembryonic) pupae [an exception is Diversinervus smithi]. The length of the pupal stage can be variable or remarkably equal among the progeny of one female/day (Legner 1969).
Rate of Development
The overall rate of parasitoid development is known to be affected by host density, and usually accelerates with a higher average density of the host (Legner 1969, Olton & Legner 1974).
Exit From the Host.--The progeny of one female/day may either all exit the host immediately after eclosion from the pupa, or they may remain inside for variable lengths of time depending on when the adult bites through the encasing host (Legner 1969).
Male Reproductive System
Intensive work has been done on Spalangia cameroni Perkins (Gerling & Legner 1968 ). The male internal reproductive system in this species matures during the last few days of pupal life. One day before emergence the testes are already filled with fully developed sperm arranged in bundles within the sperm tubes. Numerous large cells are present in the testes in addition to these sperm bundles, which are more apparent at the anterior end of the testes. The testes become depleted of sperm during the last day of the pupal stage. The testes of emerging males, although depleted, still retain more or less the external appearance of those of unemerged males. However, a few days later they assume the shape of long thin tubes. Unidentified cells and sperm residues are present in these old testes, and its seems that no sperm producing function is carried out by them during the adult male's life.
The seminal vesicle is composed of two chambers; an anterior globular cavity and a posterior elongated one. The anterior part is mostly thin walled with two slightly thickened valvelike areas on its walls. The walls of the anterior portion undulate continuously from the final pupal period until males die. Sperm enter the vesicle about 1/2 day before emergence where they are maintained in a helix-like formation. The constantly undulating vesicle walls massage the sperm, seemingly to keep them alive, but some independent movement is characteristic (Gerling & Legner 1968 ).
Exercise 17.1--Define embryology and distinguish it from ontogeny.
Exercise 17.2--What are the characteristics of the early stages of ontogeny? Discuss post natal development in Hymenoptera.
Exercise 17.3--What is polyembryony?
Exercise 17.4--Discuss prenatal development in Hymenoptera.
Exercise 17.5--How does the function of the testes in Spalangia cameroni differ from other known examples? Describe the morphology and function of the seminal vesicle.
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