Box 54 Control of mating and oviposition in a blow fly

Number of prior matings by male Number of prior matings by male

Number of prior matings by male Number of prior matings by male

The sheep blow fly, Lucilia cuprina (Diptera: Calliphori-dae), costs the Australian sheep industry many millions of dollars annually through losses caused by myiases or "strikes". This pestiferous fly may have been introduced to Australia from Africa in the late 19th century. The reproductive behavior of L. cuprina has been studied in some detail because of its relevance to a control program for this pest. Ovarian development and reproductive behavior of the adult female are highly stereotyped and readily manipulated via precise feeding of protein. Most females are anautogenous, i.e. they require a protein meal in order to develop their eggs, and usually mate after feeding and before their oocytes have reached early vitellogenesis. After their first mating, females reject further mating attempts for several days. The "switch-off" is activated by a peptide produced in the accessory glands of the male and transferred to the female during mating. Mating also stimulates oviposition; virgin females rarely lay eggs, whereas mated females readily do so. The eggs of each fly are laid in a single mass of a few hundred (illustration at top right) and then a new ovarian cycle commences with another batch of synchronously developing oocytes. Females may lay one to four egg masses before remating.

Unreceptive females respond to male mating attempts by curling their abdomen under their body (illustration at top left), by kicking at the males (illustration at top centre), or by actively avoiding them. Receptivity gradually returns to previously mated females, in contrast to their gradually diminishing tendency to lay. If remated, such non-laying females resume laying. Neither the size of the female's sperm store nor the mechanical stimulation of copulation can explain these changes in female behavior. Experimentally, it has been demonstrated that the female mating refractory period and readiness to lay are related to the amount of male accessory gland substance deposited in the female's bursa copulatrix during copulation. If a male repeatedly mates during one day (a multiply-mated male), less gland material is transferred at each successive copulation. Thus, if one male is mated, during one day, to a succession of females, which are later tested at intervals for their receptivity and readiness to lay, then the proportion of females either unreceptive or laying is inversely related to the number of females with which the male had previously mated. The graph on the left shows the percentage of females unreceptive to further mating when tested 1 day (o) or 8 days (•) after having mated with multiply-mated males. The percentage unreceptive values are based on 1-29 tests of different females. The graph on the right shows the percentage of females that laid eggs during 6 h of access to oviposition substrate presented 1 day (o) or 8 days (•) after mating with multiply-mated males. The percentage laid values are based on tests of 1-15 females. These two plots represent data from different groups of 30 males; samples of female flies numbering less than five are represented by smaller symbols. (After Bartell et al. 1969; Barton Browne et al. 1990; Smith et al. 1990.)

Fig. 5.8 A copulating pair of stink or shield bugs of the genus Poecilometis (Hemiptera: Pentatomidae). Many heteropteran bugs engage in prolonged copulation, which prevents other males from inseminating the female until either she becomes non-receptive to further males or she lays the eggs fertilized by the "guarding" male.

Fig. 5.8 A copulating pair of stink or shield bugs of the genus Poecilometis (Hemiptera: Pentatomidae). Many heteropteran bugs engage in prolonged copulation, which prevents other males from inseminating the female until either she becomes non-receptive to further males or she lays the eggs fertilized by the "guarding" male.

(Fig. 5.10). Ovarian follicle cells produce the eggshell and the surface sculpturing of the chorion usually reflects the outline of these cells. Typically, the eggs are yolk-rich and thus large relative to the size of the adult

Fig. 5.9 Oviposition by a South African ladybird beetle, Chilomenes lunulata (Coleoptera: Coccinellidae). The eggs adhere to the leaf surface because of a sticky secretion applied to each egg. (After Blaney 1976.)

insect; egg cells range in length from 0.2 mm to about 13 mm. Embryonic development within the egg begins after egg activation (section 6.2.1).

The eggshell has a number of important functions. Its design allows selective entry of the sperm at the time of fertilization (section 5.6). Its elasticity facilitates oviposition, especially for species in which the eggs are compressed during passage down a narrow egg-laying tube, as described below. Its structure and composition afford the embryo protection from deleterious conditions such as unfavorable humidity and temperature, and microbial infection, while also allowing the exchange of oxygen and carbon dioxide between the inside and outside of the egg.

The differences seen in composition and complexity of layering of the eggshell in different insect groups generally are correlated with the environmental conditions encountered at the site of oviposition. In parasitic wasps the eggshell is usually thin and relatively homogeneous, allowing flexibility during passage down the narrow ovipositor, but, because the embryo develops within host tissues where desiccation is not a hazard, the wax layer of the eggshell is absent. In contrast, many insects lay their eggs in dry places and here the problem of avoiding water loss while obtaining oxygen is often acute because of the high surface area to volume ratio of most eggs. The majority of terrestrial eggs have a hydrofuge waxy chorion that contains a meshwork holding a layer of gas in contact with the outside atmosphere via narrow holes, or aeropyles.

The females of many insects (e.g. Zygentoma, many Odonata, Orthoptera, some Hemiptera, some Thysano-ptera, and Hymenoptera) have appendages of the eighth and ninth abdominal segments modified to

Box 5.5 Egg-tending fathers - the giant water bugs

Care of eggs by adult insects is common in those that show sociality (Chapter 12), but tending solely by male insects is very unusual. This behavior is known best in the giant water bugs, the Nepoidea, comprising the families Belostomatidae and Nepidae whose common names - giant water bugs, water scorpions, toe biters - reflect their size and behaviors. These are predators, amongst which the largest species specialize in vertebrate prey such as tadpoles and small fish, which they capture with raptorial forelegs and piercing mouthparts. Evolutionary attainment of the large adult body size necessary for feeding on these large items is inhibited by the fixed number of five nymphal instars in Heteroptera and the limited size increase at each molt (Dyar's rule; section 6.9.1). These phylogenetic (evolutionary inherited) constraints have been overcome in intriguing ways - by the commencement of develop ment at a large size via oviposition of large eggs, and in one family, with specialized paternal protection of the eggs.

Egg tending in the subfamily Belostomatinae involves the males "back-brooding" - carrying the eggs on their backs, in a behavior shared by over a hundred species in five genera. The male mates repeatedly with a female, perhaps up to a hundred times, thus guaranteeing that the eggs she deposits on his back are his alone, which encourages his subsequent tending behavior. Active male-tending behavior, called "brood-pumping", involves underwater undulating "press-ups" by the anchored male, creating water currents across the eggs. This is an identical, but slowed-down, form of the pumping display used in courtship. Males of other taxa "surface-brood", with the back (and thus eggs) held horizontally at the water surface such that the interstices of the eggs are wet and the apices aerial. This position, which is unique to brooding males, exposes the males to higher levels of predation. A third behavior, "brood-stroking", involves the submerged male sweeping and circulating water over the egg pad. Tending results in >95% successful emergence, in contrast to death of all eggs if removed from the male, whether aerial or submerged.

Members of the Lethocerinae, sister group to the Belostomatinae, show related behaviors that help us to understand the origins of aspects of these paternal egg defenses. Following courtship that involves display pumping as in Belostomatinae, the pair copulate frequently between bouts of laying in which eggs are placed on a stem or other projection above the surface of a pond or lake. After completion of egg-laying, the female leaves the male to attend the eggs and she swims away and plays no further role. The "emergent brooding" male tends the aerial eggs for the few days to a week until they hatch. His roles include periodically submerging himself to absorb and drink water that he regurgitates over the eggs, shielding the eggs, and display posturing against airborne threats. Unattended eggs die from desiccation; those immersed by rising water are abandoned and drown.

Insect eggs have a well-developed chorion that enables gas exchange between the external environment and the developing embryo (see section 5.8). The problem with a large egg relative to a smaller one is that the surface area increase of the sphere is much less than the increase in volume. Because oxygen is scarce in water and diffuses much more slowly than in air (section 10.3) the increased sized egg hits a limit of the ability for oxygen diffusion from water to egg. For such an egg in a terrestrial environment gas exchange is easy, but desiccation through loss of water becomes an issue. Although terrestrial insects use waxes around the chorion to avoid desiccation, the long aquatic history of the Nepoidea means that any such a mechanism has been lost and is unavailable, providing another example of phylogenetic inertia.

In the phylogeny of Nepoidea (shown opposite in reduced form from Smith 1997) a stepwise pattern of acquisition of paternal care can be seen. In the sister family to Belostomatidae, the Nepidae (the water-scorpions), all eggs, including the largest, develop immersed. Gas exchange is facilitated by expansion of the chorion surface area into either a crown or two long horns: the eggs never are brooded. No such chorionic elaboration evolved in Belostomatidae: the requirement by large eggs for oxygen with the need to avoid drowning or desiccation could have been fulfilled by oviposi-tion on a wave-swept rock - although this strategy is unknown in any extant taxa. Two alternatives devel oped - avoidance of submersion and drowning by egg-laying on emergent structures (Lethocerinae), or, perhaps in the absence of any other suitable substrate, egg-laying onto the back of the attendant mate (Belostomatinae). In Lethocerinae, watering behaviors of the males counter the desiccation problems encountered during emergent brooding of aerial eggs; in Belostomatinae, the pre-existing male courtship pumping behavior is a pre-adaptation for the oxygenating movements of the back-brooding male. Surface-brooding and brood-stroking are seen as more derived male-tending behaviors.

The traits of large eggs and male brooding behavior appeared together, and the traits of large eggs and egg respiratory horns also appeared together, because the first was impossible without the second. Thus, large body size in Nepoidea must have evolved twice. Paternal care and egg respiratory horns are different adaptations that facilitate gas exchange and thus survival of large eggs.

endochorion

Fig. 5.10 The generalized structure of a libelluloid dragonfly egg (Odonata: Corduliidae, Libellulidae). Libelluloid dragonflies oviposit into freshwater but always exophytically (i.e. outside of plant tissues). The endochorionic and exochorionic layers of the eggshell are separated by a distinct gap in some species. A gelatinous matrix may be present on the exochorion or as connecting strands between eggs. (After Trueman 1991.)

endochorion

Fig. 5.10 The generalized structure of a libelluloid dragonfly egg (Odonata: Corduliidae, Libellulidae). Libelluloid dragonflies oviposit into freshwater but always exophytically (i.e. outside of plant tissues). The endochorionic and exochorionic layers of the eggshell are separated by a distinct gap in some species. A gelatinous matrix may be present on the exochorion or as connecting strands between eggs. (After Trueman 1991.)

Fig. 5.12 Tip of the ovipositor of a female of the black field cricket, Teleogryllus commodus (Orthoptera: Gryllidae), split open to reveal the inside surface of the two halves of the ovipositor. Enlargements show: (a) posteriorly directed ovipositor scales; (b) distal group of sensilla. (After Austin & Browning 1981.)

Fig. 5.11 A female of the parasitic wasp Megarhyssa nortoni (Hymenoptera: Ichneumonidae) probing a pine log with her very long ovipositor in search of a larva of the sirex wood wasp, Sirex noctilio (Hymenoptera: Siricidae). If a larva is located, she stings and paralyses it before laying an egg on it.

form an egg-laying organ or ovipositor (section 2.5.1). In other insects (e.g. many Lepidoptera, Coleoptera, and Diptera) it is the posterior segments rather than appendages of the female's abdomen that function as an ovipositor (a "substitutional" ovipositor). Often these segments can be protracted into a telescopic tube in which the opening of the egg passage is close to the distal end. The ovipositor or the modified end of the abdomen enables the insect to insert its eggs into particular sites, such as into crevices, soil, plant tissues, or, in the case of many parasitic species, into an arthropod host. Other insects, such as Isoptera, Phthiraptera, and many Plecoptera, lack an egg-laying organ and eggs are deposited simply on a surface.

In certain Hymenoptera (some wasps, bees, and ants) the ovipositor has lost its egg-laying function and is used as a poison-injecting sting. The stinging Hymenoptera eject the eggs from the opening of the genital chamber at the base of the modified ovipositor. However, in most wasps the eggs pass down the canal of the ovipositor shaft, even if the shaft is very narrow (Fig. 5.11). In some parasitic wasps with very slender ovipositors the eggs are extremely compressed and stretched as they move through the narrow canal of the shaft.

Fig. 5.12 Tip of the ovipositor of a female of the black field cricket, Teleogryllus commodus (Orthoptera: Gryllidae), split open to reveal the inside surface of the two halves of the ovipositor. Enlargements show: (a) posteriorly directed ovipositor scales; (b) distal group of sensilla. (After Austin & Browning 1981.)

The valves of an insect ovipositor usually are held together by interlocking tongue-and-groove joints, which prevent lateral movement but allow the valves to slide back and forth on one another. Such movement, and sometimes also the presence of serrations on the tip of the ovipositor, is responsible for the piercing action of the ovipositor into an egg-laying site. Movement of eggs down the ovipositor tube is possible because of many posteriorly directed "scales" (micro-sculpturing) located on the inside surface of the valves. Ovipositor scales vary in shape (from plate-like to spinelike) and in arrangement among insect groups, and are seen best under the scanning electron microscope.

The scales found in the conspicuous ovipositors of crickets and katydids exemplify these variations (Orthoptera: Gryllidae and Tettigoniidae). The ovipositor of the field cricket Teleogryllus commodus (Fig. 5.12) possesses overlapping plate-like scales and scattered, short sensilla along the length of the egg canal. These sensilla may provide information on the position of the egg as it moves down the canal, whereas a group of larger sensilla at the apex of each dorsal valve presumably signals that the egg has been expelled. In addition, in T. commodus and some other insects, there are scales on the outer surface of the ovipositor tip, which are orientated in the opposite direction to those on the inner surface. These are thought to assist with penetration of the substrate and holding the ovipositor in position during egg-laying.

In addition to the eggshell, many eggs are provided with a proteinaceous secretion or cement which coats and fastens them to a substrate, such as a vertebrate hair in the case of sucking lice, or a plant surface in the case of many beetles (Fig. 5.9). Colleterial glands, accessory glands of the female reproductive tract, produce such secretions. In other insects, groups of thin-shelled eggs are enclosed in an ootheca, which protects the developing embryos from desiccation. The colleterial glands produce the tanned, purse-like ootheca of cockroaches (Box 9.8) and the frothy ootheca of mantids (see Plate 3.3, facing p. 14), whereas the foamy ootheca that surrounds locust and other orthopteran eggs in the soil is formed from the accessory glands in conjunction with other parts of the reproductive tract.

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