Oviposition behavior comprises one of the final steps in insect reproduction. It involves the deposition of the mature egg outside the body of the female and includes a series of behavioral and physiological events that begin with the movement of the egg through the oviduct and end with the placement of the egg on a substrate that will support the development of the larva. Specialized behaviors and structures on the female allow her to place the eggs within a protected environment during oviposition.
Insect eggs develop within the ovaries, the reproductive structures of the female that are composed of tapering units called ovarioles. The oocytes differentiate from stem cells at the tip of the ovariole, and as they begin their downward movement in the ovariole they are first completely surrounded by a monolayer of follicle cells (Fig. 1). These follicle cells are involved in the transport of substances from the hemolymph into the cytoplasm of the oocyte that are stored for later use during embryogenesis. Nurse cells may also be present to provide the oocyte with other maternal contributions, such as messenger
FIGURE 1 A cluster of three ovarioles that comprise the larger ovary. Each has a calyx that connects to the lateral oviduct. Stem cells give rise to oocytes within the germarium, and as the oocyte descends within the ovariole, it becomes enclosed by follicle cells and deposits yolk into its cytoplasm. Upon degeneration of the follicle cells, the egg is free to move into the lateral oviduct in the process of ovulation.
RNA and mitochondria. The nurse cells subsequently degenerate, and the bulk of the yolk proteins deposited in the oocyte cytoplasm must then cross the layer of follicle cells after their synthesis in the fat body. During a later stage of development, the follicle cells also synthesize the eggshell (or chorion), which provides protection and waterproofing once the egg has been laid. After deposition of the chorion, the follicle cells degenerate, leaving the chorion as the outermost egg layer. With the follicle cells no longer on the outside of the egg, the egg is free to move out of the ovariole and into the oviduct, under the impetus of contractions of muscles in the oviduct walls. This movement of the egg to the outside of the ovariole is termed ovulation. Ovulation of the egg must occur before oviposition can take place.
The muscular contractions of the ovariole and oviduct that propel the egg through the reproductive tract are coordinated by hormones called myotropins. Myotropins are secreted by neurosecretory cells in the brain once the central nervous system has received the physiological confirmation that mating has occurred and that the eggs are mature. For example, in the bloodsucking bug Rhodnius prolixus , ovulation is initiated by a myotropin that is released only after the spermatheca has been filled with enough sperm and male accessory gland substances to produce a factor that induces the maturing eggs to begin producing 20-hydroxyecdysone. In the tsetse fly, Glossina, ovulation is initiated when a mature egg is present in the ovariole and the female has mated, but the stimulus from mating is not released until the female has received prolonged mechanical stimuli associated with copulation in addition to substances from the male accessory glands. Even several short copulatory experiences that fail to transfer sperm can initiate ovu-lation if their total duration is as long as a single successful copulation.
As the egg passes through the median oviduct, it is fertilized by sperm already stored within the female’s capsulelike spermath-eca (Fig. 2). Sensory receptors within the oviduct are mechanically
FIGURE 2 The female reproductive system, consisting of the ovaries that contain the ovarioles. As the egg moves down the median oviduct, it is fertilized by sperm released from the spermatheca. The egg is oviposited when it is deposited outside the body.
stimulated by the distension the egg creates as it descends; motor neurons activate the muscular walls of the spermathecal duct that allow the sperm to exit the spermatheca.
In hymenopterans, where sex determination occurs by haplodip-loidy, the process of sperm release is controlled more directly by the female. Eggs that are fertilized develop into female workers, but those that are not fertilized develop into male drones. The workers ultimately control whether the queen fertilizes the egg; they determine the size of the cells for rearing the larvae into which the queen deposits the egg. Before the egg is laid, the queen evaluates each cell with sensory receptors on her ovipositor, opening her spermath-ecal duct only when placing an egg into the larger cell for female rearing.
The sperms enter the egg through the micropyle, a small channel built into the normally impermeable chorion. Some insect eggs have several of these micropyles. The oocyte has been arrested in met-aphase of the first meiotic division prior to fertilzation, but shortly after the sperm has penetrated the egg and oviposition has occured, the oocyte completes its meiosis. The meiotic division results in a hap-loid oocyte nucleus and three polar nuclei that inhabit the periplasm at the periphery of the egg. The oocyte nucleus, surrounded by an island of cytoplasm, then moves to the interior of the egg, where it meets the sperm that has already entered. Syngamy, the union of sperm and egg, occurs in the interior. In some insects whose eggs develop by parthenogenesis (i.e., without the fertilization by sperm), a haploid polar nucleus combines with the haploid oocyte nucleus to restore the diploid number without requiring fertilization by male gametes.
After ovulation and fertilization, the eggs are usually deposited outside the female’s body during oviposition. The eggs move down the common oviduct by peristaltic waves of muscle contractions and out of the body through the ovipositor. The movement of the egg downward through the oviducts is facilitated by backwardly directed scales inside the oviduct, which act like a ratchet mechanism, allowing the egg to move in only one direction, down toward the genital opening.
Modified dermal glands known as female accessory glands may also be present on the common oviduct. These glands produce cement that allows the deposited eggs to be glued together or attached to the substrate. In some insects that retain their eggs after the young hatch, such as the tsetse Glossina, the accessory glands produce a nutritive secretion that nourishes the larvae during their entire larval period. In cockroaches and mantids, the female accessory glands produce the hardened egg case, or ootheca.
The spermathecae are used for the storage of sperm in the inseminated female. Also ectodermal in origin, the spermatheca generally opens into the common oviduct and releases sperm as the fully formed egg passes by. The spermathecal duct may contain glycogen deposits that can serve as an energy source for the sperm as they pass through to the egg. Nearest its opening to the outside, the common oviduct may be modified into a genital chamber that can be used to incubate eggs internally. The bursa copulatrix is an additional pouch within the chamber that is present in some insects into which sperm may first be deposited after mating. The sperm leave the bursa and then move into the spermatheca, where they are permanently stored. The bursa may have a series of toothlike structures that disrupt the spermatophore, the vessel in which the sperm are contained in more primitive insects, and facilitate their release. It may also secrete chemical signals into the hemolymph when it is filled with sperm to signal to the female that mating has occurred.
The control of oviposition in the cockroach Spodromantis is a good example of how environmental and physiological information must be integrated for egg laying to occur. This insect normally lays its eggs at the beginning of the photophase. The brain integrates the information it receives about the photoperiod and the presence of mature oocytes, and triggers the release of an oviposition-stimulating hormone that activates the ovipositor, ovariole, and oviduct muscles. As the substrate is probed with the insect’s ovipositor, tactile sensations from sensilla are sent to the terminal abdominal ganglion, where further movements of the egg and secretions by the accessory glands are controlled.
In most species, ovulation and oviposition may be part of a continuum, but in others they may be separate events in which the eggs are retained for a variable period between ovulation and oviposition. Some species of ovoviviparous cockroaches retain within a brood sac eggs that have been ovulated, until the female finds a suitable place to lay them. The nymphs hatch inside the female. The viviparous tsetse that retain and nourish their larvae after they have hatched from the egg larviposit late instar larvae that pupate after they burrow into the soil.
Most insects lack specialized structures for the deposition of eggs, but in some species the terminal segments of the abdomen form a telescoping ovipositor that can be used to deposit eggs into crevices or even, when the tip is modified into sawlike blades, into hardened substrates such as wood. This ovipositor may be derived from the modified appendages just described or from the modified terminal abdominal segments themselves. Special muscles within the ovipositor allow it to engage in superextension, lengthening considerably to reach hidden sites into which the eggs can be placed. Both the tips of the abdomen and the ovipositor may contain sensory receptors that can provide the female with information about the nature of the oviposition substrate. Sensory cues that are evaluated by the receptors are important in locating an oviposition site and in initiating ovi-position once the site has been found.
Prior to depositing her eggs, the female must engage in behaviors that will bring her to an environment that is suitable for larval development. This is especially necessary for the eggs of holometabolous insects, since the larvae are very different from the adults. Being relatively immobile, the larvae depend on the adult to locate a site on which they can develop. For example, adult mosquitoes are terrestrial but their larvae must develop in water. Although the adults are generally attracted to stimuli from vertebrate hosts for blood, when they carry mature eggs they become more sensitive to the stimuli from potential oviposition sites. The presence of mature eggs appears to trigger a physiological switch that changes the behavior of the female, attracting her to oviposition sites suitable for her eggs. In the absence of mature eggs, the female is more attracted to a host for a blood meal that would support another batch of eggs.
Lepidopterans undergo a sequence of behaviors, including searching, orientation, encounter, landing, evaluation of the surface, and acceptance. Stimuli received during each phase are integrated by the central nervous system, which processes the sensory information from sensory receptors on the antennae, tarsi, and ovipositor. Visual cues such as plant color and shape are important during searching behavior. Volatile chemicals produced by the plant initiate the orientation and encounter behaviors that attract the female from a distance of several meters. Visual cues are once again important in landing behavior, with the involvement of chemical cues that act as attractants, arrestants, or repellents. Once on the host plant, the female evaluates the physical and chemical cues from the plant surface and often begins drumming her front legs on the leaf surface, perhaps to provide more chemical information about the plant to tarsal sensory receptors. By using the total sensory input to the central nervous system, the female is able to recognize the suitability of the substrate for her eggs before they are laid.
The torsalo, Dermatobia hominis, has an unusual way of finding an oviposition site. The gravid female captures another bloodsucking fly and glues her eggs to the underside of the carrier’s body. When the carrier seeks out a vertebrate host for a blood meal, the larva hatches and burrows through the skin of the host. The larva develops in the vertebrate host, exits prior to the pupal stage, and pupates in the soil.