The evolution of male external genitalia made it possible for insects to transfer sperm directly from male to female during copulation. All but the most primitive insects were freed from reliance on indirect methods, such as the male depositing a spermatophore (sperm packet) for the female to pick up from the substrate, as in Collembola, Diplura, and apterygote insects. In pterygote insects, copulation (sometimes referred to as mating) involves the physical apposition of male and female genitalia, usually followed by insemination — the transfer of sperm via the insertion of part of the male’s aedeagus (edeagus), the penis, into the reproductive tract of the female. In males of many species the extrusion of the aedeagus during copulation is a two-stage process. The complete aedeagus is extended from the abdomen, then the intromittent organ is everted or extended to produce an expanded, often elongate structure (variably called the endophallus, flagellum, or vesica) capable of depositing semen deep within the female’s reproductive tract (Fig. 5.4). In many insects the male terminalia have specially modified claspers, which lock with specific parts of the female terminalia to maintain the connection of their genitalia during sperm transfer.
This mechanistic definition of copulation ignores the sensory stimulation that is a vital part of the copulatory act in insects, as it is in other animals. In over a third of all insect species surveyed, the male indulges in copulatory courtship — behavior that appears to stimulate the female during mating. The male may stroke, tap, or bite the body or legs of the female, wave antennae, produce sounds, or thrust or vibrate parts of his genitalia.
Sperm are received by the female insect in a copulatory pouch (genital chamber, vagina, or bursa copulatrix) or directly into a spermatheca or its duct (as in Oncopeltus; Fig. 5.4). A spermatophore is the means of sperm transfer in most orders of insects; only some Heteroptera, Coleoptera, Diptera, and Hymenoptera deposit unpackaged sperm. Sperm transfer requires lubrication, obtained from the seminal fluids, and, in insects that use a spermatophore, packaging of sperm.
Secretions of the male accessory glands serve both of these functions as well as sometimes facilitating the final maturation of sperm, supplying energy for sperm maintenance, regulating female physiology and, in a few species, providing nourishment to the female (Box 5.2). The male accessory secretions may elicit one or two major responses in the female — induction of oviposition (egg-laying) and/or repression of sexual receptivity — by entering the female hemolymph and acting on her nervous and/or endocrine system.
Mating commences with the pair facing in the same direction, then the male rotates his eighth abdominal segment (90°) and genital capsule (180°), erects the aedeagus and gains entry to the female’s genital chamber, before he swings around to face in the opposite direction. The bugs may copulate for several hours, during which they walk around with the female leading and the male walking backwards. (a) Lateral view of the terminal segments, showing the valves of the female’s ovipositor in the male genital chamber; (b) longitudinal section showing internal structures of the reproductive system, with the tip of the male’s aedeagus in the fem ale’s spermatheca. (After Bonhag & Wick 1953)