Neural and Endocrine Control of Pheromone Production and Release in Cockroaches

Abstract

Integration of physiological and behavioral events is required to produce and emit sex pheromones in coordination with other reproductive events. Thus, insects usually produce and emit sex pheromones, and exhibit specific behaviors associated with sexual receptivity, only when they are reproductively competent. While the production of pheromones is regulated biochemically or developmentally, emission of pheromones, particularly of volatile attractants, can also be regulated behaviorally, involving specific central nervous (CNS)-generated motor patterns. Insects thus employ a variety of mechanisms in the production and emission of sex pheromones:

• · Pheromone production in some insects depends upon availability of biosynthetic precursors from host plants. Some danaid butterflies and arctiid moths modify plant pyrrolizidine alkaloids into volatile derivatives that are used as male pheromones (e.g., Schneider et al. 1975). It has become accepted that bark beetles detoxify tree monoterpenes through allylic oxidation into corresponding alcohols, which are then used as pheromones (review: Vanderwel 1994). However, recent data have demonstrated that Ips paraconfusus and I. pini synthesize the monoterpene mercene and the hydroxylated pheromone products ipsenol and ipsdienol (I. pini synthesizes only ipsdienol) from labeled acetate injected into the insects (Seybold et al. unpublished results). This raises the question of the relative importance of the de novo pathway versus the use of plant derived precursors to form the hydroxylated pheromone components in this group of insects.

• · Neural mechanisms are involved in regulating both production and emission of pheromone in the gypsy moth, Lymantria dispar; neural messages from the anterior portion of the CNS descend to the terminal abdominal ganglion (TAG) through the ventral nerve cord (VNC) (Tang et al. 1987). In this, as well as in other insects, neural signals originating from the abdomen of mated females ascend the VNC and inactivate sex pheromone production and/or release (e.g., Foster and Roelofs 1994).

• · The bulk of recent work on regulation of pheromone production in insects, as well as emphasis in the present volume, is on humoral pheromonotropins, particularly the pheromone biosynthesis activating neuropeptides (PBAN) and related myotropic peptides with homologous carboxyl-terminal amino acids (reviews: Raina 1993; Nagasawa et al. 1994). In some insects, PBAN may stimulate release of other factors, such as a bursa copulatrix factor in the redbanded leafroller moth, Argyrotaenia velutinana,which in turn stimulates pheromone production (Jurenka and Roelofs 1993).

• · Work with the housefly, Musca domestica, has shown that ecdysteroids, produced by the vitellogenic ovary, stimulate synthesis of the sex pheromone Z-9-tricosene (review: Blomquist et al. 1993). On the other hand, evidence from the moth Heliothis virescens suggests the involvement of 20-hydroxyecdysone in suppression of pheromone production after mating (Ramaswamy and Cohen 1992).

• · Juvenile hormone (JH), a product of the corpora allata (CA), was shown to induce pheromone production and release in several coleopterans, cockroaches, and some lepidopterans (reviews: Cusson et al. 1994a; Schal and Smith 1990; Vanderwel 1994). In some insects, however, indirect evidence suggests that JH may also exert pheromonostatic effects (Webster and Cardé 1984). Although evidence for a direct action of JH on the site of pheromone production is lacking in the majority of cases, recent evidence from the boll weevil suggests that JH III enhances the production of sex pheromone by isolated male fat body in vitro (Wiygul et al. 1990).

• · Developmental regulation of pheromone-producing glands occurs in all insects in which a sex-specific gland appears in the adult. In some lepidopterans, functional competency of the gland may be regulated by changing ecdysteroid titers during organogenesis (e.g., Tang et al. 1991). In cockroaches, cyclic maturational changes in the gland coincide with the ovarian cycle (Liang and Schal 1993c).

• · Multiple mechanisms probably occur in most insects. In cockroaches and lepidopterans that respond to JH, it is likely that peptides are released in response to elevated titers of JH. For example, while either JH or PBAN can stimulate sex pheromone production in allatectomizedAgrotis ipsilon (black cutworm moth), JH alone fails to induce pheromone production in decapitated females; it is therefore suggested that JH induces release of pheromonotropic factors from the CNS (Picombon et al. 1995). Also, neural inactivation of pheromone production in many lepidopterans conceivably operates through suppression of pheromonotropic peptide release.