Juvenile hormone inhibits differentiation of olfactory sense organs during postembryonic development of cockroaches

Sexual dimorphism of antennal sense organs appears only at the adult stage during normal development of the cockroach, Periplaneta arnericana. Adult males acquire approximately twice as many olfactory sensilla as females at the terminal ecdysis. When terminal instar larvae are subjected to unilateral antennectomy, most ecdyse to supernumerary larvae rather than adults. Sexual dimorphism is not evident in the intact (unamputated) antenna during the extra larval stage, but appears at the following ecdysis which leads to the adult stage. Allatectomy of male and female larvae in the penultimate instar produces adultoids which show antennal sexual dimorphism. Whole-body treatment of terminal instar larvae with exogenous juvenile hormone-mimic (JH-M) results in supernumerary larvae which lack antennal sexual dimorphism. When these superlarvae are removed from the influence of JH-M, they ecdyse to adults with antennal sexual dimorphism. Topical application of JH-M to male antennae early in the terminal larval instar results in the emergence of adults which lack the total male complement of antennal sensilla, but are otherwise normal-appearing. These results indicate that an inhibitory action of juvenile hormone prevents the appearance of antennal sexual dimorphism during normal larval development.The postembryonic development of antennal olfactory receptors in cockroaches is regulated, in part, by the juvenile hormone (JH) (Schafer and Sanchez, '74). In the African woodroach, Leucophaea maderue, the density of antennal olfactory sensilla remains constant at about 400 sensilla per mm2 during each stage of larval development, because olfactory sensilla are added at each ecdysis in direct proportion to the increase in antennal surface area. However, at the terminal ecdysis leading to the adult stage, the density of olfactory receptor organs increases to 620 sensilla per mm2 in both males and females. Exogenously applied juvenile hormonemimic (JH-M) prevents this increase; or, the increase can be induced precociously by removing the corpora allata, endocrine organs which produce juvenile hormone in larval insects (Schafer and Sanchez, '74).J. EXP. UXIL., 198: 323-336.We chose to perform similar experiments on the American cockroach, Periplaneta americana, since the antennae show distinct sexual dimorphism related to the pheromone-dependent sexual behavior of males of this species. For example, the initial step in courtship behavior of P. americam is the male's reception of a femaleproduced sex attractant (Roth and Willis, '52; Barth, '70; Simon, '71). Of particular interest was the possibility that the differentiation of sex attractant receptors is inhibited by juvenile hormone during larval development. There are approximately twice as many olfactory sensilla on adult male P. americana antennae as on adult female antennae (Schafer and Sanchez, '73). In contrast, no sexual dimorphism is seen in the antennae of Leucophaea at any

The nature and development of sex attractant specificity in cockroaches of the genus Periplaneta. II. Juvenile hormone regulates sexual dimorphism in the distribution of antennal olfactory receptors

Schafer¹,

Sanchez²

1976

The nature and development of sex attractant specificity in cockroaches of the genus Periplaneta. III. Normal intra‐ and interspecific behavioral responses and responses of insects with juvenile hormone‐altered antennae

Schafer

1977

Male cockroaches of the species Periplaneta americana rely on a female-produced airborne pheromone to initiate courting behavior, The male responds to the presence of the pheromone with rapid, oriented locomotion. Contact with the female (or other males or larvae) elicits wing-raising and other responses characteristic of male courtship behavior. Males of other species within the genus Periplaneta also respond to a female-produced pheromone, but with less intensity than P. americana. Cross-species testing shows that P. brunnea males respond to the Periplaneta pheromone with the same intensity elicited by the P. brunnea pheromone. A second reaction group containing P. australasiae, P. fuliginosa, and P. japonica also responds to the P. americana pheromone and their conspecific pheromones, but with a low intensity characteristic of these species. Alteration of the antennal morphology of P. americana males can be experimentally induced by manipulating the level of juvenile hormone during development. Males with a full adult complement of olfactory receptors all respond behaviorally to the pheromone. Adult males with larval antennae produced by bilateral treatment with exogenous juvenile hormone-mimic do not respond to the pheromone, although they are completely adult in other respects.Cockroaches employ pheromones or sex attractants to initiate courtship behavior (Roth and Barth, '67). The mating behavior of species within the genus Periplaneta, especially that of the American cockroach, Periplaneta americana, has been described in detail by several workers (Roth and Willis, '52; Wharton et al., '54a;b; Barth, '61, '70; Roth and Barth, '67; Frazier, '70; Simon, '71). In general, these studies indicate that in the genus Periplaneta the initial step in male mating behavior is olfactory reception of a female-produced sex attractant.Mating behavior in cockroaches is also under endocrine control. The production of sex attractant by adult females in some species is under the control of the corpora allata, endocrine glands associated with the cerebral ganglia (Barth, '65, '68). In P. americana sex attractant is produced in large quantities by virgin females one to two weeks after the adult ecdysis ( m a rton and Wharton, '57; Bodenstein, '70). Pheromone production stops during pregnancy and generally declines with age (Barth, '68). The midgut is the most likely site of pheromone production in P. americana (Bodenstein, '701, which makes female feces a good source of sex attractant for experimental studies (cf. Raisbeck, '75) * Sex attractant reception in males is accomplished by antennae which have a large number of olfactory sense organs (Roth and Barth, '67). As 73

The nature and development of sex attractant specificity in cockroaches of the genus periplaneta. IV. Electrophysiological study of attractant specificity and its determination by juvenile hormone

Schafer

1977

The antennae of male Periplaneta americana acquire a large number of olfactory receptors at the adult stage. Electrophysiological methods (single unit and electroantennogram recording) show that a portion of the receptors added at the adult ecdysis are sex attractant receptors. Sex attractant receptors are not present in large numbers on larval and adult female antennae. The differentiation of pheromone receptors is inhibited during normal larval development by juvenile hormone. Topical application of juvenile hormone-mimic to male antennae during the terminal larval instar inhibits their development. Comparative electrophysiological studies indicate a high degree of cross-reactivity of the P. americana sex attractant among four other species within the genus Periplaneta.