Ecdysteroids: the overlooked sex steroids of insects? Males: the black box

Abstract

The paradigm, still around in textbooks, that ‘in insects sex is strictly genetic, thus that they do not have sex hormones’, is mainly based on a wrong interpretation of the ‘gynandromorph argument’. It is no longer tenable. Given the fact that vertebrates and invertebrates probably had a common, sexually reproducing ancestor, there is no reason to assume that only vertebrates need sex hormones. The major function of sex hormones is to inform the somatoplasm about developmental changes that take place in the gonads. In contrast to juvenile hormone and neuropeptides, ecdysteroids meet all criteria to act as sex hormones, which was probably their ancient role. Their much better documented role in moulting and metamorphosis was a secondary acquisition that enabled arthropods to cope with growth problems, imposed by a rigid cuticle. Female insects use 20‐hydroxyecdysone (20E), secreted by the follicle cells of the ovary, in a similar way as females of egg‐laying vertebrates use estrogens. For a variety of reasons, the possibility that ecdysteroids, in particular ecdysone (E), might also act as sex hormones in male insects, thus as the counterpart of testosterone of vertebrates, has been very much overlooked. Thanks to the recent discovery of the molecular basis of the haploid‐diploid system of sex determination in the honeybee, the characterization of Halloween genes, proteomics, RNAi and so on, it now becomes possible to verify whether in insects, as with vertebrates, males are the endocrinologically default gender form.

Anopheles gambiaemales produce and transfer the vitellogenic steroid hormone 20-hydroxyecdysone to females during mating

“…Indeed, in several dipteran species including Drosophila, no ecdysteroids have been evidenced in males (20,35). In the few other insect species that were assessed for 20E production during male adulthood, steroid titers were much lower than in adult females and no prominent compound was identified (19). Whether the situation reported here for A. gambiae could be extended to other mosquito species has yet to be demonstrated.…”

“…However, only small amounts of steroids were released in vitro when compared with the amounts produced by ovaries, and no prominent compound has been identified. The demonstration of a significant production of one major hormonal steroid is still lacking in male insects, and this has led to the current dogma that they do not have sex steroids (18)(19)(20).…”

Sex Steroids in Insects and the Role of the Endosymbiont Wolbachia:A New Perspective

“…The 20E has also been shown to affect sexual behaviour, having a role in courtship initiation by males, and promoting male-male sexual attraction (Ganter et al, 2007). De Loof (2006Loof ( , 2008 suggests that ecdysteroids already served as sex hormones long before they acquired a function in moulting. In particular, 20E secreted by the follicle cells of the insect ovary could be the physiological equivalent of vertebrate estrogens, while E -the precursor of the active moulting hormone 20E -should act as a distinct hormone, being the physiological equivalent of the vertebrate testosterone (De Loof & Huybrechts, 1998;De Loof, 2006).…”

“…De Loof (2006) proposes that ecdysteroids are the best candidates for a role as sex steroids in insects since, for example, they are involved in the appearance of sex dimorphic structures; are produced by the gonads; and induce different gender-specific physiological effects. Indeed the role of ecdysteroids is not restricted to moulting but they have a much wider effect on the insect biology, both at the larval and adult stages.…”

“…sex hormones) is conceivable. In his fine review, De Loof (2006) suggests that the loss of an X chromosome in Drosophila embryonic cells possibly makes the mutant cells react differently to a given hormonal environment and/or signals from their neighbours than XX cells. Finally, it is noteworthy to note that, in addition to gynandromorphs, intersexes specimens do exist in insects.…”