Juvenile hormone III skipped bisepoxide is widespread in true bugs (Hemiptera: Heteroptera)

Abstract

Juvenile hormone (JH) plays important roles in almost every aspect of insect development and reproduction. JHs are a group of acyclic sesquiterpenoids, and their farnesol backbone has been chemically modified to generate a homologous series of hormones in some insect lineages. JH III (methyl farnesoate, 10,11-epoxide) is the most common JH in insects, but Lepidoptera (butterflies and moths) and 'higher' Diptera (suborder: Brachycera; flies) have developed their own unique JHs. Although JH was first proposed in the hemipteran suborder Heteroptera (true bugs), the chemical identity of the heteropteran JH was only recently determined. Furthermore, recent studies revealed the presence of a novel JH, JH III skipped bisepoxide (JHSB₃), in some heteropterans, but its taxonomic distribution remains largely unknown. In the present study, we investigated JHSB₃ production in 31 heteropteran species, covering almost all heteropteran lineages, through ultra-performance liquid chromatography coupled with tandem mass spectrometry. We found that all of the focal species produced JHSB₃, indicating that JHSB₃ is widespread in heteropteran bugs and the evolutionary occurrence of JHSB₃ ascends to the common ancestor of Heteroptera.

Keywords: Hemiptera; Heteroptera; juvenile hormone; juvenile hormone III skipped bisepoxide; true bugs; ultra-performance liquid chromatography coupled with tandem mass spectrometry.

Figure 1.

Structures of various JHs.

Figure 2.

Species tested in the present study mapped on the hemipteran phylogenetic tree inferred from a previous mitogenomic analysis [26]. An outgroup included Psocidae, Lepidopsocidae, Ectobiidae, Rhinotermitidae and Mantidae. Photographs of some species tested in the present study are also shown. The common ancestors of Hemiptera and Heteroptera are marked by closed circles.

Figure 3.

Chiral ultra-performance liquid chromatography coupled with tandem mass spectrometry of the corpus allatum products from various heteropteran species. The vertical axis indicates the signal intensity of the product ion at m/z 233.2 produced from the precursor ion at m/z 283.2. Panels (a–l) are the results of each analytical session. The retention time of authentic JHSB₃ was clarified before each session. (g) and (k) contain a noise peak in the JHSB₃ standard (#). Small peaks corresponding to 10S-JHSB₃ were detected in Plautia stali, Riptortus pedestris, Dolycoris baccarum, Geocoris jucundus and Cletus punctiger indicated by asterisks (*). Full species names can be found in figure 2 and electronic supplementary material table S1.