Abstract
Holometaboly is a key evolutionary innovation that has facilitated the spectacular radiation of insects. Despite the undeniable advantage of complete metamorphosis, the female of some holometabolous species have lost the typical holometabolous development through neoteny. In Xenos vesparum Rossi (Strepsiptera: Stylopidae), a derived species of the holometabolous endoparasitic order Strepsiptera, neotenic females reach sexual maturity without the pupal and the imaginal stages, thus retaining their larval morphology (with the exception of the anterior part of the body or cephalothorax), while males undergo normal pupal-based metamorphosis. Expression of the “adult-specifier” E93 factor has been shown to be required for proper metamorphosis in holometabolous insects. Here, we investigated the involvement of E93 in female neoteny by cloning XvE93. Interestingly, while we detected a clear up-regulation of XvE93 expression in pupal and adult stages of males, persistent low levels of XvE93 were detected in X. vesparum females. However, a specific up-regulation of XvE93 was observed in the cephalothorax of late 4th female instar larva, which correlates with the occurrence of neotenic-specific features in the anterior part of the female body. Moreover, the same expression dynamic in the cephalothorax and abdomen was also observed for other two critical metamorphic regulators, the anti-metamorphic XvKr-h1 and the pupal specifier XvBr-C. The specific up-regulation of XvE93 and XvBr-C in the female cephalothorax seems to be the result of an increase in 20-hydroxyecdysone (20E) signaling in this region for we detected higher expression levels of the 20E-dependent nuclear receptors XvHR3 and XvE75 in the cephalothorax. Overall, our results detect a sex-specific expression pattern of critical metamorphic genes in X. vesparum, suggesting that neoteny in Strepsiptera results from the modification of the normal expression of E93, Br-C and Kr-h1 genes.
Highlights
From their origin approximately 400 Mya[1,2], insects have developed three basic types of metamorphic development: (i) ametaboly (Apterygota), the most primitive type that is characterized by the absence of a morphological transformation between the wingless immature individuals and the adults; (ii) hemimetaboly (Exopterygota), in which the juvenile wingless nymphs resemble miniature adults and metamorphose into winged adults during the last juvenile instar; and (iii) holometaboly (Endopterygota), in which the crawling juvenile larvae undergo a dramatic morphological transformation to form the winged adult through a two-stage metamorphic process bridged by the holometabolous-specific intermediate pupal stage[3,4]
In order to characterize the genetic control of neoteny in holometabolous insects, a recent pilot study proposed that the appearance of neotenic females in Strepsiptera is linked to the modification of regulatory pathways that underlie pupal determination[36]
RHF-1 presents 91–98% similarity compared to other insects and a 67% compared to the Caenorhabditis elegans homolog MBR-1, while RHF-2 presents 93–100% similarity compared to other insects, 71% compared to MBR-1 and 53% compared to the human homolog Ligand Co-Repressor (LCoR)
Summary
From their origin approximately 400 Mya[1,2], insects have developed three basic types of metamorphic development: (i) ametaboly (Apterygota), the most primitive type that is characterized by the absence of a morphological transformation between the wingless immature individuals and the adults; (ii) hemimetaboly (Exopterygota), in which the juvenile wingless nymphs resemble miniature adults and metamorphose into winged adults during the last juvenile instar; and (iii) holometaboly (Endopterygota), in which the crawling juvenile larvae undergo a dramatic morphological transformation to form the winged adult through a two-stage metamorphic process bridged by the holometabolous-specific intermediate pupal stage[3,4]. After three consecutive endoparasitic stages where no ecdysis occurs, the male larva extrudes the head (cephalotheca) through the host cuticle and continues the typical holometabolous development whereby it undergoes complete metamorphosis through pupation. Similar to the repressive activity on Br-C, Kr-h1 binds to the promoter region of E93, suppressing its expression before the pupal stage and preventing larvae to undergo precocious larval-adult metamorphosis[35]. Due to their critical importance in the control of metamorphosis in holometabolous and hemimetabolous insects, Kr-h1, Br-C and E93 form what we have recently defined as the Metamorphic Gene Network (MGN)[1]. It has been shown in T. castaneum that depletion of TcBr-C does not result in the maintenance of larval status but rather to a developmental arrest of the animal at the larval-pupal transition with knockdown animals showing a mix of larval, pupal and adult features[1,28,29,30,31], suggesting that additional factors are required to induce complete metamorphosis
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