Parallel alterations in the timing of ovarian Ecdysone Receptor and Ultraspiracle expression characterize the independent evolution of larval reproduction in two species of gall midges (Diptera: Cecidomyiidae)

Abstract

Although most insects reproduce in the adult stage, facultative larval or pupal reproduction (paedogenesis) has evolved at least six times independently in insects, twice in gall midges of the family Cecidomyiidae (Diptera). Paedogenesis in gall midges involves the precocious growth and differentiation of the ovary in an otherwise larval form. We have previously shown that the timing of expression of the Ecdysone Receptor (EcR) and Ultraspiracle (USP), the two proteins that constitute the functional receptor for the steroid hormone 20-hydroxyecdysone, regulates the timing and progression of ovarian differentiation in Drosophila melanogaster (Diptera: Drosophilidae). Here we test the hypothesis that precocious activation of EcR and USP in the ovaries of paedogenetic gall midges allows for precocious ovarian differentiation. Using monoclonal antibodies directed against insect EcR and USP proteins, we first show that when these gall midges are reared under conditions that promote typical, metamorphic development, up- regulation of EcR and USP occurs in the final larval stage. By contrast, in the paedogenetic life cycle, EcR and USP are up-regulated early in the first larval stage. A similar pattern is seen for two independently-evolved paedogenetic gall midges, Heteropeza pygmaea and Mycophila speyeri. We discuss our results in the context of developmental constraints on the evolution of paedogenesis in dipteran insects.

The ghost sex-life of the paedogenetic beetle Micromalthus debilis

“…We think it plausible that the metamorphosis from larvae to adults is controlled by a very limited number of genes that mutated. The precocious activation of the ecdysone receptor and ultraspiracle in paedogenetic gall midge larvae are sufficient to induce the development of ovaries within the larval instars22. Metamorphosis being regulated by very few genes would facilitate the selection for the paedogenetic phenotype.…”

Expression of the Pupal Determinant broad during Metamorphic and Neotenic Development of the Strepsipteran Xenos vesparum Rossi

“…Paedogenesis, the retention of juvenile traits in adults that may occur through neoteny, has evolved at least 6 times in insects [44]. However, little is known of the genetic or endocrine mechanisms that have been altered during evolution to produce neotenic development.…”

“…In the ovaries of D. melanogaster , EcR/USP heterodimers appear in the last larval instar and are required for proper progression of ovarian differentiation [46]. Similarly, an increase in EcR/USP proteins is found in the final larval instar of the gall midges H. pygmaea and Mycophila speyeri (Barnes), during metamorphosis while EcR/USP proteins are upregulated early in the first larval instar during paedogenetic development [44]. These findings suggest that shifts in the timing of endocrine regulators of metamorphosis, like EcR/USP or br , in one tissue with respect to the entire organism may account for the development of paedogenetic development.…”

Why grow up?Aperspective on insect strategies to avoid metamorphosis

“…Insects that have lost complete metamorphosis via type I paedomorphosis are known from several independent dipteran lineages (Johannsen, ; Wyatt, , , ; Ibrahim & Gad, ; Hodin & Riddiford, ) and the unusual beetle species Micromalthus debilis (reviewed in Pollock & Normark, ). Common to all insects possessing this strategy, development and maturation of the germ line are accelerated and occur during the larval stage, resulting in arrested development of the soma, no further bodily growth, and parthenogenetic reproduction.…”