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)

In gall midges such as Mycophila speyeri, larval parthenogenesis proceeds via viviparous thelytoky, with mothers giving birth to live all-female progeny initially developing from unfertilised eggs.

“In gall midges such as Mycophila speyeri (Fig. 1a), larval parthenogenesis proceeds via viviparous thelytoky, i.e. mothers give birth to live all-female progeny initially developing from unfertilised eggs (Hodin & Riddiford, 2000; Normark, 2003).”

Sexually reproducing females of Mycophila speyeri undergo a normal metamorphic cycle, where ovary development is no longer accelerated, and follicle and oocyte formation occur during the pre-pupal and early pupal stages, respectively.

“Sexually reproducing females undergo a normal metamorphic cycle, where ovary development is no longer accelerated, and follicle and oocyte formation occur during the pre-pupal and early pupal stages, respectively (Hodin & Riddiford, 2000).”

When fresh fungal hyphae are present (high-quality food), up-regulation of EcR and USP occurs early in the first larval instar, leading to paedomorphic development.

“However, when fresh fungal hyphae are present (high-quality food), up-regulation of EcR and USP occurs early in the first larval instar, leading to paedomorphic development (Hodin & Riddiford, 2000).”

In type I paedomorphosis, gall midges have evolved an alternative strategy involving early up-regulation of ecdysone receptor (EcR) and ultraspiracle (USP) in the ovaries.

“In type I paedomorphosis, gall midges have evolved an alternative strategy involving early up-regulation of ecdysone receptor (EcR) and ultraspiracle (USP) in the ovaries.”

In gall midges with the capacity for paedomorphosis, when available fungal hyphae are old (low-quality food), EcR and USP up-regulation occurs only in the final larval stage and the flies undergo metamorphosis.

“This is also the case in gall midges with the capacity for paedomorphosis, when available fungal hyphae are old (low-quality food) and flies undergo metamorphosis (Hodin & Riddiford, 2000).”

The loss of complete metamorphosis may be more common than is currently appreciated.

“Given the lack of knowledge concerning the pre-pupal biology of most insects (Hodin & Riddiford, 2000), which can be both highly cryptic (Kathirithamby & Johnston, 2004) and difficult to study (Mjöberg, 1925), the loss of complete metamorphosis may be more common than is currently appreciated.”

The ultimate causal mechanism behind the avoidance of metamorphosis is unknown.

“the ultimate causal mechanism behind the avoidance of metamorphosis is unknown (Hodin & Riddiford, 2000).”

The pattern of precocious up-regulation of EcR and USP is highly similar in both species of paedomorphic gall midge so far examined (Heteropeza pygmaea and Mycophila speyeri), despite the proposed convergent evolution of type I paedomorphosis in these species.

“Interestingly, the pattern of precocious up-regulation of EcR and USP is highly similar in both species of paedomorphic gall midge so far examined ( Heteropeza pygmaea and Mycophila speyeri ), despite the proposed convergent evolution of type I paedomorphosis in these species (Hodin & Riddiford, 2000).”

Hodin and Riddiford (2000) postulated that the loss of complete metamorphosis by type I paedomorphosis is concentrated in more basally located dipteran lineages (except for M. debilis) due to the predominance of early germ line development in basally occurring dipteran lineages, where this process can begin as early as embryogenesis.

“For example, Hodin and Riddiford (2000) postulated that the loss of complete metamorphosis by type I paedomorphosis is concentrated in more basally located dipteran lineages (except for M. debilis ) due to the predominance of early germ line development in basally occurring dipteran lineages, where this process can begin as early as embryogenesis.”

In the typical insect pattern, including the higher flies, ovarian somatic cell types differentiate before the germ line.

“This is in contrast to the typical insect pattern, including the higher flies, where ovarian somatic cell types differentiate before the germ line (Hodin & Riddiford, 2000).”