The embryonic role of juvenile hormone in the firebrat, Thermobia domestica, reveals its function before its involvement in metamorphosis

Abstract

Juvenile hormone (JH) is a key regulator of insect metamorphosis. To understand its role before metamorphosis originated, we studied JH action in the ametabolous firebrat, Thermobia domestica. JH levels peak late in embryogenesis and are low through early juvenile stages. Chemical suppression of embryonic JH synthesis by 7-ethoxyprecocene blocks embryonic differentiation, but the latter is restored with exogenous JH. Premature exposure of younger embryos to JH suppresses growth and morphogenesis and the expression of morphogens, such as myoglianin. These embryos switch to premature differentiation as shown by muscle formation and synthesis of cuticle like that of later embryonic stages. We hypothesize that this ancestral role of JH in supporting tissue differentiation was later exploited for the evolution of metamorphosis. In embryos, the temporal separation of morphogen signaling and JH secretion results in morphogenesis preceding differentiation. With the evolution of metamorphosis, embryonic morphogen systems were redeployed during juvenile growth for morphogenesis of imaginal primordia. JH was also redeployed, but it now occurred with morphogen signaling. This co-occurrence resulted in JH maintaining a juvenile quality to the bud, which the morphogens positive allometric growth. The disappearance of JH late in growth then allowed the unantagonized morphogens to drive the primordia into metamorphosis.

Investigating the origin of insect metamorphosis

“…The extant firebrat also produces Broad-complex, Krüppel homolog 1, and E93, as did probably ancestral ametabolous insects ( Fernandez-Nicolas et al, 2023 ; Truman et al, 2023 ). This suggests that these proteins just needed to take on new functions in order for metamorphosis to evolve.…”

“…However, it is not known which features of ametabolous insects contributed to the evolution of metamorphosis. Now, in eLife, James Truman from the University of Washington and co-workers report that changing levels of a chemical signal known as juvenile hormone may have had a significant role ( Truman et al, 2023 ).…”