Lineage-specific head development in the coffin-headed cricket Loxoblemmus equestris links the final molt with novel trait evolution.

Abstract

Background: Lineage-specific adult structures form through modifications of pre-existing juvenile body parts during postembryonic development in insects. It remains unclear how these novel traits originate from ancestral structures within the constrained body plan. In the coffin-headed cricket Loxoblemmus equestris, an ancestral rounded head shape directly transforms into a flattened derived form in a sex-specific manner. To understand the origin of novel traits, we investigated the development of the adult head in L. equestris as a model of lineage-specific novelty.

Results: We found that head morphologies remained sexually monomorphic until the final molt, and the male-specific head shape emerged in the frons region during the transition to adulthood in L. equestris. Two- and three-dimensional morphological analyses revealed that the sexual dimorphism in the frons epithelial folding patterns appeared in the late final nymphal instar. These results suggest that the male-specific novel head development is linked to the final molt in L. equestris. We tested this hypothesis by knocking down the metamorphic gene network (MGN) comprised of Krüppel-homolog 1 (Kr-h1), broad (br), and Ecdysone induced protein 93F (E93). Despite the timing shifts of the nymph-to-adult transition caused by knockdown of the MGN, male-specific head structures are formed only after the final molt.

Conclusions: These results demonstrate that the novel male head structures are formed during the final molt through the formation of sex-specific epithelial patterns in L. equestris. This highlights the unique metamorphic lifecycle with the final molt as a driver that has created lineage- and sex-specific adult forms in insects.