Lineage-specific head development in the coffin-headed cricket Loxoblemmus equestris links concentrated insect metamorphosis with novel trait evolution

Background Lineage-specific adult structures form through modifications of preexisting 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 Detailed two- and three-dimensional analyses of the developing head revealed that sexually dimorphic epithelial patterns formed in a specific region, the frons, during the preadult instar. The male-specific head shapes are formed following the final molt to adulthood even after timing shifts of the metamorphosis induced by RNA interference targeting the evolutionarily conserved metamorphic gene network. Conclusions These findings demonstrate that adult metamorphosis, led by E93, locally relaxes the body plan constraint to permit dramatic transformation of juvenile body parts into a novel head shape by modifying epithelial folding in L . equestris . This highlights concentrated metamorphosis through the final molt as a driver that creates lineage- and sex-specific adult forms in the hexapod lineage.