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 crick...

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Main Authors: Mizuho Yoneda, Shinichi Morita, Teruyuki Niimi, Takaaki Daimon, Takahiro Ohde
Format: Article
Language:English
Published: BMC 2025-07-01
Series:EvoDevo
Online Access:https://doi.org/10.1186/s13227-025-00249-3
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author Mizuho Yoneda
Shinichi Morita
Teruyuki Niimi
Takaaki Daimon
Takahiro Ohde
author_facet Mizuho Yoneda
Shinichi Morita
Teruyuki Niimi
Takaaki Daimon
Takahiro Ohde
author_sort Mizuho Yoneda
collection DOAJ
description 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.
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spelling doaj-art-55d3bf0e7b654fa285b7a8798a3ffe0a2025-08-20T04:02:54ZengBMCEvoDevo2041-91392025-07-0116111310.1186/s13227-025-00249-3Lineage-specific head development in the coffin-headed cricket Loxoblemmus equestris links the final molt with novel trait evolutionMizuho Yoneda0Shinichi Morita1Teruyuki Niimi2Takaaki Daimon3Takahiro Ohde4Department of Applied Biosciences, Graduate School of Agriculture, Kyoto UniversityDivision of Evolutionary Developmental Biology, National Institute for Basic BiologyDivision of Evolutionary Developmental Biology, National Institute for Basic BiologyDepartment of Applied Biosciences, Graduate School of Agriculture, Kyoto UniversityDepartment of Applied Biosciences, Graduate School of Agriculture, Kyoto UniversityAbstract 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.https://doi.org/10.1186/s13227-025-00249-3
spellingShingle Mizuho Yoneda
Shinichi Morita
Teruyuki Niimi
Takaaki Daimon
Takahiro Ohde
Lineage-specific head development in the coffin-headed cricket Loxoblemmus equestris links the final molt with novel trait evolution
EvoDevo
title Lineage-specific head development in the coffin-headed cricket Loxoblemmus equestris links the final molt with novel trait evolution
title_full Lineage-specific head development in the coffin-headed cricket Loxoblemmus equestris links the final molt with novel trait evolution
title_fullStr Lineage-specific head development in the coffin-headed cricket Loxoblemmus equestris links the final molt with novel trait evolution
title_full_unstemmed Lineage-specific head development in the coffin-headed cricket Loxoblemmus equestris links the final molt with novel trait evolution
title_short Lineage-specific head development in the coffin-headed cricket Loxoblemmus equestris links the final molt with novel trait evolution
title_sort lineage specific head development in the coffin headed cricket loxoblemmus equestris links the final molt with novel trait evolution
url https://doi.org/10.1186/s13227-025-00249-3
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