Reduction of a nymphal instar in a dampwood termite: heterochronic shift in the caste differentiation pathways

Abstract Background Generally in termites, alates differentiate through multiple nymphal instars which gradually develop wing buds. However, in a dampwood termite, Hodotermopsis sjostedti, alates molt directly from a single nymphal instar with short wing buds. In this study, to examine the mechanism...

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Main Authors: Ryotaro Nii, Kohei Oguchi, Junpei Shinji, Shigeyuki Koshikawa, Toru Miura
Format: Article
Language:English
Published: BMC 2019-05-01
Series:EvoDevo
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13227-019-0123-8
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author Ryotaro Nii
Kohei Oguchi
Junpei Shinji
Shigeyuki Koshikawa
Toru Miura
author_facet Ryotaro Nii
Kohei Oguchi
Junpei Shinji
Shigeyuki Koshikawa
Toru Miura
author_sort Ryotaro Nii
collection DOAJ
description Abstract Background Generally in termites, alates differentiate through multiple nymphal instars which gradually develop wing buds. However, in a dampwood termite, Hodotermopsis sjostedti, alates molt directly from a single nymphal instar with short wing buds. In this study, to examine the mechanism underlying the wing formation during the alate differentiation in H. sjostedti, histological and morphological observations were carried out on the developmental process of wing formation during the nymphal instar, in comparison with those in Zootermopsis nevadensis, which has two nymphal instars. Furthermore, the expression patterns of genes that are thought to be responsible for wing formation, i.e., wing-patterning genes and genes encoding hormone-related factors, were quantified during alate differentiation and compared between the two species. Results The results showed that, in H. sjostedti, wings were formed in a complicatedly folded shape, not only inside the wing buds as seen in Z. nevadensis, but also under the dorsal thoracic cuticle, where the wing tips shifted toward the median thoracic part. Accordingly, the wing expansion pattern also differed from that in Z. nevadensis. Furthermore, the results of real-time qRT-PCR on overall expression profiles of wing-patterning genes and hormone-related genes suggest that the single nymphal instar in H. sjostedti well resembles to the second nymphal instar in Z. nevadensis. In particular, significant upregulation of vestigial (vg) and downregulation of Krüppel homolog 1 (Kr-h1) that were observed at the second nymphal instar in Z. nevadensis apparently occurred during the single nymphal instar in H. sjostedti. Conclusion The developmental events for wing formation are compacted into a single nymphal instar in H. sjostedti, and as a result, the unique wing formation is seen to compensate for the spatial restriction inside small wing buds, leading to the completion of functional wings.
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spelling doaj.art-70e5d621c9e04b05a8dbd334f8920d512022-12-21T17:59:40ZengBMCEvoDevo2041-91392019-05-0110111310.1186/s13227-019-0123-8Reduction of a nymphal instar in a dampwood termite: heterochronic shift in the caste differentiation pathwaysRyotaro Nii0Kohei Oguchi1Junpei Shinji2Shigeyuki Koshikawa3Toru Miura4Graduate School of Environmental Science, Hokkaido UniversityMisaki Marine Biological Station, School of Science, The University of TokyoMisaki Marine Biological Station, School of Science, The University of TokyoFaculty of Environmental Earth Science, Hokkaido UniversityMisaki Marine Biological Station, School of Science, The University of TokyoAbstract Background Generally in termites, alates differentiate through multiple nymphal instars which gradually develop wing buds. However, in a dampwood termite, Hodotermopsis sjostedti, alates molt directly from a single nymphal instar with short wing buds. In this study, to examine the mechanism underlying the wing formation during the alate differentiation in H. sjostedti, histological and morphological observations were carried out on the developmental process of wing formation during the nymphal instar, in comparison with those in Zootermopsis nevadensis, which has two nymphal instars. Furthermore, the expression patterns of genes that are thought to be responsible for wing formation, i.e., wing-patterning genes and genes encoding hormone-related factors, were quantified during alate differentiation and compared between the two species. Results The results showed that, in H. sjostedti, wings were formed in a complicatedly folded shape, not only inside the wing buds as seen in Z. nevadensis, but also under the dorsal thoracic cuticle, where the wing tips shifted toward the median thoracic part. Accordingly, the wing expansion pattern also differed from that in Z. nevadensis. Furthermore, the results of real-time qRT-PCR on overall expression profiles of wing-patterning genes and hormone-related genes suggest that the single nymphal instar in H. sjostedti well resembles to the second nymphal instar in Z. nevadensis. In particular, significant upregulation of vestigial (vg) and downregulation of Krüppel homolog 1 (Kr-h1) that were observed at the second nymphal instar in Z. nevadensis apparently occurred during the single nymphal instar in H. sjostedti. Conclusion The developmental events for wing formation are compacted into a single nymphal instar in H. sjostedti, and as a result, the unique wing formation is seen to compensate for the spatial restriction inside small wing buds, leading to the completion of functional wings.http://link.springer.com/article/10.1186/s13227-019-0123-8TermitesAlate differentiationCaste differentiationNymphal instarWing formationGene expression
spellingShingle Ryotaro Nii
Kohei Oguchi
Junpei Shinji
Shigeyuki Koshikawa
Toru Miura
Reduction of a nymphal instar in a dampwood termite: heterochronic shift in the caste differentiation pathways
EvoDevo
Termites
Alate differentiation
Caste differentiation
Nymphal instar
Wing formation
Gene expression
title Reduction of a nymphal instar in a dampwood termite: heterochronic shift in the caste differentiation pathways
title_full Reduction of a nymphal instar in a dampwood termite: heterochronic shift in the caste differentiation pathways
title_fullStr Reduction of a nymphal instar in a dampwood termite: heterochronic shift in the caste differentiation pathways
title_full_unstemmed Reduction of a nymphal instar in a dampwood termite: heterochronic shift in the caste differentiation pathways
title_short Reduction of a nymphal instar in a dampwood termite: heterochronic shift in the caste differentiation pathways
title_sort reduction of a nymphal instar in a dampwood termite heterochronic shift in the caste differentiation pathways
topic Termites
Alate differentiation
Caste differentiation
Nymphal instar
Wing formation
Gene expression
url http://link.springer.com/article/10.1186/s13227-019-0123-8
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AT shigeyukikoshikawa reductionofanymphalinstarinadampwoodtermiteheterochronicshiftinthecastedifferentiationpathways
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