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

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 underly...

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Autores principales: Nii, Ryotaro, Oguchi, Kohei, Shinji, Junpei, Koshikawa, Shigeyuki, Miura, Toru
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6521406/
https://www.ncbi.nlm.nih.gov/pubmed/31123582
http://dx.doi.org/10.1186/s13227-019-0123-8
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author Nii, Ryotaro
Oguchi, Kohei
Shinji, Junpei
Koshikawa, Shigeyuki
Miura, Toru
author_facet Nii, Ryotaro
Oguchi, Kohei
Shinji, Junpei
Koshikawa, Shigeyuki
Miura, Toru
author_sort Nii, Ryotaro
collection PubMed
description 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13227-019-0123-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-65214062019-05-23 Reduction of a nymphal instar in a dampwood termite: heterochronic shift in the caste differentiation pathways Nii, Ryotaro Oguchi, Kohei Shinji, Junpei Koshikawa, Shigeyuki Miura, Toru EvoDevo Research 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13227-019-0123-8) contains supplementary material, which is available to authorized users. BioMed Central 2019-05-16 /pmc/articles/PMC6521406/ /pubmed/31123582 http://dx.doi.org/10.1186/s13227-019-0123-8 Text en © The Author(s) 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Nii, Ryotaro
Oguchi, Kohei
Shinji, Junpei
Koshikawa, Shigeyuki
Miura, Toru
Reduction of a nymphal instar in a dampwood termite: heterochronic shift in the caste differentiation pathways
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 Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6521406/
https://www.ncbi.nlm.nih.gov/pubmed/31123582
http://dx.doi.org/10.1186/s13227-019-0123-8
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