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The Morphological Transformation of the Thorax during the Eclosion of Drosophila melanogaster (Diptera: Drosophilidae)

SIMPLE SUMMARY: The developmental process, divided into four different stages (egg, larva, pupa and adult), is the main reason for their remarkable diversification and expansion of the insect group Holometabola. Advanced morphological techniques have been used to demonstrate the 3D thoracic anatomic...

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Autores principales: Liu, Si-Pei, Yin, Hao-Dong, Li, Wen-Jie, Qin, Zhuang-Hui, Yang, Yi, Huang, Zheng-Zhong, Zong, Le, Liu, Xiao-Kun, Du, Zhong, Fan, Wei-Li, Zhang, Ya-Qiong, Zhang, Dan, Zhang, Yong E., Liu, Xing-Yue, Yang, Ding, Ge, Si-Qin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10671814/
https://www.ncbi.nlm.nih.gov/pubmed/37999092
http://dx.doi.org/10.3390/insects14110893
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author Liu, Si-Pei
Yin, Hao-Dong
Li, Wen-Jie
Qin, Zhuang-Hui
Yang, Yi
Huang, Zheng-Zhong
Zong, Le
Liu, Xiao-Kun
Du, Zhong
Fan, Wei-Li
Zhang, Ya-Qiong
Zhang, Dan
Zhang, Yong E.
Liu, Xing-Yue
Yang, Ding
Ge, Si-Qin
author_facet Liu, Si-Pei
Yin, Hao-Dong
Li, Wen-Jie
Qin, Zhuang-Hui
Yang, Yi
Huang, Zheng-Zhong
Zong, Le
Liu, Xiao-Kun
Du, Zhong
Fan, Wei-Li
Zhang, Ya-Qiong
Zhang, Dan
Zhang, Yong E.
Liu, Xing-Yue
Yang, Ding
Ge, Si-Qin
author_sort Liu, Si-Pei
collection PubMed
description SIMPLE SUMMARY: The developmental process, divided into four different stages (egg, larva, pupa and adult), is the main reason for their remarkable diversification and expansion of the insect group Holometabola. Advanced morphological techniques have been used to demonstrate the 3D thoracic anatomical structures of the holometalous model organism fruit fly, Drosophila melanogaster, before and after emergence, in order to uncover the transformation process of the muscles, nerves, and gut during development. Skeletal changes affect the original positions of the muscles. The muscles vary in size, not only becoming longer and broader, but also shorter and narrower. Different muscle shapes may appear during development. The number of bundles may also vary. The soft tissues in the body may fix the free ends of the growing muscles, and a strong adult skeleton likely causes the absence of some muscles and tendons. The flight muscles appear very early, probably to achieve full functionality of these very large adult-specific muscles in time. There are some differences during the same developmental period between the two sexes. Most muscles of the larvae and adults with similar attachment positions change their functions from supporting crawling to supporting flying and walking under the control of a more complex ventral nerve cord. The midguts of the larva and the adult are nearly the same. ABSTRACT: The model organism Drosophila melanogaster, as a species of Holometabola, undergoes a series of transformations during metamorphosis. To deeply understand its development, it is crucial to study its anatomy during the key developmental stages. We describe the anatomical systems of the thorax, including the endoskeleton, musculature, nervous ganglion, and digestive system, from the late pupal stage to the adult stage, based on micro-CT and 3D visualizations. The development of the endoskeleton causes original and insertional changes in muscles. Several muscles change their shape during development in a non-uniform manner with respect to both absolute and relative size; some become longer and broader, while others shorten and become narrower. Muscular shape may vary during development. The number of muscular bundles also increases or decreases. Growing muscles are probably anchored by the tissues in the stroma. Some muscles and tendons are absent in the adult stage, possibly due to the hardened sclerites. Nearly all flight muscles are present by the third day of the pupal stage, which may be due to the presence of more myofibers with enough mitochondria to support flight power. There are sexual differences in the same developmental period. In contrast to the endodermal digestive system, the functions of most thoracic muscles change in the development from the larva to the adult in order to support more complex locomotion under the control of a more structured ventral nerve cord based on the serial homology proposed herein.
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spelling pubmed-106718142023-11-18 The Morphological Transformation of the Thorax during the Eclosion of Drosophila melanogaster (Diptera: Drosophilidae) Liu, Si-Pei Yin, Hao-Dong Li, Wen-Jie Qin, Zhuang-Hui Yang, Yi Huang, Zheng-Zhong Zong, Le Liu, Xiao-Kun Du, Zhong Fan, Wei-Li Zhang, Ya-Qiong Zhang, Dan Zhang, Yong E. Liu, Xing-Yue Yang, Ding Ge, Si-Qin Insects Article SIMPLE SUMMARY: The developmental process, divided into four different stages (egg, larva, pupa and adult), is the main reason for their remarkable diversification and expansion of the insect group Holometabola. Advanced morphological techniques have been used to demonstrate the 3D thoracic anatomical structures of the holometalous model organism fruit fly, Drosophila melanogaster, before and after emergence, in order to uncover the transformation process of the muscles, nerves, and gut during development. Skeletal changes affect the original positions of the muscles. The muscles vary in size, not only becoming longer and broader, but also shorter and narrower. Different muscle shapes may appear during development. The number of bundles may also vary. The soft tissues in the body may fix the free ends of the growing muscles, and a strong adult skeleton likely causes the absence of some muscles and tendons. The flight muscles appear very early, probably to achieve full functionality of these very large adult-specific muscles in time. There are some differences during the same developmental period between the two sexes. Most muscles of the larvae and adults with similar attachment positions change their functions from supporting crawling to supporting flying and walking under the control of a more complex ventral nerve cord. The midguts of the larva and the adult are nearly the same. ABSTRACT: The model organism Drosophila melanogaster, as a species of Holometabola, undergoes a series of transformations during metamorphosis. To deeply understand its development, it is crucial to study its anatomy during the key developmental stages. We describe the anatomical systems of the thorax, including the endoskeleton, musculature, nervous ganglion, and digestive system, from the late pupal stage to the adult stage, based on micro-CT and 3D visualizations. The development of the endoskeleton causes original and insertional changes in muscles. Several muscles change their shape during development in a non-uniform manner with respect to both absolute and relative size; some become longer and broader, while others shorten and become narrower. Muscular shape may vary during development. The number of muscular bundles also increases or decreases. Growing muscles are probably anchored by the tissues in the stroma. Some muscles and tendons are absent in the adult stage, possibly due to the hardened sclerites. Nearly all flight muscles are present by the third day of the pupal stage, which may be due to the presence of more myofibers with enough mitochondria to support flight power. There are sexual differences in the same developmental period. In contrast to the endodermal digestive system, the functions of most thoracic muscles change in the development from the larva to the adult in order to support more complex locomotion under the control of a more structured ventral nerve cord based on the serial homology proposed herein. MDPI 2023-11-18 /pmc/articles/PMC10671814/ /pubmed/37999092 http://dx.doi.org/10.3390/insects14110893 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Liu, Si-Pei
Yin, Hao-Dong
Li, Wen-Jie
Qin, Zhuang-Hui
Yang, Yi
Huang, Zheng-Zhong
Zong, Le
Liu, Xiao-Kun
Du, Zhong
Fan, Wei-Li
Zhang, Ya-Qiong
Zhang, Dan
Zhang, Yong E.
Liu, Xing-Yue
Yang, Ding
Ge, Si-Qin
The Morphological Transformation of the Thorax during the Eclosion of Drosophila melanogaster (Diptera: Drosophilidae)
title The Morphological Transformation of the Thorax during the Eclosion of Drosophila melanogaster (Diptera: Drosophilidae)
title_full The Morphological Transformation of the Thorax during the Eclosion of Drosophila melanogaster (Diptera: Drosophilidae)
title_fullStr The Morphological Transformation of the Thorax during the Eclosion of Drosophila melanogaster (Diptera: Drosophilidae)
title_full_unstemmed The Morphological Transformation of the Thorax during the Eclosion of Drosophila melanogaster (Diptera: Drosophilidae)
title_short The Morphological Transformation of the Thorax during the Eclosion of Drosophila melanogaster (Diptera: Drosophilidae)
title_sort morphological transformation of the thorax during the eclosion of drosophila melanogaster (diptera: drosophilidae)
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10671814/
https://www.ncbi.nlm.nih.gov/pubmed/37999092
http://dx.doi.org/10.3390/insects14110893
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