TY - JOUR
T1 - Developmental plasticity and stability in the tracheal networks supplying Drosophila flight muscle in response to rearing oxygen level
AU - Harrison, Jon
AU - Waters, James S.
AU - Biddulph, Taylor A.
AU - Kovacevic, Aleksandra
AU - Klok, C. Jaco
AU - Socha, John J.
N1 - Funding Information:
Use of the Advanced Photon Source, an Office of Science User Facility operated for the U.S. Department of Energy (DOE) Office of Science by Argonne National Laboratory, was supported by the U.S. DOE under Contract No. DE-AC02-06CH11357. Francesco De Carlo, Xianghui Xiao, Kamel Fezzaa, and Wah-Keat Lee were especially helpful with developing protocols for synchrotron x-ray imaging, and Xianghui Xiao and Francesco De Carlo performed the three-dimensional reconstructions of the SR-µCT images. We thank Elizabeth Lee for help with Fig. 2 . Carsten Duch, Claudia Kuehn, Fernando Vonhoff, and Erin McKiernan taught us how to dissect Drosophila flight muscle. Robert Roberson, Douglas Chandler, David Lowry, Bret Judson, and Deborah Baluch were instrumental in supporting our use of the Keck Bioimaging Facility at Arizona State University. The manuscript was substantially improved by the comments of two anonymous reviewers. This research was supported by NSF IOS 1122157, NSF IOS 0419704 to J.F.H., and NSF EFRI 0938047 and NSF IOS 1558052 to J.J.S. and J.F.H.
Publisher Copyright:
© 2017 Elsevier Ltd
PY - 2018/4
Y1 - 2018/4
N2 - While it is clear that the insect tracheal system can respond in a compensatory manner to both hypoxia and hyperoxia, there is substantial variation in how different parts of the system respond. However, the response of tracheal structures, from the tracheoles to the largest tracheal trunks, have not been studied within one species. In this study, we examined the effect of larval/pupal rearing in hypoxia, normoxia, and hyperoxia (10, 21 or 40 kPa oxygen) on body size and the tracheal supply to the flight muscles of Drosophila melanogaster, using synchrotron radiation micro-computed tomography (SR-µCT) to assess flight muscle volumes and the major tracheal trunks, and confocal microscopy to assess the tracheoles. Hypoxic rearing decreased thorax length whereas hyperoxic-rearing decreased flight muscle volumes, suggestive of negative effects of both extremes. Tomography at the broad organismal scale revealed no evidence for enlargement of the major tracheae in response to lower rearing oxygen levels, although tracheal size scaled with muscle volume. However, using confocal imaging, we found a strong inverse relationship between tracheole density within the flight muscles and rearing oxygen level, and shorter tracheolar branch lengths in hypoxic-reared animals. Although prior studies of larger tracheae in other insects indicate that axial diffusing capacity should be constant with sequential generations of branching, this pattern was not found in the fine tracheolar networks, perhaps due to the increasing importance of radial diffusion in this regime. Overall, D. melanogaster responded to rearing oxygen level with compensatory morphological changes in the small tracheae and tracheoles, but retained stability in most of the other structural components of the tracheal supply to the flight muscles.
AB - While it is clear that the insect tracheal system can respond in a compensatory manner to both hypoxia and hyperoxia, there is substantial variation in how different parts of the system respond. However, the response of tracheal structures, from the tracheoles to the largest tracheal trunks, have not been studied within one species. In this study, we examined the effect of larval/pupal rearing in hypoxia, normoxia, and hyperoxia (10, 21 or 40 kPa oxygen) on body size and the tracheal supply to the flight muscles of Drosophila melanogaster, using synchrotron radiation micro-computed tomography (SR-µCT) to assess flight muscle volumes and the major tracheal trunks, and confocal microscopy to assess the tracheoles. Hypoxic rearing decreased thorax length whereas hyperoxic-rearing decreased flight muscle volumes, suggestive of negative effects of both extremes. Tomography at the broad organismal scale revealed no evidence for enlargement of the major tracheae in response to lower rearing oxygen levels, although tracheal size scaled with muscle volume. However, using confocal imaging, we found a strong inverse relationship between tracheole density within the flight muscles and rearing oxygen level, and shorter tracheolar branch lengths in hypoxic-reared animals. Although prior studies of larger tracheae in other insects indicate that axial diffusing capacity should be constant with sequential generations of branching, this pattern was not found in the fine tracheolar networks, perhaps due to the increasing importance of radial diffusion in this regime. Overall, D. melanogaster responded to rearing oxygen level with compensatory morphological changes in the small tracheae and tracheoles, but retained stability in most of the other structural components of the tracheal supply to the flight muscles.
KW - Developmental plasticity
KW - Flight muscle
KW - Gas exchange
KW - Oxygen
KW - Tracheae
KW - Tracheoles
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U2 - 10.1016/j.jinsphys.2017.09.006
DO - 10.1016/j.jinsphys.2017.09.006
M3 - Article
C2 - 28927826
AN - SCOPUS:85029597564
VL - 106
SP - 189
EP - 198
JO - Journal of Insect Physiology
JF - Journal of Insect Physiology
SN - 0022-1910
ER -