Adaptations for gas exchange enabled the elongation of lepidopteran proboscises

Jiang, Miao; Zhang, Xinfang; Fezzaa, Kamel; Reiter, Kristen E.; Kramer-Lehnert, Valerie R.; Davis, Brandon T.; Wei, Qi-Huo; Lehnert, Matthew S.

doi:10.1016/j.cub.2023.06.014

Adaptations for gas exchange enabled the elongation of lepidopteran proboscises

Journal Article · Wed Jun 28 00:00:00 EDT 2023 · Current Biology

DOI:https://doi.org/10.1016/j.cub.2023.06.014· OSTI ID:2404972

Jiang, Miao ^[1]; Zhang, Xinfang ^[2]; Fezzaa, Kamel ^[3]; Reiter, Kristen E. ^[4]; Kramer-Lehnert, Valerie R. ^[4]; Davis, Brandon T. ^[4]; Wei, Qi-Huo ^[1]; ^[4]

Southern University of Science and Technology (SUSTech), Shenzhen (China); Kent State Univ., Kent, OH (United States)
Kent State Univ., Kent, OH (United States)
Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Kent State University at Stark, North Canton, OH (United States)

The extensive biodiversification of butterflies and moths (Lepidoptera) is partly attributed to their unique mouthparts (proboscis [Pr]) that can span in length from less than 1 mm to over 280mm in Darwin's sphinx moths. Lepi-doptera, similar to other insects, are believed to inhale and exhale respiratory gases only through valve-like spi-racles on their thorax and abdomen, making gas exchange through the narrow tracheae (Tr) challenging for the elongated Pr. How Lepidoptera overcome distance effects for gas transport to the Pr is an open question that is important to understanding how the Pr elongated over evolutionary time. Here, we show with scanning electron microscopy and X-ray imaging that distance effects on gas exchange are overcome by previously unreported micropores on the Pr surface and by superhydrophobic Tr that prevent water loss and entry. We find that the density of micropores decreases monotonically along the Pr length with the maxima proportional to the Pr length and that micropore diameters produce a Knudsen number at the boundary between the slip and transition flow regimes. By numerical estimation, we further show that the respiratory gas exchange for the Pr predominantly occurs via diffusion through the micropores. In conclusion, these adaptations are key innovations vital to Pr elongation, which likely facilitated lepidopteran biodiversification and the radiation of angiosperms by coevolutionary processes.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 2404972

Journal Information:: Current Biology, Journal Name: Current Biology Journal Issue: 14 Vol. 33; ISSN 0960-9822

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (43)

Surviving submerged—Setal tracheal gills for gas exchange in adult rheophilic diving beetles Kehl, Siegfried; Dettner, Konrad Journal of Morphology, Vol. 270, Issue 11 https://doi.org/10.1002/jmor.10762	journal	May 2009
Evolutionary functional morphology of the proboscis and feeding apparatus of hawk moths (Sphingidae: Lepidoptera) Reinwald, Caroline; Bauder, Julia A. ‐S.; Karolyi, Florian Journal of Morphology, Vol. 283, Issue 11 https://doi.org/10.1002/jmor.21510	journal	September 2022
A farewell to arms: using X-ray synchrotron imaging to investigate autotomy in brittle stars Clark, E. G.; Fezzaa, K.; Burke, J. E. Zoomorphology, Vol. 138, Issue 3 https://doi.org/10.1007/s00435-019-00451-7	journal	June 2019
Olfactory carbon dioxide detection by insects and other animals Jones, Walton Molecules and Cells, Vol. 35, Issue 2 https://doi.org/10.1007/s10059-013-0035-8	journal	February 2013
Some features of the respiratory system of Hydrocyrius columbiae Spin. (Belostomatidae, Hemiptera) Miller, P. L. Journal of Insect Physiology, Vol. 6, Issue 4 https://doi.org/10.1016/0022-1910(61)90053-1	journal	August 1961
Lipids of the insect cuticle: origin, composition and function Lockey, Kenneth H. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, Vol. 89, Issue 4 https://doi.org/10.1016/0305-0491(88)90305-7	journal	January 1988
Insect antennae: Coupling blood pressure with cuticle deformation to control movement Donley, Griffin; Sun, Yueming; Pass, Günther Acta Biomaterialia, Vol. 147 https://doi.org/10.1016/j.actbio.2022.05.044	journal	July 2022
Respiratory Biology: Why Insects Evolved Discontinuous Gas Exchange Lighton, John R. B. Current Biology, Vol. 17, Issue 16 https://doi.org/10.1016/j.cub.2007.06.007	journal	August 2007
The mechanics of airway closure Heil, Matthias; Hazel, Andrew L.; Smith, Jaclyn A. Respiratory Physiology & Neurobiology, Vol. 163, Issue 1-3 https://doi.org/10.1016/j.resp.2008.05.013	journal	November 2008
The oldest predaceous water bugs (Insecta, Heteroptera, Belostomatidae), with implications for paleolimnology of the Triassic Cow Branch Formation Criscione, Julia; Grimaldi, David Journal of Paleontology, Vol. 91, Issue 6 https://doi.org/10.1017/jpa.2017.48	journal	September 2017
Spiracular Control of Discontinuous Respiration in Insects Schneiderman, Howard A. Nature, Vol. 177, Issue 4521 https://doi.org/10.1038/1771169a0	journal	June 1956
The evolution of flowers with deep corolla tubes Nilsson, L. Anders Nature, Vol. 334, Issue 6178 https://doi.org/10.1038/334147a0	journal	July 1988
Implications of the late Palaeozoic oxygen pulse for physiology and evolution Graham, Jeffrey B.; Aguilar, Nancy M.; Dudley, Robert Nature, Vol. 375, Issue 6527 https://doi.org/10.1038/375117a0	journal	May 1995
Insects breathe discontinuously to avoid oxygen toxicity Hetz, Stefan K.; Bradley, Timothy J. Nature, Vol. 433, Issue 7025 https://doi.org/10.1038/nature03106	journal	February 2005
NIH Image to ImageJ: 25 years of image analysis Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W. Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2089	journal	June 2012
Evolutionary responses of discontinuous gas exchange in insects White, Craig R.; Blackburn, Tim M.; Terblanche, John S. Proceedings of the National Academy of Sciences, Vol. 104, Issue 20 https://doi.org/10.1073/pnas.0608968104	journal	May 2007
Increase in tracheal investment with beetle size supports hypothesis of oxygen limitation on insect gigantism Kaiser, Alexander; Klok, C. Jaco; Socha, John J. Proceedings of the National Academy of Sciences, Vol. 104, Issue 32 https://doi.org/10.1073/pnas.0611544104	journal	August 2007
Early steps of angiosperm–pollinator coevolution Hu, Shusheng; Dilcher, David L.; Jarzen, David M. Proceedings of the National Academy of Sciences, Vol. 105, Issue 1 https://doi.org/10.1073/pnas.0707989105	journal	January 2008
Phylogenomics reveals the evolutionary timing and pattern of butterflies and moths Kawahara, Akito Y.; Plotkin, David; Espeland, Marianne Proceedings of the National Academy of Sciences, Vol. 116, Issue 45 https://doi.org/10.1073/pnas.1907847116	journal	October 2019
A hemipteran insect reveals new genetic mechanisms and evolutionary insights into tracheal system development Hanna, Lisa; Popadić, Aleksandar Proceedings of the National Academy of Sciences, Vol. 117, Issue 8 https://doi.org/10.1073/pnas.1908975117	journal	February 2020
Structure of tracheae and the functional implications for collapse in the American cockroach Webster, Matthew R.; Socha, John J.; Teresi, Luciano Bioinspiration & Biomimetics, Vol. 10, Issue 6 https://doi.org/10.1088/1748-3190/10/6/066011	journal	November 2015
Do insect metabolic rates at rest and during flight scale with body mass? Niven, Jeremy E.; Scharlemann, Jörn P. W. Biology Letters, Vol. 1, Issue 3 https://doi.org/10.1098/rsbl.2005.0311	journal	June 2005
Tracheal compression in pupae of the beetle Zophobas morio Pendar, Hodjat; Kenny, Melissa C.; Socha, John J. Biology Letters, Vol. 11, Issue 6 https://doi.org/10.1098/rsbl.2015.0259	journal	June 2015
Butterfly proboscis: combining a drinking straw with a nanosponge facilitated diversification of feeding habits Monaenkova, Daria; Lehnert, Matthew S.; Andrukh, Taras Journal of The Royal Society Interface, Vol. 9, Issue 69 https://doi.org/10.1098/rsif.2011.0392	journal	August 2011
Effects of weight loading on flight performance and survival of palatable Neotropical Anartia fatima butterflies Srygley, Robert B.; Kingsolver, Joel G. Biological Journal of the Linnean Society, Vol. 70, Issue 4 https://doi.org/10.1111/j.1095-8312.2000.tb00225.x	journal	August 2000
‘Good Heavens what insect can suck it’- Charles Darwin, Angraecum sesquipedale and Xanthopan morganii praedicta Arditti, Joseph; Elliott, John; Kitching, Ian J. Botanical Journal of the Linnean Society, Vol. 169, Issue 3 https://doi.org/10.1111/j.1095-8339.2012.01250.x	journal	June 2012
The Pollinators of the Malagasy Star OrchidsAngraecum sesquipedale, A. sororiumandA. compactumand the Evolution of Extremely Long Spurs by Pollinator Shift Wasserthal, L. T. Botanica Acta, Vol. 110, Issue 5 https://doi.org/10.1111/j.1438-8677.1997.tb00650.x	journal	October 1997
On the Appearance of gas in the Tracheae of Insects Keilin, D. Biological Reviews, Vol. 1, Issue 2 https://doi.org/10.1111/j.1469-185X.1924.tb00534.x	journal	April 1924
A Triassic-Jurassic window into the evolution of Lepidoptera van Eldijk, Timo J. B.; Wappler, Torsten; Strother, Paul K. Science Advances, Vol. 4, Issue 1 https://doi.org/10.1126/sciadv.1701568	journal	January 2018
Tracheal Respiration in Insects Visualized with Synchrotron X-ray Imaging Westneat, M. W. Science, Vol. 299, Issue 5606 https://doi.org/10.1126/science.1078008	journal	January 2003
Phylogenomics resolves the timing and pattern of insect evolution Misof, B.; Liu, S.; Meusemann, K. Science, Vol. 346, Issue 6210 https://doi.org/10.1126/science.1257570	journal	November 2014
Feeding Mechanisms of Adult Lepidoptera: Structure, Function, and Evolution of the Mouthparts Krenn, Harald W. Annual Review of Entomology, Vol. 55, Issue 1 https://doi.org/10.1146/annurev-ento-112408-085338	journal	January 2010
Wetting and Roughness Quéré, David Annual Review of Materials Research, Vol. 38, Issue 1, p. 71-99 https://doi.org/10.1146/annurev.matsci.38.060407.132434	journal	August 2008
How Locusts Breathe Harrison, Jon F.; Waters, James S.; Cease, Arianne J. Physiology, Vol. 28, Issue 1 https://doi.org/10.1152/physiol.00043.2012	journal	January 2013
The Structure of Insect Tracheae Locke, M. Journal of Cell Science, Vol. S3-98, Issue 44 https://doi.org/10.1242/jcs.s3-98.44.487	journal	December 1957
The role of discontinuous gas exchange in insects: the chthonic hypothesis does not hold water Gibbs, Allen G.; Johnson, Robert A. Journal of Experimental Biology, Vol. 207, Issue 20 https://doi.org/10.1242/jeb.01168	journal	September 2004
Correlated patterns of tracheal compression and convective gas exchange in a carabid beetle Socha, J. J.; Lee, W. -K.; Harrison, J. F. Journal of Experimental Biology, Vol. 211, Issue 21 https://doi.org/10.1242/jeb.019877	journal	November 2008
Metabolic rate controls respiratory pattern in insects Contreras, H. L.; Bradley, T. J. Journal of Experimental Biology, Vol. 212, Issue 3 https://doi.org/10.1242/jeb.024091	journal	February 2009
Cavitation in the embryonic tracheal system ofManduca sexta Woods, H. Arthur; Sprague, Jonathan C.; Smith, Jennifer N. Journal of Experimental Biology, Vol. 212, Issue 20 https://doi.org/10.1242/jeb.027458	journal	October 2009
Cutaneous respiration by diving beetles from underground aquifers of Western Australia (Coleoptera: Dytiscidae) Jones, Karl K.; Cooper, Steven J. B.; Seymour, Roger S. Journal of Experimental Biology, Vol. 222, Issue 7 https://doi.org/10.1242/jeb.196659	journal	April 2019
Haemolymph Acid–Base Status, Tracheal gas Levels and the Control of Post-Exercise Ventilation Rate in Grasshoppers Krolikowski, Katherine; Harrison, Jon F. Journal of Experimental Biology, Vol. 199, Issue 2 https://doi.org/10.1242/jeb.199.2.391	journal	February 1996
Acid–Base and Respiratory Responses to Hypoxia in the Grasshopper Schistocerca Americana Greenlee, Kendra J.; Harrison, Jon F. Journal of Experimental Biology, Vol. 201, Issue 20 https://doi.org/10.1242/jeb.201.20.2843	journal	October 1998
Respiration and Tracheal Ventilation in Locusts and other Flying Insects Weis-Fogh, Torkel Journal of Experimental Biology, Vol. 47, Issue 3 https://doi.org/10.1242/jeb.47.3.561	journal	December 1967

Similar Records

Biomechanical drivers of the evolution of butterflies and moths with a coilable proboscis

Journal Article · Tue Nov 26 19:00:00 EST 2024 · Proceedings of the Royal Society B: Biological Sciences · OSTI ID:2478890

Mouthpart conduit sizes of fluid-feeding insects determine the ability to feed from pores

Journal Article · Tue Jan 03 19:00:00 EST 2017 · Proceedings of the Royal Society B: Biological Sciences · OSTI ID:1341685

Mevalonate Pathway Promiscuity Enables Noncanonical Terpene Production

Journal Article · Tue Sep 17 20:00:00 EDT 2019 · ACS Synthetic Biology · OSTI ID:1594932

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
coevolution
diffusion
insect respiration
micropore
superhydrophobicity

Adaptations for gas exchange enabled the elongation of lepidopteran proboscises

Citation Formats

References (43)

Similar Records

Related Subjects