{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,19]],"date-time":"2026-06-19T02:01:34Z","timestamp":1781834494402,"version":"3.54.5"},"reference-count":49,"publisher":"PeerJ","license":[{"start":{"date-parts":[[2022,7,13]],"date-time":"2022-07-13T00:00:00Z","timestamp":1657670400000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Preludium 12 Project from the National Science Center, Poland","award":["Number 2016\/23\/N\/NZ8\/02815"],"award-info":[{"award-number":["Number 2016\/23\/N\/NZ8\/02815"]}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"crossref","award":["WI 4324\/4-1"],"award-info":[{"award-number":["WI 4324\/4-1"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:p>\n                    The tracheal system comprises one of the major adaptations of insects towards a terrestrial lifestyle. Many aspects such as the modifications towards wing reduction or a life in an arid climate are still poorly understood. To address these issues, we performed the first three-dimensional morphometric analyses of the tracheal system of a wingless insect, the desert beetle\n                    <jats:italic>Gonopus tibialis<\/jats:italic>\n                    and compared it with a flying beetle (\n                    <jats:italic>Tenebrio molitor<\/jats:italic>\n                    ). Our results clearly show that the reduction of the flight apparatus has severe consequences for the tracheal system. This includes the reduction of the tracheal density, the relative volume of the trachea, the volume of the respective spiracles and the complete loss of individual tracheae. At the same time, the reduction of wings in the desert beetle allows modifications of the tracheal system that would be impossible in an animal with a functional flight apparatus such as the formation of a subelytral cavity as a part of the tracheal system, the strong elongation of the digestive tract including its tracheal system or the respiration through a single spiracle. Finally, we addressed when these modifications of the tracheal system take place during the development of the studied beetles. We can clearly show that they develop during pupation while the larvae of both species are almost identical in their tracheal system and body shape.\n                  <\/jats:p>","DOI":"10.7717\/peerj.13378","type":"journal-article","created":{"date-parts":[[2022,7,13]],"date-time":"2022-07-13T04:08:18Z","timestamp":1657685298000},"page":"e13378","source":"Crossref","is-referenced-by-count":4,"title":["Postembryonic development of the tracheal system of beetles in the context of aptery and adaptations towards an arid environment"],"prefix":"10.7717","volume":"10","author":[{"given":"Marcin","family":"Ra\u015b","sequence":"first","affiliation":[{"name":"Zoological Museum, Museum and Institute of Zoology, Polish Academy of Sciences, Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Benjamin","family":"Wipfler","sequence":"additional","affiliation":[{"name":"Zoologisches Forschungsmuseum Alexander Koenig, Leibniz-Institut zur Analyse des Biodiversit\u00e4tswandels, Bonn, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tim","family":"Dannenfeld","sequence":"additional","affiliation":[{"name":"Zoologisches Forschungsmuseum Alexander Koenig, Leibniz-Institut zur Analyse des Biodiversit\u00e4tswandels, Bonn, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dariusz","family":"Iwan","sequence":"additional","affiliation":[{"name":"Zoological Museum, Museum and Institute of Zoology, Polish Academy of Sciences, Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"4443","published-online":{"date-parts":[[2022,7,13]]},"reference":[{"key":"10.7717\/peerj.13378\/ref-1","article-title":"Geomorph: software for geometric morphometric analyses","author":"Adams","year":"2019"},{"key":"10.7717\/peerj.13378\/ref-2","doi-asserted-by":"publisher","first-page":"1377","DOI":"10.1016\/S0022-1910(01)00128-7","article-title":"Revisiting water loss in insects: a large scale view","volume":"47","author":"Addo-Bediako","year":"2001","journal-title":"Journal of Insect Physiology"},{"key":"10.7717\/peerj.13378\/ref-3","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1146\/annurev-ento-112408-085356","article-title":"Insect fat body: energy, metabolism, and regulation","volume":"55","author":"Arrese","year":"2010","journal-title":"Annual Review of Entomology"},{"key":"10.7717\/peerj.13378\/ref-4","doi-asserted-by":"publisher","DOI":"10.1002\/9780470015902.a0022854","article-title":"Origin and evolution of insect metamorphosis","volume-title":"Encyclopedia of life sciences (ELS)","author":"Belles","year":"2011"},{"issue":"2","key":"10.7717\/peerj.13378\/ref-5","first-page":"454","article-title":"Experiments on the regulation of the body temperature of certain tenebrionid beetles","volume":"20","author":"Bolwig","year":"1957","journal-title":"Journal of the Entomological Society of Southern Africa"},{"key":"10.7717\/peerj.13378\/ref-6","doi-asserted-by":"publisher","first-page":"101072","DOI":"10.1016\/j.asd.2021.101072","article-title":"A review of the hexapod tracheal system with a focus on the apterygote groups","volume":"63","author":"Dittrich","year":"2021","journal-title":"Arthropod Structure & Development"},{"issue":"4","key":"10.7717\/peerj.13378\/ref-7","doi-asserted-by":"publisher","first-page":"539","DOI":"10.2307\/3495783","article-title":"The subelytral cavity of desert Tenebrionids","volume":"76","author":"Draney","year":"1993","journal-title":"Florida Entomologist"},{"issue":"2","key":"10.7717\/peerj.13378\/ref-8","doi-asserted-by":"publisher","first-page":"253","DOI":"10.14411\/eje.2002.034","article-title":"The role of the subelytral cavity in water loss in the flightless dung beetle, Circellium bacchus (Coleoptera: Scarabaeinae)","volume":"99","author":"Duncan","year":"2002","journal-title":"European Journal of Entomology"},{"issue":"4","key":"10.7717\/peerj.13378\/ref-9","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1016\/S0022-1910(03)00018-0","article-title":"The role of the subelytral cavity in respiration in a tenebrionid beetle, Onymacris multistriata (Tenebrionidae: Adesmiini)","volume":"49","author":"Duncan","year":"2003","journal-title":"Journal of Insect Physiology"},{"issue":"4","key":"10.7717\/peerj.13378\/ref-10","doi-asserted-by":"publisher","first-page":"452","DOI":"10.1007\/s004420050966","article-title":"Discontinuous gas exchange in dung beetles: patterns and ecological implications","volume":"122","author":"Duncan","year":"2000","journal-title":"Oecologia"},{"key":"10.7717\/peerj.13378\/ref-11","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1242\/jcs.s3-96.34.151","article-title":"The function and metabolism of certain insect muscles in relation to their structure","volume":"3","author":"Edwards","year":"1955","journal-title":"Journal of Cell Science"},{"key":"10.7717\/peerj.13378\/ref-12","doi-asserted-by":"publisher","first-page":"611","DOI":"10.1016\/j.asd.2016.10.007","article-title":"Comparative thoracic anatomy of the wild type and wingless (wg1cn1) mutant of Drosophila melanogaster (Diptera)","volume":"45","author":"Fabian","year":"2016","journal-title":"Arthropod Structure & Development"},{"key":"10.7717\/peerj.13378\/ref-13","doi-asserted-by":"publisher","first-page":"270","DOI":"10.1111\/eea.12417","article-title":"Ordinal species richness in insects\u2014a preliminary study of the influence of morphology, life history, and ecology","volume":"159","author":"Ferns","year":"2016","journal-title":"Entomologia Experimentalis et Applicata"},{"key":"10.7717\/peerj.13378\/ref-14","doi-asserted-by":"publisher","first-page":"84","DOI":"10.1016\/j.jtherbio.2018.03.009","article-title":"Comparative thermoregulation between different species of dung beetles (Coleoptera: Geotrupinae)","volume":"74","author":"Gallegoa","year":"2018","journal-title":"Journal of Thermal Biology"},{"issue":"4","key":"10.7717\/peerj.13378\/ref-15","doi-asserted-by":"publisher","first-page":"797","DOI":"10.1086\/physzool.67.4.30163866","article-title":"Why not to do two-species comparative studies: limitations on inferring adaptation","volume":"67","author":"Garland Jr","year":"1994","journal-title":"Physiological Zoology"},{"issue":"1","key":"10.7717\/peerj.13378\/ref-16","doi-asserted-by":"crossref","first-page":"129","DOI":"10.3897\/asp.73.e31821","article-title":"Transformation of head structures during the metamorphosis of Chrysomela populi (Coleoptera: Chrysomelidae)","volume":"73","author":"Ge","year":"2015","journal-title":"Arthropod Systematics & Phylogeny"},{"key":"10.7717\/peerj.13378\/ref-17","doi-asserted-by":"publisher","first-page":"2293","DOI":"10.1242\/jeb.082479","article-title":"Hypoxia-induced compression in the tracheal system in the caterpillar, Manduca sexta L","volume":"216","author":"Greenlee","year":"2013","journal-title":"Journal of Experimental Biology"},{"issue":"788","key":"10.7717\/peerj.13378\/ref-18","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1098\/rstb.1968.0004","article-title":"Further studies on the rectal complex of mealworm Tenebrio molitor, L. (Coleoptera, Tenebrionidae)","volume":"253","author":"Grimstone","year":"1968","journal-title":"Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences"},{"issue":"3","key":"10.7717\/peerj.13378\/ref-19","doi-asserted-by":"crossref","first-page":"434","DOI":"10.2307\/1935378","article-title":"Micrometeorology and energy exchange in two desert arthropods","volume":"51","author":"Hadley","year":"1970","journal-title":"Ecology"},{"key":"10.7717\/peerj.13378\/ref-20","doi-asserted-by":"publisher","first-page":"20190071","DOI":"10.1098\/rstb.2019.0071","article-title":"Visualization of insect metamorphosis","volume":"374","author":"Hall","year":"2019","journal-title":"Philosophical Transactions of the Royal Society of London B: Biological Sciences"},{"key":"10.7717\/peerj.13378\/ref-21","doi-asserted-by":"publisher","first-page":"160699","DOI":"10.1098\/rsos.160699","article-title":"The \u2018dance\u2019 of life: visualizing metamorphosis during pupation in the blow fly Calliphora vicina by X-ray video imaging and micro-computed tomography","volume":"4","author":"Hall","year":"2017","journal-title":"Royal Society Open Science"},{"key":"10.7717\/peerj.13378\/ref-22","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1146\/annurev.physiol.62.1.179","article-title":"Flight respiration and energetics","volume":"62","author":"Harrison","year":"2000","journal-title":"Annual Review of Physiology"},{"issue":"5","key":"10.7717\/peerj.13378\/ref-23","doi-asserted-by":"publisher","first-page":"521","DOI":"10.1016\/j.asd.2018.05.001","article-title":"Micro-computed tomography of pupal metamorphosis in the solitary bee Megachile rotundata","volume":"47","author":"Helm","year":"2018","journal-title":"Arthropod Structure and Development"},{"issue":"1","key":"10.7717\/peerj.13378\/ref-24","first-page":"11","article-title":"Brachyptery and aptery in Lepidoptera","volume":"2","author":"Heppner","year":"1991","journal-title":"Tropical Lepidoptera"},{"key":"10.7717\/peerj.13378\/ref-25","doi-asserted-by":"crossref","first-page":"2018","DOI":"10.1016\/j.asd.2015.02.002","article-title":"The last breath: a lCT-based method for investigating the tracheal system in Hexapoda","volume":"44","author":"Iwan","year":"2015","journal-title":"Arthropod Structure and Development"},{"issue":"32","key":"10.7717\/peerj.13378\/ref-26","doi-asserted-by":"publisher","first-page":"13198","DOI":"10.1073\/pnas.0611544104","article-title":"Increase in tracheal investment with beetle size supports hypothesis of oxygen limitation on insect gigantism","volume":"104","author":"Kaiser","year":"2007","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"10.7717\/peerj.13378\/ref-27","doi-asserted-by":"publisher","first-page":"825","DOI":"10.3161\/00034541ANZ2018.68.4.006","article-title":"Immature stages of beetles representing the \u2018Opatrinoid\u2019 clade (Coleoptera: Tenebrionidae): an overview of current knowledge of the pupal morphology","volume":"68","author":"Kami\u0144ski","year":"2018","journal-title":"Annales Zoologici"},{"key":"10.7717\/peerj.13378\/ref-28","first-page":"9","article-title":"Some aspects of abundant life in the vegetationless sand at the Namib Desert dunes","volume":"1","author":"Koch","year":"1961","journal-title":"Scientific Papers of the Namib Desert Research Station"},{"issue":"21","key":"10.7717\/peerj.13378\/ref-29","first-page":"3412","article-title":"The opening\u2013closing rhythms of the subelytral cavity associated with gas exchange patterns in diapausing Colorado potato beetle, Leptinotarsa decemlineata","volume":"219","author":"Kuusik","year":"2016","journal-title":"Journal of Experimental Biology"},{"key":"10.7717\/peerj.13378\/ref-30","doi-asserted-by":"publisher","first-page":"20130304","DOI":"10.1098\/rsif.2013.0304","article-title":"Metamorphosis revealed: time-lapse three dimensional imaging inside a living chrysalis","volume":"10","author":"Lowe","year":"2013","journal-title":"Journal of The Royal Society Interface"},{"issue":"49","key":"10.7717\/peerj.13378\/ref-31","doi-asserted-by":"publisher","first-page":"24729","DOI":"10.1073\/pnas.1909655116","article-title":"The evolution and genomic basis of beetle diversity","volume":"116","author":"McKenna","year":"2019","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"issue":"6210","key":"10.7717\/peerj.13378\/ref-32","doi-asserted-by":"publisher","first-page":"763","DOI":"10.1126\/science.1257570","article-title":"Phylogenomics resolves the timing and pattern of insect evolution","volume":"346","author":"Misof","year":"2014","journal-title":"Science"},{"key":"10.7717\/peerj.13378\/ref-33","doi-asserted-by":"publisher","first-page":"20141823","DOI":"10.1098\/rspb.2014.1823","article-title":"Fossil evidence for key innovations in the evolution of insect diversity","volume":"281","author":"Nicholson","year":"2014","journal-title":"Proceedings of the Royal Society B: Biological Sciences"},{"key":"10.7717\/peerj.13378\/ref-34","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1016\/j.ydbio.2006.09.022","article-title":"Tracheal development in the Drosophila brain is constrained by glial cells","volume":"302","author":"Perenau","year":"2007","journal-title":"Developmental Biology"},{"key":"10.7717\/peerj.13378\/ref-35","doi-asserted-by":"publisher","DOI":"10.7910\/DVN\/P1HRUQ","article-title":"Postembryonic development of the tracheal system of beetles in the context of aptery; supplementary material. Harvard Dataverse, V2","author":"Ra\u015b","year":"2020"},{"key":"10.7717\/peerj.13378\/ref-36","doi-asserted-by":"publisher","first-page":"997","DOI":"10.1111\/joa.12808","article-title":"The tracheal system in post-embryonic development of holometabolous insects: a case study using the mealworm beetle","volume":"232","author":"Ra\u015b","year":"2018","journal-title":"Journal of Anatomy"},{"key":"10.7717\/peerj.13378\/ref-37","article-title":"R: a language and environment for statistical computing","author":"R Core Team","year":"2017"},{"issue":"4","key":"10.7717\/peerj.13378\/ref-38","doi-asserted-by":"publisher","first-page":"389","DOI":"10.2307\/1943013","article-title":"The evolution of flightlessness in insects","volume":"60","author":"Roff","year":"1990","journal-title":"Ecological Monographs"},{"key":"10.7717\/peerj.13378\/ref-39","first-page":"1","article-title":"The Tenebrionidae of southern Africa, XXXIII. Description of the larvae of Gonopus tibialis Fabricius and Gonopus agrestis Fahraeus (Gonopina, sensu Koch 1956)","volume":"5","author":"Schulze","year":"1962","journal-title":"Cimbebasia"},{"key":"10.7717\/peerj.13378\/ref-40","first-page":"205","article-title":"mclust 5: clustering, classification and density estimation using Gaussian finite mixture models","volume":"8\/1","author":"Scrucca","year":"2016","journal-title":"The R Journal"},{"issue":"3\/4","key":"10.7717\/peerj.13378\/ref-41","doi-asserted-by":"publisher","first-page":"198","DOI":"10.1660\/062.112.0407","article-title":"The use of HMDS (hexamethyldisilazane) to replace Critical Point Drying (CPD) in the preparation of tardigrade for SEM (Scanning Electron Microscope) imaging","volume":"112","author":"Shively","year":"2009","journal-title":"Transactions of the Kansas Academy of Science"},{"key":"10.7717\/peerj.13378\/ref-42","doi-asserted-by":"publisher","first-page":"3409","DOI":"10.1242\/jeb.019877","article-title":"Correlated patterns of tracheal compression and convective gas exchange in a carabid beetle","volume":"211","author":"Socha","year":"2008","journal-title":"The Journal of Experimental Biology"},{"issue":"24","key":"10.7717\/peerj.13378\/ref-43","doi-asserted-by":"publisher","first-page":"7519","DOI":"10.1073\/pnas.1502408112","article-title":"New approaches narrow global species estimates for beetles, insects, and terrestrial arthropods","volume":"112","author":"Stork","year":"2015","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"10.7717\/peerj.13378\/ref-44","doi-asserted-by":"publisher","first-page":"R621","DOI":"10.1152\/ajpregu.00500.2012","article-title":"Dynamics of tracheal compression in the horned passalus beetle","volume":"304","author":"Waters","year":"2013","journal-title":"American Journal of Physiology-Regulatory, Integrative and Comparative Physiology"},{"issue":"1","key":"10.7717\/peerj.13378\/ref-45","first-page":"115","article-title":"Growth and regeneration in the tracheal system of an insect, rhodnius prolixus (Hemiptera)","volume":"95","author":"Wigglesworth","year":"1954","journal-title":"Quarterly Journal of Microscopical Science"},{"key":"10.7717\/peerj.13378\/ref-46","doi-asserted-by":"publisher","first-page":"501","DOI":"10.1016\/0040-8166(82)90043-X","article-title":"The supply of oxygen to the flight muscles of insects: a theory of tracheole physiology","volume":"14","author":"Wigglesworth","year":"1982","journal-title":"Tissue and Cell"},{"key":"10.7717\/peerj.13378\/ref-47","doi-asserted-by":"publisher","first-page":"50","DOI":"10.1111\/cla.12068","article-title":"The thorax of Mantophasmatodea, the morphology of flightlessness, and the evolution of the neopteran insects","volume":"31","author":"Wipfler","year":"2015","journal-title":"Cladistics"},{"issue":"1","key":"10.7717\/peerj.13378\/ref-48","doi-asserted-by":"publisher","first-page":"425","DOI":"10.1242\/jeb.157.1.425","article-title":"Routes of transpiratory water loss in a dry-habitat tenebrionid beetle","volume":"157","author":"Zachariassen","year":"1991","journal-title":"Journal of Experimental Biology"},{"key":"10.7717\/peerj.13378\/ref-49","first-page":"359","article-title":"The water conserving physiological compromise of desert insects","volume":"93","author":"Zachariassen","year":"1996","journal-title":"European Journal of Entomology"}],"container-title":["PeerJ"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/peerj.com\/articles\/13378.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/peerj.com\/articles\/13378.xml","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/peerj.com\/articles\/13378.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/peerj.com\/articles\/13378.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,11,24]],"date-time":"2023-11-24T09:15:19Z","timestamp":1700817319000},"score":1,"resource":{"primary":{"URL":"https:\/\/peerj.com\/articles\/13378"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,7,13]]},"references-count":49,"alternative-id":["10.7717\/peerj.13378"],"URL":"https:\/\/doi.org\/10.7717\/peerj.13378","archive":["CLOCKSS","LOCKSS","Portico"],"relation":{"has-review":[{"id-type":"doi","id":"10.7287\/peerj.13378v0.1\/reviews\/1","asserted-by":"object"},{"id-type":"doi","id":"10.7287\/peerj.13378v0.1\/reviews\/2","asserted-by":"object"},{"id-type":"doi","id":"10.7287\/peerj.13378v0.2\/reviews\/1","asserted-by":"object"}]},"ISSN":["2167-8359"],"issn-type":[{"value":"2167-8359","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,7,13]]},"article-number":"e13378"}}