One of the fundamental questions in insect evolution is the origin of their wings and primary function of ancestral wing precursors. Recent phylogenomic and comparative morphological studies broadly support a terrestrial ancestor of pterygotes, but an aquatic or semiaquatic ancestor cannot be ruled out. Here new features of the branchial system of palaeodictyopteran larvae of several different instars of Katosaxoniapteron brauneri gen. et sp. nov. (Eugereonoidea) from the late Carboniferous collected at Piesberg (Germany) are described, which consist of delicate dorsolateral and lamellate caudal abdominal gills that support an aquatic or at least semiaquatic lifestyle for these insects. Moreover, the similar form and surface microstructures on the lateral abdominal outgrowths and thoracic wing pads indicate that paired serial outgrowths on segments of both tagmata presumably functioned as ancestral type of gills resembling a protopterygote model. This is consistent with the hypothesis that the wing sheaths of later stage damselfly larvae in hypoxic conditions have a respiratory role similar to abdominal tracheal gills. Hence, the primary function and driving force for the evolution of the precursors of wing pads and their abdominal homologues could be respiration.

Department of Zoology Faculty of Science Charles University Viničná 7 128 00 Praha 2 Czech Republic

Institute of Entomology Biology Centre of the Czech Academy of Sciences Branišovská 31 370 05 České Budějovice Czech Republic

Museum Schölerberg Klaus Strick Weg 10 49082 Osnabrück Germany

Erratum In

Commun Biol. 2024 Jan 25;7(1):128. doi: 10.1038/s42003-024-05803-8. PubMed

See more in PubMed

Clark-Hachtel CM, Tomoyasu Y. Exploring the origin of insect wings from an evo-devo perspective. Curr. Opin. Insect Sci. 2016;13:77–85. doi: 10.1016/j.cois.2015.12.005. PubMed DOI

Ohde T, Mito T, Niimi T. A hemimetabolous wing development suggests the wing origin from lateral tergum of a wingless ancestor. Nat. Commun. 2022;13:979. doi: 10.1038/s41467-022-28624-x. PubMed DOI PMC

Hasenfuss I. The evolutionary pathway to insect flight - a tentative reconstruction. Arthropod Syst. Phyl. 2008;66:19–35. doi: 10.3897/asp.66.e31678. DOI

Marden JH, Kramer MG. Surface-skimming stoneflies: a possible intermediate stage in insect flight evolution. Science. 1994;266:427. doi: 10.1126/science.266.5184.427. PubMed DOI

Averof M, Cohen SM. Evolutionary origin of insect wings from ancestral gills. Nature. 1997;385:627–630. doi: 10.1038/385627a0. PubMed DOI

Franch-Marro X, Martín N, Averof M, Casanova J. Association of tracheal placodes with leg primordia in Drosophila and implications for the origin of insect tracheal systems. Development. 2006;133:785–790. doi: 10.1242/dev.02260. PubMed DOI

Tomoyasu Y. What crustaceans can tell us about the evolution of insect wings and other morphologically novel structures. Curr. Opin. Genet. Dev. 2021;69:48–55. doi: 10.1016/j.gde.2021.02.008. PubMed DOI

Wipfler B, et al. Evolutionary history of Polyneoptera and its implications for our understanding of early winged insects. Proc. Natl Acad. Sci. USA. 2019;116:3024–3029. doi: 10.1073/pnas.1817794116. PubMed DOI PMC

Sharma PP. Integrating morphology and phylogenomics supports a terrestrial origin of insect flight. Proc. Natl Acad. Sci. USA. 2019;116:2796–2798. doi: 10.1073/pnas.1822087116. PubMed DOI PMC

Carpenter, F. M. in Treatise on Invertebrate Paleontology, Part R, Arthropoda 4 Vols. 3 and 4 (eds Moore, R. C. & Kaesler, R. L.) 1-655 (The Geological Society of America and the University of Kansas, 1992).

Engel, M. S., Davis, S. R. & Prokop, J. in Arthropod Biology and Evolution - Molecules, Development, Morphology (eds Minelli A., Boxshall G. & Fusco G.) Ch. XII (Springer, 2013).

Prokop J, Nel A, Engel MS. Diversity, form, and postembryonic development of Paleozoic insects. Annu. Rev. Entomol. 2023;68:401–429. doi: 10.1146/annurev-ento-120220-022637. PubMed DOI

Sroka P, Staniczek AH, Bechly G. Revision of the giant pterygote insect Bojophlebia prokopi Kukalová-Peck, 1985 (Hydropalaeoptera: Bojophlebiidae) from the Carboniferous of the Czech Republic, with the first cladistic analysis of fossil palaeopterous insects. J. Syst. Palaeont. 2015;13:963–982. doi: 10.1080/14772019.2014.987958. DOI

Prokop J, Engel MS. Palaeodictyopterida. Curr. Biol. 2019;29:R306–R309. doi: 10.1016/j.cub.2019.02.056. PubMed DOI

Lancaster, J. & Downes, B. J. Aquatic Entomology (Oxford University Press, 2013).

Kukalová-Peck J. Carboniferous protodonatoid dragonfly nymphs and the synapomorphies of Odonatoptera and Ephemeroptera (Insecta: Palaeoptera) Palaeodiversity. 2009;2:169–198.

Sroka P, Godunko RJ, Sinitshenkova ND, Prokop J. Life history, systematics and flight ability of the Early Permian stem-mayflies in the genus Misthodotes Sellards, 1909 (Insecta, Ephemerida, Permoplectoptera) BMC Ecol. Evol. 2021;21:97. doi: 10.1186/s12862-021-01820-x. PubMed DOI PMC

Hennig, W. Insect Phylogeny (Wiley, 1981).

Sinitshenkova, N. D. in History of Insects (eds Rasnitsyn, A. P. & Quicke, D. L. J.) Ch. 2.2.2.2.2 (Kluwer Academic Publishers, 2002).

Brauckmann C, Schneider J. Ein unter-karbonisches Insekt aus dem Raum Bitterfeld/Delitz (Pterygota, Arnsbergium, Deutschland) N. Jb. Geol. Paläont. Mh. 1996;1996:17–30.

Brongniart C. Recherches pour servir à l’histoire des insectes fossiles des temps primaires précédées d’une étude sur la nervation des ailes des insectes. Bull. Soc. Ind. Minéral. St.-Etienne. 1893;3:1–491.

Handlirsch, A. Die Fossilen Insekten und die Phylogenie der rezenten Formen. Ein Handbuch für Paläontologen und Zoologen (Engelman V.W. Publ., 1906).

Lameere A. Révision sommaire des insectes fossiles du Stéphanien de Commentry. Bull. Mus. Nat. Hist. Natur. 1917;23:141–200.

Kukalová -Peck J. Origin and evolution of insect wings and their relation to metamorphosis, as documented by the fossil record. J. Morphol. 1978;156:53–126. doi: 10.1002/jmor.1051560104. PubMed DOI

Prokop J, et al. Ecomorphological diversification of the Late Palaeozoic Palaeodictyopterida reveals different larval strategies and amphibious lifestyle in adults. R. Soc. Open Sci. 2019;6:190460. doi: 10.1098/rsos.190460. PubMed DOI PMC

Prokop J, Pecharová M, Jarzembowski EA, Ross AJ. New palaeodictyopterans from the Late Carboniferous of the UK (Insecta: Palaeodictyopterida) Earth Environ. Sci. Trans. R. Soc. Edinb. 2018;107:99–107.

Wootton RJ. Nymphs of Palaeodictyoptera (Insecta) from the Westphalian of England. Palaeontology. 1972;15:662–675.

Prokop J, Nel A, Engel MS, Pecharová M, Hörnschemeyer T. New Carboniferous fossils of Spilapteridae enlighten postembryonic wing development in Palaeodictyoptera. Syst. Entomol. 2016;41:178–190. doi: 10.1111/syen.12148. DOI

Kiesmüller C, Hörnig MK, Leipner A, Haug C, Haug JT. Palaeozoic palaeodictyopteran insect nymphs with prominent ovipositors from a new locality. Bull. Geosci. 2019;94:23–40. doi: 10.3140/bull.geosci.1717. DOI

Hamilton KGA. The insect wing, Part 1. Origin and development of wings from notal lobes. J. Kans. Entomol. Soc. 1971;44:421–433.

Prokop J, et al. Paleozoic nymphal wing pads support dual model of insect wing origins. Curr. Biol. 2017;27:263–269. doi: 10.1016/j.cub.2016.11.021. PubMed DOI

Rosová K, Sinitshenkova ND, Prokop J. Evidence for wing development in the Late Palaeozoic Palaeodictyoptera revisited. Arthropod Struct. Dev. 2021;63:101061. doi: 10.1016/j.asd.2021.101061. PubMed DOI

Prokop J, Ren D. New significant fossil insects from the Upper Carboniferous of Ningxia in northern China (Palaeodictyoptera, Archaeorthoptera) Eur. J. Entomol. 2007;104:267–275. doi: 10.14411/eje.2007.041. DOI

Brauckmann C, Herd KJ, Leipner A. Insekten-Funde aus dem Westfalium D (Ober-Karbon) des Piesberges bei Osnabrück (Deutschland). Nachtrag 1: Palaeodictyopteroida. Osnabrücker Naturwiss. Mitteil. 2009;35:1–30.

Brauckmann, C. Herd, K. J. & Leipner, A. First Eugereonidae (Insecta: Palaeodictyoptera) from the Pennsylvanian (Late Carboniferous) of the Piesberg site near Osnabrück, Germany. PalZ10.1007/s12542-021-00578-3 (2021).

Rosová K, Pecharová M, Leipner A, Prokop J. New palaeodictyopterid insects from the Pennsylvanian of Piesberg uncover spectacular disparity of wing venation patterns (Megasecoptera, Palaeodictyoptera) Hist. Biol. 2023;35:152–162. doi: 10.1080/08912963.2021.2025229. DOI

Rolfe WDI. Rochdalia, a Carboniferous insect nymph (Palaeodictyoptera) Palaeontology. 1967;10:307–313.

Wootton RJ. The historical ecology of aquatic insects: an overview. Palaeogr. Palaeoclimol. Palaeoecol. 1988;62:477–492. doi: 10.1016/0031-0182(88)90068-5. DOI

Hutchinson EG. Thoughts on aquatic insects. Bioscience. 1981;31:495–500. doi: 10.2307/1308491. DOI

Kukalová-Peck J. Origin of the insect wing and wing articulation from the arthropodan leg. Can. J. Zool. 1983;61:1618–1669. doi: 10.1139/z83-217. DOI

Prokop J, et al. Abdominal serial homologues of wings in Paleozoic insects. Curr. Biol. 2022;32:3414–3422. doi: 10.1016/j.cub.2022.06.024. PubMed DOI

Merritt, R. W. & Cummins, K. W. An Introduction to the Aquatic Insects of North America (Kendall/Hunt Publishing Co., 1978).

Wigglesworth VB, Rainey RC. Chapter 13. The evolution of insect flight. Insect Flight Symp. R. Entomol. Soc. 1976;7:255–269.

Kluge, N. Y. The Phylogenetic System of Ephemeroptera (Kluwer Publishers, 2004).

Almudi I, et al. Genomic adaptations to aquatic and aerial life in mayflies and the origin of insect wings. Nat. Commun. 2020;11:2631. doi: 10.1038/s41467-020-16284-8. PubMed DOI PMC

Norling U. Structure and ontogeny of the lateral abdominal gills and the caudal gills in Euphaeidae (Odonata: Zygoptera) larvae. Zool. Jahrb. Abt. Anat. Ontog. Tierre. 1982;107:343–389.

Rowe RJ. Ontogeny of agonistic behaviour in the territorial damselfly larvae, Xanthocnemis zealandica (Zygoptera: Coenagrionidae) J. Zool. 1992;226:81–93. doi: 10.1111/j.1469-7998.1992.tb06128.x. DOI

Tillyard RJ. On the morphology of the caudal gills of the larvae of zygopterid dragonflies. Proc. Linn. Soc. N. S. W. 1917;42:606–632.

Tillyard, R. J. The Biology of Dragonflies (Odonata or Paraneuroptera) (Cambridge University Press, 1917).

Corbet, P. S. Dragonflies: Behavior and Ecology of Odonata (Comstock Publishing Associates, Cornell University Press, 1999).

Sinitshenkova ND. A new family of the Palaeodictyoptera from the Carboniferous of Siberia. Paleont. J. 1979;13:192–205.

Kukalová J. Revisional study of the order Palaeodictyoptera in the Upper Carboniferous shales of Commentry, France. Part 2. Psyche. 1969;76:439–486. doi: 10.1155/1969/20732. DOI

Zahner R. Über die Bindung der mitteleuropäischen Calopteryx-Arten (Odonata, Zygoptera) an den Lebensraum des strömenden Wassers. Intern. Rev. Gesam. Hydrobiol. Hydrogr. 1959;45:101–123. doi: 10.1002/iroh.19600450106. DOI

Brauer F. Ansichten über die paläozoischen Insekten und deren Deutung. Ann. Naturhist. Mus. Wien. 1886;1:87–126.

Shear WA, Kukalová-Peck J. The ecology of Paleozoic terrestrial arthropods: the fossil evidence. Can. J. Zool. 1989;68:1807–1834. doi: 10.1139/z90-262. DOI

Kingsolver JG, Koehl MAR. Selective factors in the evolution of insect wings. Annu. Rev. Entomol. 1994;39:425–451. doi: 10.1146/annurev.en.39.010194.002233. DOI

Simon S, Blanke A, Meusemann K. Reanalyzing the Palaeoptera problem – the origin of insect flight remains obscure. Arthropod Struct. Dev. 2018;47:328e338. doi: 10.1016/j.asd.2018.05.002. PubMed DOI

Rasnitsyn, A. P. in History of Insects (eds Rasnitsyn, A. P. & Quicke, D. L. J.) Ch. 2.1 (Kluwer Academic, 2002).

Kukalová-Peck J. Ephemeroid wing venation based upon new gigantic Carboniferous mayflies and basis morphological phylogeny and metamorphosis of pterygopte insects (Insecta, Ephemerida) Can. J. Zool. 1985;63:933–955. doi: 10.1139/z85-139. DOI

Staniczek AH, Sroka P, Bechly G. Neither silverfish nor fowl: the enigmatic Carboniferous Carbotriplura kukalovae Kluge, 1996 (Insecta: Carbotriplurida) is the putative fossil sister group of winged insects (Insecta: Pterygota) Syst. Entomol. 2015;39:619–632. doi: 10.1111/syen.12076. DOI

Štys P, Soldán T. Retention of tracheal gills in adult Ephemeroptera and other insects. Acta Univ. Carol. Biol. 1980;1978:409–435.

Sroka P, Staniczek AH. Retention of cervical and abdominal gills in the adult of a new fossil stonefly (Insecta, Plecoptera, Petroperlidae) from mid-Cretacous Burmese amber. Cret. Res. 2020;107:104277. doi: 10.1016/j.cretres.2019.104277. DOI

Wootton, R. J. & Ellington, C. P. in Biomechanics and Evolution (eds Rayner, J. M. V. & Wootton, R. J.) 99–112 (Cambridge Univ. Press, 1991).

Ross A. Evolution: the origin of insect wings revisited. Curr. Biol. 2022;32:R851–R852. doi: 10.1016/j.cub.2022.06.087. PubMed DOI

Marden JH, Kramer MG. Locomotor performance of insects with rudimentary wings. Nature. 1995;377:332–334. doi: 10.1038/377332a0. DOI

Marden JH, Thomas MA. Rowing locomotion by a stonefly that possesses the ancestral pterygote condition of co-occurring wings and abdominal gills. Biol. J. Linn. Soc. 2003;79:341–349. doi: 10.1046/j.1095-8312.2003.00192.x. DOI

Guillermo-Ferreira R, Appel E, Urban P, Bispo PC, Gorb SN. The unusual tracheal system within the wing membrane of a dragonfly. Biol. Lett. 2017;13:20160960. doi: 10.1098/rsbl.2016.0960. PubMed DOI PMC

Kukalová J. Permian mayfly nymphs. Psyche. 1968;75:311–327.

Demoulin G. Remarques critiques sur des larves “éphéméromorphes” du Permien. Bull. Mus. R. Hist. Nat. Belg. 1970;46:1–10.

Leipner A, Fischer T, Chellouche P. The Piesberg: a NW-German site of international importance for the Pennsylvanian (Late Carboniferous) Geoconserv. Res. 2021;4:218–234.

Brauckmann C, Herd KJ. Insekten-Funde aus dem Westfalium D (Ober-Karbon) des Piesberges bei Osnabrück (Deutschland). Teil 1: Palaeoptera. Osnabrücker Naturwiss. Mitteil. 2002;28:27–69.

Brauckmann C, Herd KJ. Insekten-Funde aus dem Westfalium D (Ober-Karbon) des Piesberges bei Osnabrück (Deutschland). Teil 2: Neoptera. Osnabrücker Naturwiss. Mitteil. 2005;30:19–65.