BACKGROUND: The stem-group of Ephemeroptera is phylogenetically important for understanding key steps in evolutionary history of early pterygote insects. However, these taxa have been mostly studied from the taxonomy point of view focused on the pattern of wing venation and often using only classical optical microscopy devices. In-depth studies on detailed morphology of the different body structures are scarcely performed, although the results are critical for elucidation of life history traits and their evolutionary pattern among the basal pterygotes. RESULTS: New information is presented on the morphology of two species of Misthodotes, which are stem-mayflies from the Early Permian. Based on new results obtained from a re-examination of the type specimens and supplementary material, we infer the life history traits of both the adult and larval stages of these Palaeozoic insects and reconsider previous interpretations. For the first time, we report the structure of the thoracic pleura and the articulation at the base of the wing in a stem-group of Ephemeroptera and compare them with those of extant mayflies. We also provide additional support for the systematic placement of investigated taxa and an amended diagnosis of the genus Misthodotes. CONCLUSIONS: Adult Misthodotes sharovi and Misthodotes zalesskyi had chewing mouthparts, which enabled them to scavenge or feed on plants. The wing apparatus was adapted for slow powered flapping flight and gliding, using long caudal filaments for steering. The wing base does not have rows of articulary sclerites as previously hypothesized for some Palaeozoic taxa but inflexible axilla similar to that found in modern mayflies. The structure of the thoracic pleura is also similar to that in the crown group of Ephemeroptera, while differences in the course of sutures may be explained by an evolutionary trend towards more powerful dorsoventral flying musculature and forewing-based flight (anteromotorism) in modern taxa. There is no evidence for swarming behaviour and mating in the air as occurs in modern mayflies as they had none of the associated morphological adaptations. Putative larvae of Misthodotes can not be unambiguously associated with the adults. They also exhibit some morphological specializations of Protereismatidae like 9 pairs of abdominal tracheal gills supporting their benthic lifestyle with legs adapted to burrowing.

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

Department of Invertebrate Zoology and Hydrobiology University of Łódź Banacha 12 16 90237 Łódź Poland

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

Palaeontological Institute of the Russian Academy of Sciences Profsoyuznaya 123 Moscow Russia

State Museum of Natural History NASU Teatralna 18 Lviv Ukraine

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Aristov DS, Rasnitsyn AP. New insects from the Kungurian of Tshekarda fossil site in Permian Territory of Russia. Rus Entomol J. 2015;24(1):17–35. doi: 10.15298/rusentj.24.1.03. DOI

Aristov DS. The fauna of grylloblattid insects (Grylloblattida) of the lower permian locality of Tshekarda. Paleont J. 2004;38(2):80–145.

Bauernfeind E, Soldán T. The Mayflies of Europe (Ephemeroptera) Ollerup: Apollo Books; 2012. pp. 1–781.

Brodsky AK. Swarming behaviour of may-flies (Ephemeroptera) Entomol Rev. 1973;52(1):33–39.

Brodsky AK. Evolution of the wing apparatus in the Ephemeroptera. Entomol Rev. 1974;53(2):35–43.

Brodsky AK. The evolution of insect flight. New York: Oxford University Press; 1994. pp. 1–229.

Carpenter FM. Arthropoda 4, superclass Hexapoda. In: Moore RC, Kaesler RL, editors. Treatise on invertebrate paleontology. Colorado: The Geological Society of America and the University of Kansas; 1992. p. 1–655.

Carpenter FM. Lower Permian insects from Oklahoma. Part 2. Orders Ephemeroptera and Palaeodictyoptera. Psyche. 1979;86(2–3):261–90Carpenter FM. Lower Permian insects from Oklahoma. Part 2. Orders Ephemeroptera and Palaeodictyoptera. Psyche. 1979;86(2–3):261–90. 10.1155/1979/96359.

Carpenter FM. The Lower Permian insects of Kansas. Part 6. Delopteridae, Protelytroptera, Plectoptera and a new collection of Protodonata, Odonata, Megasecoptera, Homoptera and Psocoptera. Proc Am Acad Arts Sci. 1933;68:411–503.

Carpenter FM. The Lower Permian insects of Kansas. Part 8. Additional Megasecoptera, Protodonata, Odonata, Homoptera, Psocoptera, Protoelytroptera, Plectoptera, and Protoperlaria. Proc Am Acad Arts Sci. 1939;73:29–70.

Cianciara S. Stages and physiological periods in the development of Cloeon dipterum (L.) (Baetidae). In: Flannagan JF, Marshall KE, editors. Advances in Ephemeroptera biology. New York: Plenum Press; 1979. p. 265–76.

Corbet PS. Dragonflies: behavior and ecology of Odonata. New York: Cornell University Press, Comstock Publishing Associates; 1999. p. 1–829.

Demoulin G. Remarques sur les Ephéméroptères Misthodotidae d'Europe et sur leurs rapports avec les autres Ephéméroptères permiens. Bull Inst Roy Sci Natur Belg. 1966;42(15):1–5.

Edmunds GF, Jensen SL, Berner L. The mayflies of North and Central America. Minneapolis: Univ. of Minnesota Press; 1976. pp. 1–330.

Edmunds GF, McCafferty WP. The mayfly subimago. Annu Rev Entomol. 1988;33:509–529. doi: 10.1146/annurev.en.33.010188.002453. DOI

Engel MS, Davis SR, Prokop J. Insect wings: the evolutionary development of nature’s first flyers. In: Minelli A, et al., editors. Arthropod biology and evolution. Berlin: Springer-Verlag; 2013. p. 269–98.

Handlirsch A. Die fossilen Insekten und die Phylogenie der rezenten Formen. Ein Handbuch für Paläontologen und Zoologen. Leipzig: Engelman, V.W. publ.; 1906-1908. p. 1–1430.

Handlirsch A. Geschichte, literatur, technik, palaeontologie, phylogenie, systematik. In: Schröder C, editor. Handbuch der entomologie, geschichte, literatur, technik, paläontologie, phylogenie, systematik. Jena: Gustav Fisher; 1925. pp. 117–306.

Handlirsch A. Über einige insektenreste aus der Permformation Russlands. Zapiski Imperatorskoj Akademii nauk. 1904;16(5):1–7.

Hubbard MD, Kukalová-Peck J. Permian mayfly nymphs: new taxa and systematic characters. In: Flannagan JF, Marshall KE, editors. Advances in Ephemeroptera biology. New York: Plenum Press; 1980. pp. 19–31.

Hubbard MD. Ephemeroptera fossilium catalogus. I: Animalia. 1987;129:1–99.

Kinzelbach R, Lutz H. Eine neue Eintagsfliege Misthodotes stapfi n. sp. aus dem Rotliegenden des Nahe-Gebietes (Ephemeroptera: Permoplectoptera: Misthodotidae). Palaeont Z. 1984;58(3/4):247–53.

Kluge NJ, Novikova EA, Brodsky AK. Movements of larvae of the Ephemeroptera during swimming, respiration and cleaning. Zool Zh. 1984;63(9):1345–1354.

Kluge NJ, Sinitshenkova ND. Order Ephemerida Latreille 1810. The true mayflies (= Ephemeroptera Hyatt et Arms 1892 (s.l.); = Euephemeroptera Kluge, 2000) In: Rasnitsyn AP, Quicke DLJ, editors. History of insects. Dordrecht: Kluwer Academic Publishers; 2002. pp. 89–97.

Kluge NJ. Pterothorax structure of mayflies (Ephemeroptera) and its use in systematics. Bull Soc Entomol France. 1994;99(1):41–61.

Kluge NJ. The phylogenetic system of Ephemeroptera. Dordrecht: Kluwer Acad Publ; 2004. pp. 1–442.

Kukalová J. Permian mayfly nymphs. Psyche. 1968;75(4):310–327. doi: 10.1155/1968/904597. DOI

Kukalová-Peck J, Brauckmann C. Wing folding in pterygote insects, and the oldest Diaphanopterodea from the early Late Carboniferous of West Germany. Can J Zool. 1990;68:1104–1111. doi: 10.1139/z90-163. DOI

Kukalová-Peck J, Peters JG, Soldán T. Homologisation of the anterior articular plate in the wing base of Ephemeroptera and Odonatoptera. Aquatic Insects. 2009;31(1):459–470. doi: 10.1080/01650420903024389. 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

Kukalová-Peck J. Pteralia of the Paleozoic insect orders Palaeodictyoptera, Megasecoptera and Diaphanopterodea (Paleoptera) Psyche. 1974;81:416–430. doi: 10.1155/1974/23457. DOI

Ninomiya T, Yoshizawa K. A revised interpretation of the wing base structure in Odonata. Syst Entomol. 2009;34:334–345. doi: 10.1111/j.1365-3113.2008.00455.x. DOI

Palmer ChM, Yeates DK. Diet and feeding behavior in adults of the apteropanorpidae (Mecoptera) J Insect Behav. 2005;18(2):209–231. doi: 10.1007/s10905-005-0476-9. DOI

Pecharová M, Prokop J. The morphology of mouthparts, wings and genitalia of Paleozoic insect families Protohymenidae and Scytohymenidae reveals new details and supposed function. Arthropod Struct Dev. 2018;47(1):117–129. doi: 10.1016/j.asd.2017.11.006. PubMed DOI

Ponomaryova GYU, Novokshonov VG, Naugolnykh SV. Tshekarda—a locality of permian fossil plants and insects. Perm: Perm University; 1998. pp. 1–92.

Prokop J, Nel A, Tenny A. On the phylogenetic position of the palaeopteran Syntonopteroidea (Insecta: Ephemeroptera), with a new species from the Upper Carboniferous of England. Org Divers Evol. 2010;10:331–340. doi: 10.1007/s13127-010-0022-2. DOI

Prokop J, Pecharová M, Nel A, Hörnschemeyer T. The wing base of the palaeodictyopteran genus Dunbaria Tillyard: Where are we now? Arthropod Struct Dev. 2018;47(4):339–351. doi: 10.1016/j.asd.2018.04.002. PubMed DOI

Prokop J, Pecharová M, Ren D. Hidden surface microstructures on Carboniferous insect Brodioptera sinensis (Megasecoptera) enlighten functional morphology and sensorial perception. Sci Rep. 2016;6:28316. doi: 10.1038/srep28316. PubMed DOI PMC

Prokop J, Pecharová M, Sinitshenkova ND, Klass KD. Male postabdomen reveals ancestral traits of Megasecoptera among winged insects. Arthropod Struct Dev. 2020;57:100944. doi: 10.1016/j.asd.2020.100944. PubMed DOI

Sartori M, Brittain JE. Chapter 34. Order Ephemeroptera. In: Thorp J, Rogers DC, editors. Ecology and general biology: Thorp and Covich's freshwater invertebrates. Cambridge: Academic Press; 2015. pp. 873–891.

Savolainen E, Saura A, Hantula J. Mode of swarming in relation to reproductive isolation in mayflies. Evol. 1993;47(6):1796–1804. doi: 10.2307/2410222. PubMed DOI

Sellards EH. Types of Permian insects. Part 3: Megasecoptera, Oryctoblattinidae Protorthoptera. Am J Sci Wash. 1909;4(27):151–8173. doi: 10.2475/ajs.s4-27.158.151. DOI

Sinitshenkova ND, Vasilenko DV. The latest record of mayflies of the family Protereismatidae Sellards (Ephemerida = Ephemeroptera) and a new species of the family misthodotidae in the Upper Permian of Europe. Paleont J. 2012;46(1):61–65. doi: 10.1134/S0031030112010121. DOI

Sinitshenkova ND, Marchal-Papier F, Grauvogel-Stamm L, Gall J-C. The Ephemeridea (Insecta) from the Grès à Voltzia (early Middle Triassic) of the Vosges (NE France) Paläontol Z. 2005;79(3):377–397. doi: 10.1007/BF02991930. DOI

Sinitshenkova ND. New mayflies (Insecta: Ephemerida = Ephemeroptera) from the Upper Permian locality of Isady Northern European Russia. Paleontol J. 2013;47(2):162–5. 10.1134/S0031030113020135.

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

Staniczek AH, Bechly G, Godunko RJ. Coxoplectoptera, a new fossil order of Palaeoptera (Arthropoda: Insecta), with comments on the phylogeny of the stem group of mayflies (Ephemeroptera) Insect Syst Evol. 2011;42:101–138. doi: 10.1163/187631211X578406. DOI

Tillyard RJ. Kansas Permian nsects. Part 15. The order Plectoptera. Am J Sci. 1932;23:97–134. doi: 10.2475/ajs.s5-23.134.97. DOI

Tshernova OA. Some fossil mayflies (Ephemeroptera Misthodotidae) from Permian-beds of the urals (in Russian) Entomol Obozr. 1965;44(2):353–361.

Tshernova OA. The order Ephemerida Latreille, 1810 in historical development of the class Insecta (in Russian). Tr Paleont inst Akad N SSSR. 1980;175:31–6.

Willkommen J, Hörnschemeyer T. The homology of wing base sclerites and flight muscles in Ephemeroptera and Neoptera and the morphology of the pterothorax of Habroleptoides confusa (Insecta: Ephemeroptera: Leptophlebiidae) Arthropod Struct Dev. 2007;36:253–269. doi: 10.1016/j.asd.2007.01.003. PubMed DOI

Willkommen J. The morphology of the pterothorax of Ephemeroptera, Odonata and Plecoptera (Insecta) and the homology of wing base sclerites and flight muscles. Stutt Beitr Naturkund. 2008;1:203–300. PubMed

Willmann R. Advances and problems in insect phylogeny. In: Fortey RA, Thomas RH, editors. Arthropod relationships (systematics association, Special Volume Series 55) London: Chapman & Hall; 1998. pp. 269–279.

Willmann R. Die Stammgruppenvertreter der Ephemeroptera und ihre systematische Stellung (Insecta) Species, Phyl Evol. 2007;1(2):109–128.

Wootton RJ, Kukalová-Peck J. Flight adaptations in Palaeozoic Palaeoptera (Insecta) Biol Rev. 2000;75:129–167. doi: 10.1017/S0006323199005459. PubMed DOI

Wootton RJ. Function, homology and terminology in insect wing. Syst Entomol. 1979;4:81–93. doi: 10.1111/j.1365-3113.1979.tb00614.x. DOI

Nebesna sotnia gen. & sp. nov. from Baltic amber supports a Pangean distribution of the amphinotic family Ameletopsidae (Ephemeroptera)

Thoracic and abdominal outgrowths in early pterygotes: a clue to the common ancestor of winged insects?