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The earliest known holometabolous insects

Nature volume 503, pages 257–261 (2013)Cite this article

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Abstract

The Eumetabola (Endopterygota (also known as Holometabola) plus Paraneoptera)1 have the highest number of species of any clade, and greatly contribute to animal species biodiversity2,3. The palaeoecological circumstances that favoured their emergence and success remain an intriguing question3,4,5,6. Recent molecular phylogenetic analyses have suggested a wide range of dates for the initial appearance of the Holometabola, from the Middle Devonian epoch (391 million years (Myr) ago) to the Late Pennsylvanian epoch (311 Myr ago7,8,9,10,11,12), and Hemiptera (310 Myr ago13). Palaeoenvironments greatly changed over these periods, with global cooling and increasing complexity of green forests14. The Pennsylvanian-period crown-eumetabolan fossil record remains notably incomplete15,16,17,18,19, particularly as several fossils have been erroneously considered to be stem Holometabola1,15,20,21 (Supplementary Information); the earliest definitive beetles are from the start of the Permian period21,22. The emergence of the hymenopterids, sister group to other Holometabola, is dated between 350 and 309 Myr ago8,9,12, incongruent with their current earliest record (Middle Triassic epoch)1,20. Here we describe five fossils— a Gzhelian-age stem coleopterid, a holometabolous larva of uncertain ordinal affinity, a stem hymenopterid, and early Hemiptera and Psocodea, all from the Moscovian age—and reveal a notable penecontemporaneous breadth of early eumetabolan insects. These discoveries are more congruent with current hypotheses of clade divergence. Eumetabola experienced episodes of diversification during the Bashkirian–Moscovian and the Kasimovian–Gzhelian ages. This cladogenetic activity is perhaps related to notable episodes of drying resulting from glaciations, leading to the eventual demise in Euramerica of coal-swamp ecosystems, evidenced by floral turnover during this interval23,24. These ancient species were of very small size, living in the shadow of Palaeozoic-era ‘giant’ insects. Although these discoveries reveal unexpected Pennsylvanian eumetabolan diversity, the lineage radiated more successfully only after the mass extinctions at the end of the Permian period, giving rise to the familiar crown groups of their respective clades.

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Figure 1: Representatives of stem hymenopterids and stem coleopterids.
Figure 2: Holometabolous larva and representatives of stem Psocodea and Euhemiptera.
Figure 3: Phylogeny of main insect clades.
Figure 4: Comparison of the sizes of Carboniferous fossil Pterygota and extant Pterygota.

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Acknowledgements

We thank C. C. Labandeira for comments on the first version of the manuscript that helped to improve the paper. We are grateful to A. P. Rasnitsyn, S. I. Golovach and B. R. Striganova, M. Fikáček, A.A. Przhiboro, R. Beutel, T. Hörnschemeyer and V. Krassilov for early discussions. C. Garrouste and P. A. Kirejtshuk assisted in the preparation of illustrations for this publication. Financial support was provided by the Grant Agency of the Czech Republic no. P210/10/0633 (to J.P.) and the German Science Foundation WA 1492/6-1 (to T.W.). The study was supported by the program for visiting researchers and professors of the Smithsonian Institution National Museum of Natural History (NMNH) and partly carried out within the framework of the program of the Presidium of the Russian Academy of Sciences ‘Problems of the origin of life and formation of the biosphere’. A.A.P. and A.G.K. were supported by the Russian Foundation of Basic Research (grant 12-04-00663-a). This paper is a participation to the team project ‘Biodiversity: Origin, Structure, Evolution and Geology’ allotted to D.A. by the Lebanese University.

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Authors and Affiliations

  1. CNRS UMR 7205, Muséum National d’Histoire Naturelle, CP 50, Entomologie, 45 Rue Buffon, Paris F-75231, France,

    André Nel, Patrick Roques, Patricia Nel, Thierry Bourgoin, Dany Azar, Laure Desutter-Grandcolas, Romain Garrouste, David Coty & Alexander G. Kirejtshuk

  2. Département Sciences de la Vie et Santé, AgroParisTech, 16 rue Claude Bernard, Paris Cedex 05 F-75231, France,

    Patricia Nel

  3. Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, Borok, Nekouzsky District, Yaroslavl Oblast 152742, Russia,

    Alexander A. Prokin

  4. Department of Zoology, Charles University in Prague, Faculty of Science, Viničná 7, CZ-128 44, Praha 2, Czech Republic,

    Jakub Prokop

  5. Department of Palaeozoology, Museum and Institute of Zoology, Polish Academy of Sciences, 64, Wilcza Street, Warszawa PL00-679, Poland,

    Jacek Szwedo

  6. Department of Natural Sciences, Lebanese University, Faculty of Sciences II, Fanar, Fanar – MatnP.O. Box 26110217, Lebanon,

    Dany Azar

  7. Steinmann-Institut für Geologie, Mineralogie und Paläontologie, Universität Bonn, Nussallee 8, Bonn 53115, Germany,

    Torsten Wappler

  8. State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, 210008, China

    Diying Huang

  9. Division of Entomology, Natural History Museum, University of Kansas, Lawrence, 66045, Kansas, USA

    Michael S. Engel

  10. Department of Ecology & Evolutionary Biology, University of Kansas, Lawrence, 66045, Kansas, USA

    Michael S. Engel

  11. Zoological Institute of the Russian Academy of Sciences, 1 Universitetskaya Embankment, Saint Petersburg 199034, Russia,

    Alexander G. Kirejtshuk

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  1. André Nel
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Contributions

A.N., P.R., P.N., A.A.P., T.B., J.P., J.S., D.A., R.G., D.C., D.H., M.S.E. and A.G.K. participated in morphological studies and prepared the manuscript. P.N. and D.C. prepared the figures. P.R. discovered the fossils. The authors of the taxonomic data are associated with the names of the species in the Supplementary Information. A.N. designed the program. M.S.E. and A.G.K. are last authors with equal rank.

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Correspondence to André Nel.

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Extended data figures and tables

Extended Data Figure 1 Representative of the stem hymenopterids, Avioxyela gallica gen. et sp. nov.

a, Photograph of counterpart. b, Reconstruction of forewing based on part and counterpart. CuA, cubitus anterior; CuP, cubitus posterior; MA, median anterior; MP, median posterior; R, radius; RA, radius anterior; RP, radius posterior; ScP, subcosta posterior. Scale bar, 1 mm (a, b).

Extended Data Figure 2 Representative of the stem hymenopterids, Avioxyela gallica gen. et sp. nov., electron scanning photograph.

a, Two wings partly overlapping. b, Reconstruction of the two forewings. c, Mirror of the second wing to show the identity of pattern with the first wing. d, e, Electron scanning photograph of radial vein of second wing with interpretation of the veins. Scale bar, 1 mm (a, b, c).

Extended Data Figure 3 Representative of the stem coleopterids, Stephanastus polinae gen. et sp. nov.

Electron scanning photographs. a, Foreleg and pronotum. b, Mid-leg. Scale bar, 1 mm (a, b).

Extended Data Figure 4 Holometabolous larva, Metabolarva bella gen. et sp. nov.

Photograph of posterior half of body. Scale bar, 1 mm.

Extended Data Figure 5 Representative of stem Euhemiptera, Aviorrhyncha magnifica gen. et sp. nov.

a, Photograph of part. b, Electron scanning photograph of counterpart. AA1 + 2, first anal anterior vein; AA3 + 4, second anal anterior vein; PC, precosta. Scale bar, 1 mm (a, b).

Extended Data Figure 6 Euhemiptera wing venation.

a, Wing base of Aviorrhyncha magnifica gen. et sp. nov. b, Wing base of a modern Fulgoroidea. Scale bar, 1 mm (a, b).

Extended Data Figure 7 Representative of stem Psocodea, Westphalopsocus pumilio gen. et sp. nov.

a, Reconstruction of forewing. b, Photograph. A, anal veins. Scale bar, 1 mm (a, b).

Extended Data Figure 8 Very small forewing of a dictyopteran from Avion. Specimen Avion 13.

Scale bar, 1 mm.

Supplementary information

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Nel, A., Roques, P., Nel, P. et al. The earliest known holometabolous insects. Nature 503, 257–261 (2013). https://doi.org/10.1038/nature12629

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