Subjects

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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    & Evolution of the Insects. (Cambridge Univ. Press, 2005)

  2. 2.

    & in The Timetree of Life (eds & ) 260–263 (Oxford University Press, 2009)

  3. 3.

    Why are there so many insect species? Perspectives from fossils and phylogenies. Biol. Rev. Camb. Philos. Soc. 82, 425–454 (2007)

  4. 4.

    Evolutionary contrasts in insects: nutritional advantages of holometabolous development. Physiol. Entomol. 11, 377–382 (1986)

  5. 5.

    Modularity, evolvability, and adaptive radiations: a comparison of the hemi- and holometabolous insects. Evol. Dev. 3, 59–72 (2001)

  6. 6.

    & Clade age and not diversification rate explains species richness among animal taxa. Am. Nat. 169, E97–E106 (2007)

  7. 7.

    et al. Dating the arthropod tree based on large-scale transcriptome data. Mol. Phylogenet. Evol. 61, 880–887 (2011)

  8. 8.

    , & Exploring uncertainty in the calibration of the molecular clock. Biol. Lett. 8, 156–159 (2012)

  9. 9.

    et al. Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. BMC Biol. 7, 34 (2009)

  10. 10.

    , & A view from the edge of the forest: recent progress in understanding the relationships of the insect orders. Aust. J. Entomol. 51, 79–87 (2012)

  11. 11.

    & Phylogenomic insights into the Cambrian explosion, the colonization of land and the evolution of flight in Arthropoda. Syst. Biol. 62, 93–109 (2013)

  12. 12.

    et al. A total-evidence approach to dating with fossils, applied to the early radiation of the Hymenoptera. Syst. Biol. 61, 973–999 (2012)

  13. 13.

    & A preliminary molecular phylogeny of planthoppers (Hemiptera: Fulgoroidea) based on nuclear and mitochondrial DNA sequences. PLoS ONE 8, e58400 (2013)

  14. 14.

    , , & Diversification of land plants: insights from a family-level phylogenetic analysis. BMC Evol. Biol. 11, 341 (2011)

  15. 15.

    et al. Traits and evolution of wing venation pattern in paraneopteran insects. J. Morphol. 273, 480–506 (2012)

  16. 16.

    et al. The earliest holometabolous insect: a “crucial” innovation with delayed success (Insecta Protomeropina Protomeropidae). Ann. Soc. Entomol. Fr. (NS) 43, 349–355 (2007)

  17. 17.

    et al. From Carboniferous to recent: wing venation enlightens evolution of thysanopteran lineage. J. Syst. Palaeontology 10, 385–399 (2012)

  18. 18.

    Evidence for an earliest Late Carboniferous divergence time and the early larval ecology and diversification of major Holometabola lineages. Entomol. Amer. 117, 9–21 (2011)

  19. 19.

    & The smallest Neoptera (Baryshnyalidae fam. n.) from Hagen-Vorhalle (early Late Carboniferous: Namurian B; Germany). ZooKeys 130, 91–102 (2011)

  20. 20.

    & History of Insects (Kluwer, 2002)

  21. 21.

    & Is the Carboniferous †Adiphlebia lacoana really the “oldest beetle”? Critical reassessment and description of a new Permian beetle family. Eur. J. Entomol. 109, 633–645 (2012)

  22. 22.

    et al. Evolution of the elytral venation and structural adaptations in the oldest Palaeozoic beetles (Insecta: Coleoptera: Tshekardocoleidae). J. Syst. Palaeontology (in the press)

  23. 23.

    , & in The Geologic Time Scale (eds , , & ) 603–651 (Elsevier, 2012)

  24. 24.

    & Changing patterns of Pennsylvanian coal-swamp vegetation and implications of climatic control on coal occurrence. Int. J. Coal Geol. 3, 205–255 (1984)

  25. 25.

    et al. A complete insect from the Late Devonian period. Nature 488, 82–85 (2012)

  26. 26.

    & Relationships among coleopteran suborders and major endoneopteran lineages: evidence from hind wing characters. Eur. J. Entomol. 101, 95–144 (2004)

  27. 27.

    & The entomofauna of the Lower Permian fossil insect beds of Kansas and Oklahoma, USA. Afr. Invertebr. 48, 23–39 (2007)

  28. 28.

    & The evolution of large size: how does Cope’s Rule work? Trends Ecol. Evol. 20, 4–6 (2005)

  29. 29.

    & Body size variation in insects: a macroecological perspective. Biol. Rev. Camb. Philos. Soc. 85, 139–169 (2010)

  30. 30.

    & Environmental and biotic controls on the evolutionary history of insect body size. Proc. Natl Acad. Sci. USA 109, 10927–10930 (2012)

Download references

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.

Author information

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. AgroParisTech, Département Sciences de la Vie et Santé, 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. Charles University in Prague, Faculty of Science, Department of Zoology, 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. Lebanese University, Faculty of Sciences II, Department of Natural Sciences, 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, Kansas 66045, USA

    • Michael S. Engel
  10. Department of Ecology & Evolutionary Biology, University of Kansas, Lawrence, Kansas 66045, USA

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

    • Alexander G. Kirejtshuk

Authors

  1. Search for André Nel in:

  2. Search for Patrick Roques in:

  3. Search for Patricia Nel in:

  4. Search for Alexander A. Prokin in:

  5. Search for Thierry Bourgoin in:

  6. Search for Jakub Prokop in:

  7. Search for Jacek Szwedo in:

  8. Search for Dany Azar in:

  9. Search for Laure Desutter-Grandcolas in:

  10. Search for Torsten Wappler in:

  11. Search for Romain Garrouste in:

  12. Search for David Coty in:

  13. Search for Diying Huang in:

  14. Search for Michael S. Engel in:

  15. Search for Alexander G. Kirejtshuk in:

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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to André Nel.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Text and Supplementary References.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature12629

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.