Loss and recovery of wings in stick insects (2024)

  • Letter
  • Published: 16 January 2003
  • Michael F. Whiting1,
  • Sven Bradler2 &
  • Taylor Maxwell3

Nature volume421,pages 264–267 (2003)Cite this article

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Abstract

The evolution of wings was the central adaptation allowing insects to escape predators, exploit scattered resources, and disperse into new niches, resulting in radiations into vast numbers of species1. Despite the presumed evolutionary advantages associated with full-sized wings (macroptery), nearly all pterygote (winged) orders have many partially winged (brachypterous) or wingless (apterous) lineages, and some entire orders are secondarily wingless (for example, fleas, lice, grylloblattids and mantophasmatids), with about 5% of extant pterygote species being flightless2,3. Thousands of independent transitions from a winged form to winglessness have occurred during the course of insect evolution; however, an evolutionary reversal from a flightless to a volant form has never been demonstrated clearly for any pterygote lineage. Such a reversal is considered highly unlikely because complex interactions between nerves, muscles, sclerites and wing foils are required to accommodate flight4. Here we show that stick insects (order Phasmatodea) diversified as wingless insects and that wings were derived secondarily, perhaps on many occasions. These results suggest that wing developmental pathways are conserved in wingless phasmids, and that ‘re-evolution’ of wings has had an unrecognized role in insect diversification.

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References

  1. Hennig, W. Insect Phylogeny (Academic, New York, 1981)

    Google Scholar

  2. Roff, D. A. The evolution of flightlessness: is history important? Evol. Ecol. 8, 639–657 (1994)

    Article Google Scholar

  3. Wagner, D. L. & Liebherr, J. K. Flightlessness in insects. Trends Ecol. Evol. 7, 216–220 (1992)

    Article CAS Google Scholar

  4. Dudley, R. The Biomechanics of Insect Flight (Princeton Univ. Press, Princeton, New Jersey, 2000)

    Google Scholar

  5. Tilgner, E. H., Kiselyova, T. G. & McHugh, J. V. A morphological study of Timema cristinae Vickery with implications for the phylogenetics of Phasmida. Dtsch. Entomol. Z. 46, 149–162 (1999)

    Article Google Scholar

  6. Kristensen, N. P. in The insects of Australia: A textbook for Students and Research Workers, 2nd edn (eds Naumann, I. D. et al.) 125–140 (CSIRO, Melbourne Univ. Press, Melbourne, 1991)

    Google Scholar

  7. Hennig, W. Die Stammesgeschichte der Insekten (Krammer, Frankfurt am Main, Germany, 1969)

    Google Scholar

  8. Wheeler, W. C., Whiting, M. F., Wheeler, Q. D. & Carpenter, J. M. The phylogeny of the extant hexapod orders. Cladistics 17, 113–169 (2001)

    Article Google Scholar

  9. Kamp, J. W. Numerical classification of the orthopteroids, with special reference to the Grylloblattodea. Can. Entomol. 105, 1235–1249 (1973)

    Article Google Scholar

  10. Beutel, R. G. & Gorb, S. N. Ultrastructure of attachment specializations of Hexapods (Arthropoda): evolutionary patterns inferred from a revised ordinal phylogeny. J. Zool Syst. Evol. Res. 39, 177–207 (2001)

    Article Google Scholar

  11. Whiting, M. F., Carpenter, J. C., Wheeler, Q. D. & Wheeler, W. C. The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Syst. Biol. 46, 1–68 (1997)

    CAS PubMed Google Scholar

  12. Günther, K. Über die taxonomische Gliederung und geographische Verbreitung der Insektenordnung der Phasmatodea. Beitr. Ent. 3, 541–563 (1953)

    Google Scholar

  13. Bradler, S. The Australian stick insects—a monophyletic group within the Phasmatodea? Zoology 104, 69 (2001)

    Google Scholar

  14. Pagel, M. The maximum likelihood approach to reconstructing ancestral characters states of discrete characters on phylogenies. Syst. Biol. 48, 612–622 (1999)

    Article Google Scholar

  15. Kim, J. et al. Integration of positional information and identity by Drosophila vestigial gene. Nature 382, 133–138 (1996)

    Article ADS CAS Google Scholar

  16. Cohen, B., Simcox, A. A. & Cohen, S. M. Allocation of the thoracic imaginal primordia in the Drosophila embryo. Development 117, 597–608 (1993)

    CAS PubMed Google Scholar

    See Also
    What animals have 6 wings?

  17. Kutsch, W. & Kittman, R. Flight motor pattern in flying and non-flying Phasmida. J. Comp. Physiol. 168, 483–490 (1991)

    Article Google Scholar

  18. Halder, G., Callaerts, P. & Gehring, W. J. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 167, 1788–1792 (1995)

    Article ADS Google Scholar

  19. Anderson, N. M. in The Origin of Biodiversity in Insects: Phylogenetic Tests of Evolutionary Scenarios (ed. Grandcolas, P.) 91–108, (Mem. Mus. Natl Hist. Nat., Paris, 1997)

    Google Scholar

  20. Colgan, D. J. et al. Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Aust. J. Zool. 46, 419–437 (1998)

    Article Google Scholar

  21. Whiting, M. F. Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zoologica Scripta 31, 93–104 (2002)

    Article Google Scholar

  22. Whiting, M. F. in Molecular Systematics and Evolution: Theory and Practice (eds DeSalle, R., Wheeler, W. C. & Giribet, G.) 69–84 (Birkhauser, Basel, 2002)

    Book Google Scholar

  23. Wheeler, W. Fixed character states and the optimization of molecular sequence data. Cladistics 15, 379–386 (1999)

    Article Google Scholar

  24. Swofford, D. L. PAUP*: Phylogenetic analysis using parsimony (*and other methods) (version 4.0b10) (Sinauer, Sunderland, Massachusetts, 2000)

  25. Sorenson, M. D. TreeRot (version 2) (Boston Univ. Press, Massachusetts, 1999)

  26. Farris, J. S., Kallersjo, M., Kluge, A. G. & Bult, C. Testing significance of incongruence. Cladistics 10, 315–320 (1994)

    Article Google Scholar

  27. Maddison, D. R. & Maddison, W. P. MacClade 4: Analysis of phylogeny and character evolution (version 4) (Sinauer, Sunderland, Massachusetts, 2000)

  28. Pagel, M. Discrete (Univ. Reading Press, Reading, UK, 1999)

  29. Lutzoni, F., Pagel, M. & Reeb, V. Major fungal lineages are derived from lichen symbiotic ancestors. Nature 411, 937–940 (2001)

    Article ADS CAS Google Scholar

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Acknowledgements

We thank E. Tilgner for providing some specimens; A. Whiting and L. Harmon for assistance in data analysis; and J. Cherry, M. Gruwell, M. Terry, H. Ogden, J. Robertson and K. Jarvis for generating sequence data. Analyses were performed in the Fulton Supercomputer Center, Brigham Young University, and parallel software implementation was performed by M. Clement and Q. Snell. DNA sequences are deposited in GenBank under accession numbers AY121129–AY121186 and AY125216–AY125326.

Author information

Authors and Affiliations

  1. Department of Integrative Biology, Brigham Young University, Provo, Utah, 84602, USA

    Michael F. Whiting

  2. Institut für Zoologie und Anthropologie, Georg August Universität, Göttingen, Germany

    Sven Bradler

  3. Department of Biology, Washington University, St Louis, Missuori, 63130, USA

    Taylor Maxwell

Authors

  1. Michael F. Whiting

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  2. Sven Bradler

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  3. Taylor Maxwell

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Corresponding author

Correspondence to Michael F. Whiting.

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The authors declare that they have no competing financial interests.

Supplementary information

41586_2003_BFnature01313_MOESM1_ESM.pdf

Supplementary Figure 1: This is the ingroup portion of the Bayesian tree, with posterior probabilities given above nodes, and the probability that the ancestral state was wingless given below the node. This reconstruction requires 5 independent wing gains and 2 wing losses. (PDF 60 kb)

41586_2003_BFnature01313_MOESM2_ESM.doc

Supplementary Information: This file provides additional details concerning taxon selection, optimization alignment methodology, incongruence length difference metrics, parsimony tree reconstruction, likelihood tree reconstruction, Bayesian analysis, congruence of molecular results with known morphological characters, parsimony character mapping, and likelihood character mapping. (DOC 168 kb)

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Whiting, M., Bradler, S. & Maxwell, T. Loss and recovery of wings in stick insects. Nature 421, 264–267 (2003). https://doi.org/10.1038/nature01313

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Loss and recovery of wings in stick insects (2024)
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