Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Loss and recovery of wings in stick insects

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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Examples of wing features in stick insects, a, Example of a fully winged (macropterous) female phasmid (Phasma gigas) with enlarged hindwings and thickened forewings.
Figure 2: Phylogeny of Phasmatodea on the basis of molecular data.
Figure 3: Character mapping of wing types on phasmid phylogeny.

References

  1. 1

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

    Google Scholar 

  2. 2

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

    Article  Google Scholar 

  3. 3

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

    CAS  Article  Google Scholar 

  4. 4

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

    Google Scholar 

  5. 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. 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. 7

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

    Google Scholar 

  8. 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. 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. 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. 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. 12

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

    Google Scholar 

  13. 13

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

    Google Scholar 

  14. 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. 15

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

    ADS  CAS  Article  Google Scholar 

  16. 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 

  17. 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. 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)

    ADS  Article  Google Scholar 

  19. 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. 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. 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. 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. 23

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

    Article  Google Scholar 

  24. 24

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

  25. 25

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

  26. 26

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

    Article  Google Scholar 

  27. 27

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

  28. 28

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

  29. 29

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

    ADS  CAS  Article  Google Scholar 

Download references

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

Affiliations

Authors

Corresponding author

Correspondence to Michael F. Whiting.

Ethics declarations

Competing interests

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)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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

Download citation

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.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing