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Body plan innovation in treehoppers through the evolution of an extra wing-like appendage


Body plans, which characterize the anatomical organization of animal groups of high taxonomic rank1, often evolve by the reduction or loss of appendages (limbs in vertebrates and legs and wings in insects, for example). In contrast, the addition of new features is extremely rare and is thought to be heavily constrained, although the nature of the constraints remains elusive2,3,4. Here we show that the treehopper (Membracidae) ‘helmet’ is actually an appendage, a wing serial homologue on the first thoracic segment. This innovation in the insect body plan is an unprecedented situation in 250 Myr of insect evolution. We provide evidence suggesting that the helmet arose by escaping the ancestral repression of wing formation imparted by a member of the Hox gene family, which sculpts the number and pattern of appendages along the body axis5,6,7,8. Moreover, we propose that the exceptional morphological diversification of the helmet was possible because, in contrast to the wings, it escaped the stringent functional requirements imposed by flight. This example illustrates how complex morphological structures can arise by the expression of ancestral developmental potentials and fuel the morphological diversification of an evolutionary lineage.

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Figure 1: Morphological diversity in treehoppers is conveyed by the helmet.
Figure 2: The helmet is a T1 dorsal appendage with a bilateral origin.
Figure 3: Wing-patterning genes are expressed in the developing helmet.
Figure 4: Scr and the evolution of T1 appendages.

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  1. Angelini, D. R. & Kaufman, T. C. Comparative developmental genetics and the evolution of arthropod body plans. Annu. Rev. Genet. 39, 95–119 (2005)

    Article  CAS  Google Scholar 

  2. Maynard Smith, J. et al. Developmental constraints and evolution. Q. Rev. Biol. 60, 265–287 (1985)

    Article  Google Scholar 

  3. Raff, R. A. The Shape of Life: Genes, Development, and the Evolution of Animal Form (Chicago Univ. Press, 1996)

    Book  Google Scholar 

  4. Riedl, R. A systems analytical approach to macroevolutionary phenomena. Q. Rev. Biol. 52, 351–370 (1977)

    Article  CAS  Google Scholar 

  5. Carroll, S. B., Weatherbee, S. D. & Langeland, J. A. Homeotic genes and the regulation and evolution of insect wing number. Nature 375, 58–61 (1995)

    Article  ADS  CAS  Google Scholar 

  6. Cohn, M. J. & Tickle, C. Developmental basis of limblessness and axial patterning in snakes. Nature 399, 474–479 (1999)

    Article  ADS  CAS  Google Scholar 

  7. Di-Poi¯, N. et al. Changes in Hox genes’ structure and function during the evolution of the squamate body plan. Nature 464, 99–103 (2010)

    Article  ADS  Google Scholar 

  8. Pavlopoulos, A. et al. Probing the evolution of appendage specialization by Hox gene misexpression in an emerging model crustacean. Proc. Natl Acad. Sci. USA 106, 13897–13902 (2009)

    Article  ADS  CAS  Google Scholar 

  9. Dietrich, C. H. Evolution of Cicadomorpha (Insecta, Hemiptera). Denisia 176, 155–170 (2002)

    Google Scholar 

  10. Fowler, W. W. in Biologia Centrali Americana Vol. II, Part 1 1–173 (Porter, 1894)

    Google Scholar 

  11. Poulton, E. B. in Monograph of the Membracidae (ed. Buckton, G. B. ) 273–285 (Lovell Reeve, 1903)

    Google Scholar 

  12. Stegmann, U. E. An exaggerated trait in insects: the prothoracic skeleton of Stictocephala bisonia (Homoptera: Membracidae). J. Morphol. 238, 157–178 (1998)

    Article  Google Scholar 

  13. Richter, L. El apendice pronotal en los Membracidos. Lozania 7, 1–4 (1953)

    Google Scholar 

  14. Boulard, M. Le pronotum des Membracides: camouflage sélectionné ou orthogenèse hypertélique? Bull. Mus. Hist. Nat. Paris (Zool.) 83, 145–165 (1973)

    Google Scholar 

  15. Snodgrass, R. E. Principles of Insect Morphology (McGraw-Hill, 1935)

    Google Scholar 

  16. Moczek, A. P., Rose, D., Sewell, W. & Kesselring, B. R. Conservation, innovation, and the evolution of horned beetle diversity. Dev. Genes Evol. 216, 655–665 (2006)

    Article  Google Scholar 

  17. Snodgrass, R. E. The thorax of insects and the articulation of the wings. Proc. US Nat. Mus. 36, 511–595, plts 540–569. (1909)

    Article  Google Scholar 

  18. Cifuentes, F. J. & Garcia-Bellido, A. Proximo-distal specification in the wing disc of Drosophila by the nubbin gene. Proc. Natl Acad. Sci. USA 94, 11405–11410 (1997)

    Article  ADS  CAS  Google Scholar 

  19. Averof, M. & Cohen, S. M. Evolutionary origin of insect wings from ancestral gills. Nature 385, 627–630 (1997)

    Article  ADS  CAS  Google Scholar 

  20. Grimaldi, D. & Engel, M. S. Evolution of the Insects (Cambridge Univ. Press, 2005)

    Google Scholar 

  21. Kukalová-Peck, J. Origin and evolution of insect wings and their relation to metamorphosis, as documented by the fossil record. J. Morphol. 156, 53–125 (1978)

    Article  Google Scholar 

  22. Beeman, R. W., Stuart, J. J., Haas, M. S. & Denell, R. E. Genetic analysis of the homeotic gene complex (HOM-C) in the beetle Tribolium castaneum . Dev. Biol. 133, 196–209 (1989)

    Article  CAS  Google Scholar 

  23. Chesebro, J., Hrycaj, S., Mahfooz, N. & Popadic, A. Diverging functions of Scr between embryonic and post-embryonic development in a hemimetabolous insect, Oncopeltus fasciatus. Dev. Biol. 329, 142–151 (2009)

    Article  CAS  Google Scholar 

  24. Rogers, B. T., Peterson, M. D. & Kaufman, T. C. Evolution of the insect body plan as revealed by the Sex combs reduced expression pattern. Development 124, 149–157 (1997)

    CAS  PubMed  Google Scholar 

  25. Tomoyasu, Y., Wheeler, S. R. & Denell, R. E. Ultrabithorax is required for membranous wing identity in the beetle Tribolium castaneum . Nature 433, 643–647 (2005)

    Article  ADS  CAS  Google Scholar 

  26. Brakefield, P. M. Evo-devo and constraints on selection. Trends Ecol. Evol. 21, 362–368 (2006)

    Article  Google Scholar 

  27. Poinar, G. & Poinar, R. The Amber Forest: A Reconstruction of a Vanished World (Princeton Univ. Press, 1999)

    Google Scholar 

  28. Comstock, J. H. The Wings of Insects (Comstock, 1918)

    Google Scholar 

  29. Darwin, C. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life (Murray, 1859)

    Google Scholar 

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We are grateful to G. Moraguès for inspiring the project and the loan of specimens. We thank S. B. Carroll for discussions and support during the early stage of the project; M. Morgan and S. Morgan for access to their field property; J. P. Chauvin for assistance with SEM; S. McKamey and C. Dietrich for help with bibliography; D. Milo for discussions; and D. Andrews, M. Averof, S. B. Carroll, A. Kopp, A. Salzberg and Y. Tomoyasu for sharing reagents. We used FlyBase for information support. We also thank F. Leulier, T. Lecuit, M. Averof, C. Desplan and S. B. Carroll for comments on the manuscript. This work was supported by a EURYI award, a Human Frontier Science Program Career Development Award and the CNRS. J.D.C. was supported by a Human Frontier Science Program Long-term fellowship.

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Authors and Affiliations



B.P. and N.G. conceived the project and designed the experiments; B.P., H.D.D., N.G. and V.A.K. collected Publilia specimens; B.P., C.M., J.D.C. and V.A.K. performed cloning; C.M., J.D.C., M.H. and N.G. did the immunostaining; and J.D.C., B.P. and N.G. carried out fly transgenesis and genetic experiments. A.A. made the histological sections, which were analysed by B.P. and N.G. N.G. and M.H. shot images and movies. N.G. made the anatomical dissections and observations. All authors participated in data analysis. B.P. and N.G. wrote the manuscript.

Corresponding authors

Correspondence to Benjamin Prud’homme or Nicolas Gompel.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Figures 1-9 with legends, Supplementary Table 1 and additional references. (PDF 5347 kb)

Supplementary Methods

The file contains Supplementary Methods and additional references. (PDF 103 kb)

Supplementary Movie 1

The movie shows flexibility of the helmet. The helmet of a living specimen of Publilia modesta is moved by the experimenter. The specimen is glued to a microscope slide by its helmet in the first part of the movie and then held with forceps. Note how the helmet returns to its initial position when relaxed, as a wing would. Also note how the wings are concealed under the helmet cavity. (MOV 13596 kb)

Supplementary Movie 2

The movie shows unfolding of the helmet upon emergence. The last (fifth) nymphal stage of a Publilia modesta specimen is emerging into an adult.The wings unfold first, as any insect wing would, presumably under the pressured hemolymph that the animal pumps into them. Then, the helmet unfolds likewise to completely cover the animal. The other specimen in the movie did not emerge successfully and remained caught in its nymphal shed. After the unfolding of all the dorsal appendages is complete the animals acquire their pigments. The entire process lasts about one hour. This video is accelerated 20 times. (MOV 12038 kb)

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Prud’homme, B., Minervino, C., Hocine, M. et al. Body plan innovation in treehoppers through the evolution of an extra wing-like appendage. Nature 473, 83–86 (2011).

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