Chemical usurpation of a nest by paper wasp parasites

Science

Volumn 272, Issue 5263, 1996, Pages 889-892

  Bagnères, Anne Geneviève ^a   Lorenzi, Maria Cristina ^b   Dusticier, Georges ^a   Turillazzi, Stefano ^c   Clément, Jean Luc ^a  

^a UPR 9024   (France)

^b UNIVERSITY OF TURIN   (Italy)

^c UNIVERSITY OF FLORENCE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALKENE;

ARTICLE; CUTICLE; GAS CHROMATOGRAPHY; MASS SPECTROMETRY; PARASITE; PRIORITY JOURNAL; WASP;

POLISTES ATRIMANDIBULARIS; HYMENOPTERA; POLISTES BIGLUMIS BIMACULATUS;

CHEMICAL SIGNATURE; NEST USURPATION; PAPER WASP; PARASITE; SOCIAL PARASITE;

EID: 0029668495     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.272.5263.889     Document Type: Article

References (50)

1. The colonial cycle of P. biglumis bimaculatus is subjected to rigid climatic conditions because it occurs at high altitude (∼1800 m) near Montgenèvre in the French Alps where the colonies were collected.
2. M.-C. Lorenzi and S. Turillazzi, Ecol. Entomol. 11, 199 (1986); M.-C. Lorenzi, R. Cervo, S. Turillazzi, Ethol. Ecol. Evol. Special Issue 1, 45 (1991).
3. M.-C. Lorenzi and S. Turillazzi, Ecol. Entomol. 11, 199 (1986); M.-C. Lorenzi, R. Cervo, S. Turillazzi, Ethol. Ecol. Evol. Special Issue 1, 45 (1991).
4. R. Cervo, M.-C. Lorenzi, S. Turillazzi, Insectes Soc. 37, 333 (1990).
5. G. J. Gamboa, H. K. Reeves, D. Ferguson, T. L. Wacker, Anim. Behav. 34, 685 (1986); G. J. Gamboa, in Natural History and Evolution of Paper Wasps, S. Turillazzi and M. J. West-Eberhard, Eds. (Oxford Univ. Press, New York, 1996), chap. 9.
6. G. J. Gamboa, H. K. Reeves, D. Ferguson, T. L. Wacker, Anim. Behav. 34, 685 (1986); G. J. Gamboa, in Natural History and Evolution of Paper Wasps, S. Turillazzi and M. J. West-Eberhard, Eds. (Oxford Univ. Press, New York, 1996), chap. 9.
7. Polistes biglumis bimaculatus has a specific and colonial chemical signature [M.-C. Lorenzi, A.-G. Bagnères, J.-L. Clément, S. Turillazzi, Insectes Soc., in preparation] that, unlike that of P. atrimandibularis, does not depend on social environment, as can be seen in this work.
8. A.-G. Bagnères, A. Killian, J.-L. Clément, C. Lange, J. Chem. Ecol. 17, 2397 (1991); A. Bonavita-Cougourdan, J.-L. Clément, C. Lange, J. Entomol. Sci. 22, 1 (1987); K. E. Espelie, J. W. Wenzel, G. Chang, J. Chem. Ecol. 16, 2229 (1990); R. W. Howard, in Insect Lipids: Chemistry, Biochemistry and Biology, D. W. Stanley-Samuelson and D. R. Nelson, Eds. (Univ. Nebraska Press, Lincoln, NE, and London, 1993), pp. 179-225.
9. A.-G. Bagnères, A. Killian, J.-L. Clément, C. Lange, J. Chem. Ecol. 17, 2397 (1991); A. Bonavita-Cougourdan, J.-L. Clément, C. Lange, J. Entomol. Sci. 22, 1 (1987); K. E. Espelie, J. W. Wenzel, G. Chang, J. Chem. Ecol. 16, 2229 (1990); R. W. Howard, in Insect Lipids: Chemistry, Biochemistry and Biology, D. W. Stanley-Samuelson and D. R. Nelson, Eds. (Univ. Nebraska Press, Lincoln, NE, and London, 1993), pp. 179-225.
10. A.-G. Bagnères, A. Killian, J.-L. Clément, C. Lange, J. Chem. Ecol. 17, 2397 (1991); A. Bonavita-Cougourdan, J.-L. Clément, C. Lange, J. Entomol. Sci. 22, 1 (1987); K. E. Espelie, J. W. Wenzel, G. Chang, J. Chem. Ecol. 16, 2229 (1990); R. W. Howard, in Insect Lipids: Chemistry, Biochemistry and Biology, D. W. Stanley-Samuelson and D. R. Nelson, Eds. (Univ. Nebraska Press, Lincoln, NE, and London, 1993), pp. 179-225.
11. A.-G. Bagnères, A. Killian, J.-L. Clément, C. Lange, J. Chem. Ecol. 17, 2397 (1991); A. Bonavita-Cougourdan, J.-L. Clément, C. Lange, J. Entomol. Sci. 22, 1 (1987); K. E. Espelie, J. W. Wenzel, G. Chang, J. Chem. Ecol. 16, 2229 (1990); R. W. Howard, in Insect Lipids: Chemistry, Biochemistry and Biology, D. W. Stanley-Samuelson and D. R. Nelson, Eds. (Univ. Nebraska Press, Lincoln, NE, and London, 1993), pp. 179-225.
12. A. Bonavita-Cougourdan, J.-L. Clément, C. Lange, Sociobiology 16, 49 (1989); A. Bonavita-Cougourdan et al., Comp. Biochem. Physiol. B 110, 667 (1991); A. Bonavita-Cougourdan et al., ibid., in press.
13. A. Bonavita-Cougourdan, J.-L. Clément, C. Lange, Sociobiology 16, 49 (1989); A. Bonavita-Cougourdan et al., Comp. Biochem. Physiol. B 110, 667 (1991); A. Bonavita-Cougourdan et al., ibid., in press.
14. A. Bonavita-Cougourdan, J.-L. Clément, C. Lange, Sociobiology 16, 49 (1989); A. Bonavita-Cougourdan et al., Comp. Biochem. Physiol. B 110, 667 (1991); A. Bonavita-Cougourdan et al., ibid., in press.
15. Natural heterospecific colonies: R. W. Howard, C. A. McDaniel, G. J. Blomquist, Science 210, 431 (1980); Psyche 89, 157 (1982); R. W. Howard, R. D. Akre, W. B. Gamett, Ann. Entomol. Soc. Am. 83, 607 (1990); R. K. Vander Meer and D. P. Wojcik, Science 218, 806 (1982); R. K. Vander Meer, D. P. Jouvenaz, D. P. Wojcik, J. Chem. Ecol. 15, 2247 (1989); N. Franks, M. S. Blum, R. K. Smith, A. B. Allies, ibid. 16, 1431 (1990); K. Dettner and C. Liepert, Annu. Rev. Entomol. 39, 129 (1994); C. Uepert and K. Dettner, J. Chem. Ecol. 19, 2143 (1993). Artificial heterospecific colonies: A.-G. Bagnères, C. Errard, C. Mulheim, C. Joulie, C. Lange, J. Chem. Ecol. 17, 1641 (1991); B. Vauchot, E. Provost, A.-G. Bagnères, J.-L. Clément, J. Insect. Physiol. 42, 309 (1996). Unlike natural heterospecific colonies, the mixed signature in experimental models results from the addition of the two signatures and seems to be poorly regulated probably because of the lack of genetic programming.
16. Natural heterospecific colonies: R. W. Howard, C. A. McDaniel, G. J. Blomquist, Science 210, 431 (1980); Psyche 89, 157 (1982); R. W. Howard, R. D. Akre, W. B. Gamett, Ann. Entomol. Soc. Am. 83, 607 (1990); R. K. Vander Meer and D. P. Wojcik, Science 218, 806 (1982); R. K. Vander Meer, D. P. Jouvenaz, D. P. Wojcik, J. Chem. Ecol. 15, 2247 (1989); N. Franks, M. S. Blum, R. K. Smith, A. B. Allies, ibid. 16, 1431 (1990); K. Dettner and C. Liepert, Annu. Rev. Entomol. 39, 129 (1994); C. Uepert and K. Dettner, J. Chem. Ecol. 19, 2143 (1993). Artificial heterospecific colonies: A.-G. Bagnères, C. Errard, C. Mulheim, C. Joulie, C. Lange, J. Chem. Ecol. 17, 1641 (1991); B. Vauchot, E. Provost, A.-G. Bagnères, J.-L. Clément, J. Insect. Physiol. 42, 309 (1996). Unlike natural heterospecific colonies, the mixed signature in experimental models results from the addition of the two signatures and seems to be poorly regulated probably because of the lack of genetic programming.
17. Natural heterospecific colonies: R. W. Howard, C. A. McDaniel, G. J. Blomquist, Science 210, 431 (1980); Psyche 89, 157 (1982); R. W. Howard, R. D. Akre, W. B. Gamett, Ann. Entomol. Soc. Am. 83, 607 (1990); R. K. Vander Meer and D. P. Wojcik, Science 218, 806 (1982); R. K. Vander Meer, D. P. Jouvenaz, D. P. Wojcik, J. Chem. Ecol. 15, 2247 (1989); N. Franks, M. S. Blum, R. K. Smith, A. B. Allies, ibid. 16, 1431 (1990); K. Dettner and C. Liepert, Annu. Rev. Entomol. 39, 129 (1994); C. Uepert and K. Dettner, J. Chem. Ecol. 19, 2143 (1993). Artificial heterospecific colonies: A.-G. Bagnères, C. Errard, C. Mulheim, C. Joulie, C. Lange, J. Chem. Ecol. 17, 1641 (1991); B. Vauchot, E. Provost, A.-G. Bagnères, J.-L. Clément, J. Insect. Physiol. 42, 309 (1996). Unlike natural heterospecific colonies, the mixed signature in experimental models results from the addition of the two signatures and seems to be poorly regulated probably because of the lack of genetic programming.
18. Natural heterospecific colonies: R. W. Howard, C. A. McDaniel, G. J. Blomquist, Science 210, 431 (1980); Psyche 89, 157 (1982); R. W. Howard, R. D. Akre, W. B. Gamett, Ann. Entomol. Soc. Am. 83, 607 (1990); R. K. Vander Meer and D. P. Wojcik, Science 218, 806 (1982); R. K. Vander Meer, D. P. Jouvenaz, D. P. Wojcik, J. Chem. Ecol. 15, 2247 (1989); N. Franks, M. S. Blum, R. K. Smith, A. B. Allies, ibid. 16, 1431 (1990); K. Dettner and C. Liepert, Annu. Rev. Entomol. 39, 129 (1994); C. Uepert and K. Dettner, J. Chem. Ecol. 19, 2143 (1993). Artificial heterospecific colonies: A.-G. Bagnères, C. Errard, C. Mulheim, C. Joulie, C. Lange, J. Chem. Ecol. 17, 1641 (1991); B. Vauchot, E. Provost, A.-G. Bagnères, J.-L. Clément, J. Insect. Physiol. 42, 309 (1996). Unlike natural heterospecific colonies, the mixed signature in experimental models results from the addition of the two signatures and seems to be poorly regulated probably because of the lack of genetic programming.
19. Natural heterospecific colonies: R. W. Howard, C. A. McDaniel, G. J. Blomquist, Science 210, 431 (1980); Psyche 89, 157 (1982); R. W. Howard, R. D. Akre, W. B. Gamett, Ann. Entomol. Soc. Am. 83, 607 (1990); R. K. Vander Meer and D. P. Wojcik, Science 218, 806 (1982); R. K. Vander Meer, D. P. Jouvenaz, D. P. Wojcik, J. Chem. Ecol. 15, 2247 (1989); N. Franks, M. S. Blum, R. K. Smith, A. B. Allies, ibid. 16, 1431 (1990); K. Dettner and C. Liepert, Annu. Rev. Entomol. 39, 129 (1994); C. Uepert and K. Dettner, J. Chem. Ecol. 19, 2143 (1993). Artificial heterospecific colonies: A.-G. Bagnères, C. Errard, C. Mulheim, C. Joulie, C. Lange, J. Chem. Ecol. 17, 1641 (1991); B. Vauchot, E. Provost, A.-G. Bagnères, J.-L. Clément, J. Insect. Physiol. 42, 309 (1996). Unlike natural heterospecific colonies, the mixed signature in experimental models results from the addition of the two signatures and seems to be poorly regulated probably because of the lack of genetic programming.
20. Natural heterospecific colonies: R. W. Howard, C. A. McDaniel, G. J. Blomquist, Science 210, 431 (1980); Psyche 89, 157 (1982); R. W. Howard, R. D. Akre, W. B. Gamett, Ann. Entomol. Soc. Am. 83, 607 (1990); R. K. Vander Meer and D. P. Wojcik, Science 218, 806 (1982); R. K. Vander Meer, D. P. Jouvenaz, D. P. Wojcik, J. Chem. Ecol. 15, 2247 (1989); N. Franks, M. S. Blum, R. K. Smith, A. B. Allies, ibid. 16, 1431 (1990); K. Dettner and C. Liepert, Annu. Rev. Entomol. 39, 129 (1994); C. Uepert and K. Dettner, J. Chem. Ecol. 19, 2143 (1993). Artificial heterospecific colonies: A.-G. Bagnères, C. Errard, C. Mulheim, C. Joulie, C. Lange, J. Chem. Ecol. 17, 1641 (1991); B. Vauchot, E. Provost, A.-G. Bagnères, J.-L. Clément, J. Insect. Physiol. 42, 309 (1996). Unlike natural heterospecific colonies, the mixed signature in experimental models results from the addition of the two signatures and seems to be poorly regulated probably because of the lack of genetic programming.
21. Natural heterospecific colonies: R. W. Howard, C. A. McDaniel, G. J. Blomquist, Science 210, 431 (1980); Psyche 89, 157 (1982); R. W. Howard, R. D. Akre, W. B. Gamett, Ann. Entomol. Soc. Am. 83, 607 (1990); R. K. Vander Meer and D. P. Wojcik, Science 218, 806 (1982); R. K. Vander Meer, D. P. Jouvenaz, D. P. Wojcik, J. Chem. Ecol. 15, 2247 (1989); N. Franks, M. S. Blum, R. K. Smith, A. B. Allies, ibid. 16, 1431 (1990); K. Dettner and C. Liepert, Annu. Rev. Entomol. 39, 129 (1994); C. Uepert and K. Dettner, J. Chem. Ecol. 19, 2143 (1993). Artificial heterospecific colonies: A.-G. Bagnères, C. Errard, C. Mulheim, C. Joulie, C. Lange, J. Chem. Ecol. 17, 1641 (1991); B. Vauchot, E. Provost, A.-G. Bagnères, J.-L. Clément, J. Insect. Physiol. 42, 309 (1996). Unlike natural heterospecific colonies, the mixed signature in experimental models results from the addition of the two signatures and seems to be poorly regulated probably because of the lack of genetic programming.
22. Natural heterospecific colonies: R. W. Howard, C. A. McDaniel, G. J. Blomquist, Science 210, 431 (1980); Psyche 89, 157 (1982); R. W. Howard, R. D. Akre, W. B. Gamett, Ann. Entomol. Soc. Am. 83, 607 (1990); R. K. Vander Meer and D. P. Wojcik, Science 218, 806 (1982); R. K. Vander Meer, D. P. Jouvenaz, D. P. Wojcik, J. Chem. Ecol. 15, 2247 (1989); N. Franks, M. S. Blum, R. K. Smith, A. B. Allies, ibid. 16, 1431 (1990); K. Dettner and C. Liepert, Annu. Rev. Entomol. 39, 129 (1994); C. Uepert and K. Dettner, J. Chem. Ecol. 19, 2143 (1993). Artificial heterospecific colonies: A.-G. Bagnères, C. Errard, C. Mulheim, C. Joulie, C. Lange, J. Chem. Ecol. 17, 1641 (1991); B. Vauchot, E. Provost, A.-G. Bagnères, J.-L. Clément, J. Insect. Physiol. 42, 309 (1996). Unlike natural heterospecific colonies, the mixed signature in experimental models results from the addition of the two signatures and seems to be poorly regulated probably because of the lack of genetic programming.
23. Natural heterospecific colonies: R. W. Howard, C. A. McDaniel, G. J. Blomquist, Science 210, 431 (1980); Psyche 89, 157 (1982); R. W. Howard, R. D. Akre, W. B. Gamett, Ann. Entomol. Soc. Am. 83, 607 (1990); R. K. Vander Meer and D. P. Wojcik, Science 218, 806 (1982); R. K. Vander Meer, D. P. Jouvenaz, D. P. Wojcik, J. Chem. Ecol. 15, 2247 (1989); N. Franks, M. S. Blum, R. K. Smith, A. B. Allies, ibid. 16, 1431 (1990); K. Dettner and C. Liepert, Annu. Rev. Entomol. 39, 129 (1994); C. Uepert and K. Dettner, J. Chem. Ecol. 19, 2143 (1993). Artificial heterospecific colonies: A.-G. Bagnères, C. Errard, C. Mulheim, C. Joulie, C. Lange, J. Chem. Ecol. 17, 1641 (1991); B. Vauchot, E. Provost, A.-G. Bagnères, J.-L. Clément, J. Insect. Physiol. 42, 309 (1996). Unlike natural heterospecific colonies, the mixed signature in experimental models results from the addition of the two signatures and seems to be poorly regulated probably because of the lack of genetic programming.
24. Natural heterospecific colonies: R. W. Howard, C. A. McDaniel, G. J. Blomquist, Science 210, 431 (1980); Psyche 89, 157 (1982); R. W. Howard, R. D. Akre, W. B. Gamett, Ann. Entomol. Soc. Am. 83, 607 (1990); R. K. Vander Meer and D. P. Wojcik, Science 218, 806 (1982); R. K. Vander Meer, D. P. Jouvenaz, D. P. Wojcik, J. Chem. Ecol. 15, 2247 (1989); N. Franks, M. S. Blum, R. K. Smith, A. B. Allies, ibid. 16, 1431 (1990); K. Dettner and C. Liepert, Annu. Rev. Entomol. 39, 129 (1994); C. Uepert and K. Dettner, J. Chem. Ecol. 19, 2143 (1993). Artificial heterospecific colonies: A.-G. Bagnères, C. Errard, C. Mulheim, C. Joulie, C. Lange, J. Chem. Ecol. 17, 1641 (1991); B. Vauchot, E. Provost, A.-G. Bagnères, J.-L. Clément, J. Insect. Physiol. 42, 309 (1996). Unlike natural heterospecific colonies, the mixed signature in experimental models results from the addition of the two signatures and seems to be poorly regulated probably because of the lack of genetic programming.
25. +, 1.5 bar He, 150 eV), scanning from 100 to 600 m/z. The capillary column and temperature program were the same as those used for GC. Injection was performed in the splitless mode for 1 min. Analysis was done either by total ion chromatogram or selected ion chromatogram.
26. Peak 11, which often appears in Fig. 1, was chosen as a reference to illustrate step by step the complexity of the qualitative and quantitative changes that occur in the chemical signature of P. atrimandibularis.
27. In P. biglumis bimaculatus, peak 11 contains only 2-methylhexacosane and accounts for 0.76% of the signature mixture (relative proportion). Conversely, in P. atrimandubularis peak 11 is made up mainly of a combination of heptacosene isomers and the 2-methylhexacosane and accounts for 31% of the mixture. The proportion of the 2-methylhexacosane is low.
28. At this time peak 11 accounts for 1.1% of the cuticular mixture in P. biglumis bimaculatus foundresses and 6.46% in the P. atrimandubularis queen and is composed only of 2-methylhexacosane in both species.
29. The P. biglumis bimaculatus descendants (workers and reproductives) cannot distinguish between their mother and the heterospecific parasite. They work for the parasite and contribute to her reproductive success. In contrast, they recognize a conspecific parasite and refuse to cooperate with her.
30. PCA displays different normalized variables (vectors) on a single plane, accounting for maximum dispersion. This unbiased representation allows one to distinguish or associate individuals (wasps) according to their degree of similarity using the relative proportions of the different quantitative variables (cuticular hydrocarbons).
31. It is known that cuticular mixtures from a colony, or part of a colony, change continuously over time. These changes are controlled by a dynamic system of regulation that induces a chemical drift in the whole group of insects and probably contributes to establish the colonial odor of social insects [E. Provost, G. Rivière, M. Roux, E. D. Morgan, A.-G. Bagnères, Insect Biochem. Molec. Biol. 23, 945 (1993)].
32. At the time of chemical usurpation, peak 11 is still composed only of 2-methylhexacosane and accounts for a similar relative proportion in the two species, that is, 0.58% in P. biglumis bimaculatus and 1.13% in P. atrimandibularis. 17. Peak 11 follows the same pattern: It returns to the same proportions as in June, that is, 1.06% for P. biglumis bimaculatus and 6.4% for P. atrimandibularis (including both the 2-methylhexacosane and the heptacosenes).
33. Comparable observations have been made in termites in which soldiers are fed by workers despite differences in caste signature [A.-G. Bagnères, thesis, Paris 6 University (1989)], and in slave-making ants in which the latter are fed by slaves taken at a larval stage, despite differences in specific signatures [C. Habersetzer and A. Bonavita-Cougourdan, Physiol. Entomol. 18, 160 (1993)].
34. Peak 11 accounts for 1.02% of the 2-methylhexacosane in P. biglumis bimaculatus female descendants, 6.13% of a mixture of 2-methylC26 and heptacosenes in P. atrimandibularis female descendants, and 30.3% of the heptacosenes in the P. atrimandibularis queen.
35. M.-C. Lorenzi, A.-G. Bagnères, J.-L. Clément, in Natural History and Evolution of Paper Wasps, S. Turillazzi and M. J. West-Eberhard, Eds. (Oxford Univ. Press, New York, 1996), chap. 10. Many authors working on paper wasps have suggested that chemicals covering the nest play a major role in nestmate recognition [D. W. Pfennig, G. J. Gamboa, H. K. Reeve, J. S. Shellman-Reeve, I. D. Ferguson, Behav. Ecol. Sociobiol. 13, 299 (1983); T. L. Singer and K. E. Espelie, Anim. Behav. 44, 63 (1992)].
36. M.-C. Lorenzi, A.-G. Bagnères, J.-L. Clément, in Natural History and Evolution of Paper Wasps, S. Turillazzi and M. J. West-Eberhard, Eds. (Oxford Univ. Press, New York, 1996), chap. 10. Many authors working on paper wasps have suggested that chemicals covering the nest play a major role in nestmate recognition [D. W. Pfennig, G. J. Gamboa, H. K. Reeve, J. S. Shellman-Reeve, I. D. Ferguson, Behav. Ecol. Sociobiol. 13, 299 (1983); T. L. Singer and K. E. Espelie, Anim. Behav. 44, 63 (1992)].
37. M.-C. Lorenzi, A.-G. Bagnères, J.-L. Clément, in Natural History and Evolution of Paper Wasps, S. Turillazzi and M. J. West-Eberhard, Eds. (Oxford Univ. Press, New York, 1996), chap. 10. Many authors working on paper wasps have suggested that chemicals covering the nest play a major role in nestmate recognition [D. W. Pfennig, G. J. Gamboa, H. K. Reeve, J. S. Shellman-Reeve, I. D. Ferguson, Behav. Ecol. Sociobiol. 13, 299 (1983); T. L. Singer and K. E. Espelie, Anim. Behav. 44, 63 (1992)].
38. In the present discussion the term cuticle means integument that is the cuticle plus associated epidermal cells and tissue including lipophorin (transport proteins). Oenocytes that are usually associated with the epidermal layer are currently thought to be the most likely site of biosynthesis of cuticular hydrocarbons carried to the epicuticular layer through pore and wax canals [D. R. Nelson et al., in Insect Lipids: Chemistry, Biochemistry and Biology, D. W. Stanley-Samuelson and D. R. Nelson, Eds. (Univ. Nebraska Press, Lincoln, NE, and London, 1993), pp. 271-315; G. Blomquist et al., ibid., pp. 317-351; X. Gu, D. Quilici, P. Juarez, G. J. Blomquist, C. Schal, J. Insect Physiol. 41, 257 (1995)].
39. In the present discussion the term cuticle means integument that is the cuticle plus associated epidermal cells and tissue including lipophorin (transport proteins). Oenocytes that are usually associated with the epidermal layer are currently thought to be the most likely site of biosynthesis of cuticular hydrocarbons carried to the epicuticular layer through pore and wax canals [D. R. Nelson et al., in Insect Lipids: Chemistry, Biochemistry and Biology, D. W. Stanley-Samuelson and D. R. Nelson, Eds. (Univ. Nebraska Press, Lincoln, NE, and London, 1993), pp. 271-315; G. Blomquist et al., ibid., pp. 317-351; X. Gu, D. Quilici, P. Juarez, G. J. Blomquist, C. Schal, J. Insect Physiol. 41, 257 (1995)].
40. In the present discussion the term cuticle means integument that is the cuticle plus associated epidermal cells and tissue including lipophorin (transport proteins). Oenocytes that are usually associated with the epidermal layer are currently thought to be the most likely site of biosynthesis of cuticular hydrocarbons carried to the epicuticular layer through pore and wax canals [D. R. Nelson et al., in Insect Lipids: Chemistry, Biochemistry and Biology, D. W. Stanley-Samuelson and D. R. Nelson, Eds. (Univ. Nebraska Press, Lincoln, NE, and London, 1993), pp. 271-315; G. Blomquist et al., ibid., pp. 317-351; X. Gu, D. Quilici, P. Juarez, G. J. Blomquist, C. Schal, J. Insect Physiol. 41, 257 (1995)].
41. J. M. Carpenter et al., Cladistics 9, 129 (1993).
42. K. G. Ross, R. K. Vander Meer, D. J. C. Reicher, E. L. Vargo, Evolution 41, 280 (1987); J.-F. Ferveur, K. F. Störtkuhl, R. F. Stocker, R. J. Greenspan, Science 267, 902 (1995); J.-F. Ferveur, Genetics 128, 293 (1991); _ and J.-M. Jallon, ibid. 131, 561 (1993); J. Chase et al., Proc. Natl. Acad. Sci. U.S.A. 89, 6050 (1992); C. Wicker and J.-M. Jallon, Eur. J. Entomol. 92, 197 (1995); J. Insect Physiol. 41, 65 (1995); T. S. Adams, D. R. Nelson, G. J. Blomquist, ibid., p. 609.
43. K. G. Ross, R. K. Vander Meer, D. J. C. Reicher, E. L. Vargo, Evolution 41, 280 (1987); J.-F. Ferveur, K. F. Störtkuhl, R. F. Stocker, R. J. Greenspan, Science 267, 902 (1995); J.-F. Ferveur, Genetics 128, 293 (1991); _ and J.-M. Jallon, ibid. 131, 561 (1993); J. Chase et al., Proc. Natl. Acad. Sci. U.S.A. 89, 6050 (1992); C. Wicker and J.-M. Jallon, Eur. J. Entomol. 92, 197 (1995); J. Insect Physiol. 41, 65 (1995); T. S. Adams, D. R. Nelson, G. J. Blomquist, ibid., p. 609.
44. K. G. Ross, R. K. Vander Meer, D. J. C. Reicher, E. L. Vargo, Evolution 41, 280 (1987); J.-F. Ferveur, K. F. Störtkuhl, R. F. Stocker, R. J. Greenspan, Science 267, 902 (1995); J.-F. Ferveur, Genetics 128, 293 (1991); _ and J.-M. Jallon, ibid. 131, 561 (1993); J. Chase et al., Proc. Natl. Acad. Sci. U.S.A. 89, 6050 (1992); C. Wicker and J.-M. Jallon, Eur. J. Entomol. 92, 197 (1995); J. Insect Physiol. 41, 65 (1995); T. S. Adams, D. R. Nelson, G. J. Blomquist, ibid., p. 609.
45. K. G. Ross, R. K. Vander Meer, D. J. C. Reicher, E. L. Vargo, Evolution 41, 280 (1987); J.-F. Ferveur, K. F. Störtkuhl, R. F. Stocker, R. J. Greenspan, Science 267, 902 (1995); J.-F. Ferveur, Genetics 128, 293 (1991); _ and J.-M. Jallon, ibid. 131, 561 (1993); J. Chase et al., Proc. Natl. Acad. Sci. U.S.A. 89, 6050 (1992); C. Wicker and J.-M. Jallon, Eur. J. Entomol. 92, 197 (1995); J. Insect Physiol. 41, 65 (1995); T. S. Adams, D. R. Nelson, G. J. Blomquist, ibid., p. 609.
46. K. G. Ross, R. K. Vander Meer, D. J. C. Reicher, E. L. Vargo, Evolution 41, 280 (1987); J.-F. Ferveur, K. F. Störtkuhl, R. F. Stocker, R. J. Greenspan, Science 267, 902 (1995); J.-F. Ferveur, Genetics 128, 293 (1991); _ and J.-M. Jallon, ibid. 131, 561 (1993); J. Chase et al., Proc. Natl. Acad. Sci. U.S.A. 89, 6050 (1992); C. Wicker and J.-M. Jallon, Eur. J. Entomol. 92, 197 (1995); J. Insect Physiol. 41, 65 (1995); T. S. Adams, D. R. Nelson, G. J. Blomquist, ibid., p. 609.
47. K. G. Ross, R. K. Vander Meer, D. J. C. Reicher, E. L. Vargo, Evolution 41, 280 (1987); J.-F. Ferveur, K. F. Störtkuhl, R. F. Stocker, R. J. Greenspan, Science 267, 902 (1995); J.-F. Ferveur, Genetics 128, 293 (1991); _ and J.-M. Jallon, ibid. 131, 561 (1993); J. Chase et al., Proc. Natl. Acad. Sci. U.S.A. 89, 6050 (1992); C. Wicker and J.-M. Jallon, Eur. J. Entomol. 92, 197 (1995); J. Insect Physiol. 41, 65 (1995); T. S. Adams, D. R. Nelson, G. J. Blomquist, ibid., p. 609.
48. K. G. Ross, R. K. Vander Meer, D. J. C. Reicher, E. L. Vargo, Evolution 41, 280 (1987); J.-F. Ferveur, K. F. Störtkuhl, R. F. Stocker, R. J. Greenspan, Science 267, 902 (1995); J.-F. Ferveur, Genetics 128, 293 (1991); _ and J.-M. Jallon, ibid. 131, 561 (1993); J. Chase et al., Proc. Natl. Acad. Sci. U.S.A. 89, 6050 (1992); C. Wicker and J.-M. Jallon, Eur. J. Entomol. 92, 197 (1995); J. Insect Physiol. 41, 65 (1995); T. S. Adams, D. R. Nelson, G. J. Blomquist, ibid., p. 609.
49. K. G. Ross, R. K. Vander Meer, D. J. C. Reicher, E. L. Vargo, Evolution 41, 280 (1987); J.-F. Ferveur, K. F. Störtkuhl, R. F. Stocker, R. J. Greenspan, Science 267, 902 (1995); J.-F. Ferveur, Genetics 128, 293 (1991); _ and J.-M. Jallon, ibid. 131, 561 (1993); J. Chase et al., Proc. Natl. Acad. Sci. U.S.A. 89, 6050 (1992); C. Wicker and J.-M. Jallon, Eur. J. Entomol. 92, 197 (1995); J. Insect Physiol. 41, 65 (1995); T. S. Adams, D. R. Nelson, G. J. Blomquist, ibid., p. 609.
50. We thank A. Bonavita-Cougourdan, R. Vander Meer, and K. Espelie for their useful comments on the initial draft, A. Boyer and A. Tirard for their help on the figures, and A. Corsini, M. Renucci, and C. Ronin for work on this manuscript.