Behavioral Ecology and Sociobiology

, Volume 58, Issue 5, pp 486–496 | Cite as

Changes in the cuticular hydrocarbons of incipient reproductives correlate with triggering of worker policing in the bulldog ant Myrmecia gulosa

  • Vincent Dietemann
  • Jürgen Liebig
  • Bert Hölldobler
  • Christian Peeters
Original Article

Abstract

In social insects, conflicts over male parentage can be resolved by worker policing. However, the evolution of policing behavior is constrained by the ability of individuals to identify reproductive nestmates, or their eggs. We investigated the occurrence of worker policing and its underlying chemical communication in the bulldog ant Myrmecia gulosa. Although workers have functional ovaries and can lay male-destined eggs, they do not reproduce in queenright colonies. To determine if their sterility is a consequence of worker policing, we experimentally induced worker reproduction in the presence of a queen. Some individuals were seized and immobilized by nestmates, and sometimes killed as a consequence. Although the ovarian development of immobilized individuals was variable, their cuticular hydrocarbon profiles were intermediate between reproductive and nonreproductive workers, indicating they were in the process of starting to reproduce. Approximately 29% of these incipient reproductive workers were successfully policed. To test for policing on eggs, we transferred viable worker eggs to queenright colonies and monitored their acceptance. Furthermore, we compared the surface hydrocarbons of the different types of eggs to determine whether these chemicals could be involved in egg recognition. We found that although there were differences in hydrocarbon profiles and discrimination between queen and worker-laid eggs, viable eggs were not destroyed. Our results strongly support the idea that cuticular hydrocarbons are involved in the policing of reproductive workers. A low level of worker policing appears sufficient to select for self-restraint in workers when few fitness benefits are gained by selfish reproduction. Policing of eggs may thus be unnecessary.

Keywords

Worker reproduction Worker policing Aggression Cuticular hydrocarbons Oophagy 

Notes

Acknowledgements

We are grateful to Michael Schwarz, Katja Hogendoorn, Remko Leijs, Steve Shattuck, Archie McArthur and Russell for their hospitality and assistance during fieldwork. Ben Oldroyd, Thibaud Monnin, Liselotte Sundström and three anonymous referees gave valuable criticisms on earlier drafts. This work was funded by the Deutsche Forschungsgemeinschaft SFB 554 (C3) and the Graduiertenkolleg ‘Grundlagen des Arthropodenverhaltens’. The experiments comply with the current laws of Germany. The ants were collected under scientific investigation license A2247 issued by National Parks and Wildlife Service of New South Wales, and exported under permits PWS P993042 and PWS 20002478 issued by Environment Australia.

References

  1. Aitchison J (1986) The statistical analysis of compositional data. Monographs in statistics and applied probability. Chapman and Hall, LondonGoogle Scholar
  2. Beekman M, Komdeur J, Ratnieks F (2003) Reproductive conflicts in social animals: who has power? Trends Ecol Evol 18:277–282CrossRefGoogle Scholar
  3. Boomsma JJ, Nielsen J, Sundström L, Oldham NJ, Tentschert J, Petersen HC, Morgan ED (2003) Informational constraints on optimal sex allocation in ants. Proc Natl Acad Sci USA 100:8799–8804Google Scholar
  4. Bourke AFG (1988) Worker reproduction in the higher eusocial Hymenoptera. Q Rev Biol 63:291–311CrossRefGoogle Scholar
  5. Bourke AFG (1999) Colony size, social complexity and reproductive conflict in social insects. J Evol Biol 12:245–257CrossRefGoogle Scholar
  6. Choe J (1988) Worker reproduction and social evolution in ants (Hymenoptera: Formicidae). In: Trager JC (ed) Advances in myrmecology. Brill, Leiden, pp 163–187Google Scholar
  7. Cole BJ (1986) The social behaviour of Leptothorax allardycei (Hymenoptera: Formicidae): time budgets and the evolution of worker reproduction. Behav Ecol Sociobiol 18:165–173CrossRefGoogle Scholar
  8. Cuvillier-Hot V, Cobb M, Malosse C, Peeters C (2001) Sex, age and ovarian activity affect cuticular hydrocarbons in Diacamma ceylonense, a queenless ant. J Insect Physiol 47:485–493CrossRefPubMedGoogle Scholar
  9. Cuvillier-Hot V, Lenoir A, Crewe R, Malosse C, Peeters C (2004a) Fertility signaling and reproductive skew in queenless ants. Anim Behav 68:1209–1219CrossRefGoogle Scholar
  10. Cuvillier-Hot V, Lenoir A, Peeters C (2004b) Reproductive monopoly enforced by sterile police workers in a queenless ant. Behav Ecol 15:970-975CrossRefGoogle Scholar
  11. D’Ettorre P, Heinze J, Ratnieks FLW (2004) Worker policing by egg eating in the ponerine ant Pachycondyla inversa. Proc R Soc Lond 271:1427–1434CrossRefGoogle Scholar
  12. Dietemann V, Peeters C (2000) Queen influence on the shift from trophic to reproductive eggs laid by workers of the ponerine ant Pachycondyla apicalis. Insect Soc 47:223–228Google Scholar
  13. Dietemann V, Peeters C, Hölldobler B (2002) Caste specialization and differentiation in reproductive potential in the phylogenetically primitive ant Myrmecia gulosa. Insect Soc 49:289–298CrossRefGoogle Scholar
  14. Dietemann V, Peeters C, Liebig J, Thivet V, Hölldobler B (2003) Cuticular hydrocarbons mediate discrimination of reproductives and nonreproductives in the ant Myrmecia gulosa. Proc Natl Acad Sci USA 100:10341–10346Google Scholar
  15. Dietemann V, Peeters C, Hölldobler B (2005) Role of the queen in regulating reproduction in the bulldog ant Myrmecia gulosa: control or signalling? Anim Behav 69:777–784CrossRefGoogle Scholar
  16. Endler A, Liebig J, Schmitt T, Parker J, Jones G, Schreier P, Hölldobler B (2004) Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect. Proc Natl Acad Sci USA 101:2945–2950Google Scholar
  17. Foster KR (2004) Diminishing returns in social evolution: the not-so-tragic commons. J Evol Biol 17:1058–1072CrossRefPubMedGoogle Scholar
  18. Foster KR, Ratnieks FLW (2000) Social insects—facultative worker policing in a wasp. Nature 407:692–693CrossRefPubMedGoogle Scholar
  19. Foster KR, Ratnieks FLW (2001) Worker policing in the common wasp Vespula vulgaris. Proc R Soc Lond 268:169–174Google Scholar
  20. Gobin B, Billen J, Peeters C (1999) Policing behaviour toward virgin egg layers in a polygynous ponerine ant. Anim Behav 58:1117–1122CrossRefPubMedGoogle Scholar
  21. Gu X, Quilici D, Juarez P, Blomquist GJ, Schal C (1995) Biosynthesis of hydrocarbons and contact pheromone and their transport by lipophorin in females of the German cockroach (Blattella germanica). J Insect Physiol 41:257–267CrossRefGoogle Scholar
  22. Halling LA, Oldroyd BP, Wattanachaiyingcharoen W, Barron AB, Nanork P, Wongsiri S (2001) Worker policing in the bee Apis florea. Behav Ecol Sociobiol 49:509–513CrossRefGoogle Scholar
  23. Hammond RL, Bruford MW, Bourke AFG (2003) Male parentage does not vary with colony kin structure in a multiple-queen ant. J Evol Biol 16:446–455CrossRefPubMedGoogle Scholar
  24. Hannonen M, Sledge MF, Turillazzi S, Sundström L (2002) Queen reproduction, chemical signalling and worker behaviour in polygyne colonies of the ant Formica fusca. Anim Behav 64:477–485CrossRefGoogle Scholar
  25. Hartmann A, Wantia J, Torres JA, Heinze J (2003) Worker policing without genetic conflict in a clonal ant. Proc Natl Acad Sci USA 100:12836–12840Google Scholar
  26. Haskins CP, Haskins EF (1950) Notes on the biology and social behaviour of the archaic ponerine ants of the genera Myrmecia and Promyrmecia. Ann Ent Soc Am 43:461–491Google Scholar
  27. Heinze J, Stengl B, Sledge M (2002) Worker rank, reproductive status and cuticular hydrocarbon signature in the ant, Pachycondyla cf. inversa. Behav Ecol Sociobiol 52:59–65CrossRefGoogle Scholar
  28. Helanterä H, Sundström L (2005) Worker reproduction in the ant Formica fusca. J Evol Biol 18:162–171CrossRefPubMedGoogle Scholar
  29. Iwanishi S, Hasegawa E, Ohkawara K (2003) Worker oviposition in the myrmicine ant Aphaenogaster smythiesi japonica Forel. Anim Behav 66:513–519CrossRefGoogle Scholar
  30. Kikuta N, Tsuji K (1999) Queen and worker policing in the monogynous and monoandrous ant, Diacamma sp. Behav Ecol Sociobiol 46:180–189CrossRefGoogle Scholar
  31. Liebig J, Peeters C, Hölldobler B (1999) Worker policing limits the number of reproductives in a ponerine ant. Proc R Soc Lond 266:1865–1870CrossRefGoogle Scholar
  32. Liebig J, Peeters C, Oldham NJ, Markstädter C, Hölldobler B (2000) Are variations in cuticular hydrocarbons of queens and workers a reliable signal of fertility in the ant Harpegnathos saltator? Proc Natl Acad Sci USA 97:4124–4131Google Scholar
  33. Monnin T, Peeters C (1997) Cannibalism of subordinates’ eggs in the monogynous queenless ant Dinoponera quadriceps. Naturwissenschaften 84:499–502CrossRefGoogle Scholar
  34. Monnin T, Peeters C (1999) Dominance hierarchy and reproductive conflicts among subordinates in a monogynous queenless ant. Behav Ecol 10:323–332CrossRefGoogle Scholar
  35. Monnin T, Ratnieks FLW (2001) Policing in queenless ponerine ants. Behav Ecol Sociobiol 50:97–108CrossRefGoogle Scholar
  36. Monnin T, Malosse C, Peeters C (1998) Solid-phase microextraction and cuticular hydrocarbons differences related to reproductive activity in queenless ant Dinoponera quadriceps. J Chem Ecol 24:473–490CrossRefGoogle Scholar
  37. Nakata K, Tsuji K (1996) The effect of colony size on conflict over male-production between gamergate and dominant workers in the ponerine ant Diacamma sp. Ethol Ecol Evol 8:147–156Google Scholar
  38. Nonacs P, Carlin NF (1990) When can ants discriminate the sex of brood? A new aspect of queen-worker conflicts. Proc Natl Acad Sci USA 87:9670–9673Google Scholar
  39. Ogata K, Taylor RW (1991) Ants of the genus Myrmecia Fabricius: a preliminary review and key to the named species (Hymenoptera: Formicidae: Myrmeciinae). J Nat Hist 25:1623–1673Google Scholar
  40. Oldroyd BP, Halling LA, Good G, Wattanachaiyingcharoen W, Barron AB, Nanork P, Wongsiri S, Ratnieks FLW (2001) Worker policing and worker reproduction in Apis cerana. Behav Ecol Sociobiol 50:371–377CrossRefGoogle Scholar
  41. Pamilo P (1991) Evolution of colony characteristics in social insects. II. Number of reproductive individuals. Am Nat 138:412–433CrossRefGoogle Scholar
  42. Peeters C (1997) Morphologically “primitive” ants: comparative review of social characters, and the importance of queen-worker dimorphism. In: Choe J, Crespi BJ (eds) The evolution of social behaviour in insects and arachnids. Cambridge University Press, Cambridge, pp 372–391Google Scholar
  43. Peeters C, Monnin T, Malosse C (1999) Cuticular hydrocarbons correlated with reproductive status in a queenless ant. Proc R Soc Lond 266:1323–1327CrossRefGoogle Scholar
  44. Pirk CWW, Neumann P, Ratnieks FLW (2003) Cape honeybees, Apis mellifera capensis, police worker-laid eggs despite the absence of relatedness benefits. Behav Ecol 14:347–352CrossRefGoogle Scholar
  45. Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat 132:217–236CrossRefGoogle Scholar
  46. Ratnieks FLW (1993) Egg-laying, egg-removal, and ovary development by workers in queenright honey bee colonies. Behav Ecol Sociobiol 32:191–198CrossRefGoogle Scholar
  47. Ratnieks FLW (1995) Evidence for a queen-produced egg-marking pheromone and its use in worker policing in the honey bee. J Apic Res 34:31–37Google Scholar
  48. Ratnieks FLW, Visscher PK (1989) Worker policing in the honey bee. Nature 342:796–797CrossRefGoogle Scholar
  49. Schal C, Gu X, Burns EL, Blomquist GJ (1994) Patterns of biosynthesis and accumulation of hydrocarbons and contact sex pheromone in the female German cockroach, Blattella germanica. Arch Insect Biochem 25:375–391CrossRefGoogle Scholar
  50. Sledge M, Boscaro F, Turillazzi S (2001) Cuticular hydrocarbons and reproductive status in the social wasp Polistes dominulus. Behav Ecol Sociobiol 49:401–409CrossRefGoogle Scholar
  51. Sledge M, Trinca I, Massolo A, Boscaro F, Turillazzi S (2004) Variation in cuticular hydrocarbon signatures, hormonal correlates and establishment of reproductive dominance in a polistine wasp. J Insect Physiol 50:73–83CrossRefPubMedGoogle Scholar
  52. Tsuji K, Egashira K, Hölldobler B (1999) Regulation of worker reproduction by direct physical contact in the ant Diacamma sp. from Japan. Anim Behav 58:337–343CrossRefPubMedGoogle Scholar
  53. Villesen P, Boomsma JJ (2003) Patterns of male parentage in the fungus-growing ants. Behav Ecol Sociobiol 53:246–253CrossRefGoogle Scholar
  54. Walin L, Sundström L, Seppä P, Rosengren R (1998) Worker reproduction in ants—a genetic analysis. Heredity 81:604–612CrossRefGoogle Scholar
  55. Wenseleers T, Helanterä H, Hart A, Ratnieks FLW (2004) Worker reproduction and policing in insect societies: an ESS analysis. J Evol Biol 17:1035–1047CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Vincent Dietemann
    • 1
    • 3
  • Jürgen Liebig
    • 1
  • Bert Hölldobler
    • 1
  • Christian Peeters
    • 2
  1. 1.LS Verhaltensphysiologie und Soziobiologie, BiozentrumWürzburg UniversityWürzburgGermany
  2. 2.CNRS UMR 7625, Laboratoire d’EcologieUniversité Pierre-et-Marie CurieParisFrance
  3. 3.Department of Zoology and EntomologyPretoria UniversityPretoriaSouth Africa

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