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Experimental evidence that workers recognize reproductives through cuticular hydrocarbons in the ant Odontomachus brunneus

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Abstract

Eusociality is characterized by a reproductive division of labor, wherein workers respond to the presence of reproductive individuals by refraining from reproduction themselves and restricting the reproductive efforts of others. Our understanding of how eusociality is maintained therefore depends on characterizing the mechanism by which workers detect the presence of a reproductive. Variations in cuticular hydrocarbons correspond to changes in reproductive ability in ants, and experimental studies are beginning to reveal the function of hydrocarbons as signals. In this study, we compare the cuticular hydrocarbon profiles of dominant and reproductive workers and queens of the ant Odontomachus brunneus with profiles of non-reproductive workers. Using split/reunification tests we document the existence of worker policing in both queenless and queenright colonies; supernumerary reproductives were treated aggressively by nestmates. Finally, we induce aggression and replicate queen-like submissive nestmate responses by supplementing the hydrocarbon profile of workers with (Z)-9-nonacosene, a compound that was significantly more abundant on the cuticles of reproductives. In three bioassays, we compare this manipulation to various control manipulations of the hydrocarbon profile and demonstrate that workers gauge the reproductive activity of nestmates through changes in their cuticular hydrocarbon profiles.

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References

  • Blomquist GC, Bagnères A-G (2010) Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Bos N, Dreier S, Jorgensen CG, Nielsen J, Guerrieri FJ, d'Ettorre P (2012) Learning and perceptual similarity among cuticular hydrocarbons in ants. J Insect Physiol 58:138–146

    Article  PubMed  CAS  Google Scholar 

  • Bourke AFG (1988) Worker reproduction in the higher eusocial Hymenoptera. Q Rev Biol 63:291–311

    Article  Google Scholar 

  • Cuvillier-Hot V, Gadagkar R, Peeters C, Cobb M (2002) Regulation of reproduction in a queenless ant: aggression, pheromones and reduction in conflict. Proc R Soc Lond B 269:1295–1300

    Article  Google Scholar 

  • Cuvillier-Hot V, Lenoir A, Crewe R, Malosse C, Peeters C (2004) Fertility signalling and reproductive skew in queenless ants. Anim Behav 68:1209–1219

    Article  Google Scholar 

  • Cuvillier-Hot V, Renault V, Peeters C (2005) Rapid modification in the olfactory signal of ants following a change in reproductive status. Naturwissenschaften 92:73–77

    Article  PubMed  CAS  Google Scholar 

  • Denis D, Chameron S, Costille L, Pocheville A, Chaline N, Fresneau D (2008) Workers agonistic interactions in queenright and queenless nests of a polydomous ant society. Anim Behav 75:791–800

    Article  Google Scholar 

  • D'Ettorre P, Heinze J (2005) Individual recognition in ant queens. Curr Biol 15:2170–2174

    Article  PubMed  Google Scholar 

  • D'Ettorre P, Heinze J, Schulz C, Francke W, Ayasse M (2004) Does she smell like a queen? Chemoreception of a cuticular hydrocarbon signal in the ant Pachycondyla inversa. J Exp Biol 207:1085–1091

    Article  PubMed  Google Scholar 

  • 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 100:10341–10346

    Article  PubMed  CAS  Google Scholar 

  • Endler A, Liebig J, Schmitt T, Parker JE, Jones GR, Schreier P, Hölldobler B (2004) Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect. Proc Natl Acad Sci USA 101:2945–2950

    Article  PubMed  CAS  Google Scholar 

  • Foitzik A, Fröba J, Rüger MH, Witte V (2011) Competition over workers: fertility signalling in wingless queens of Hypoponera opacior. Insect Soc 58:271–278

    Article  Google Scholar 

  • Ginzel MD, Moreira JA, Ray AM, Millar JG, Hanks LM (2006) (Z)-9-nonacosene-major component of the contact sex pheromone of the beetle Megacyllene caryae. J Chem Ecol 32:435–451

    Article  PubMed  CAS  Google Scholar 

  • Gobin B, Ito F (2003) Sumo wrestling in ants: major workers fight over male production in Acanthomyrmex ferox. Naturwissenschaften 90:318–321

    Article  PubMed  CAS  Google Scholar 

  • Hart LM, Tschinkel WR (2012) A seasonal natural history of the ant, Odontomachus brunneus. Insect Soc 59:45–54

    Article  Google Scholar 

  • Heinze J, d'Ettorre P (2009) Honest and dishonest communication in social Hymenoptera. J Exp Biol 212:1775–1779

    Article  PubMed  CAS  Google Scholar 

  • Heinze J, Oberstadt B (1999) Worker age, size and social status in queenless colonies of the ant Leptothorax gredleri. Anim Behav 58:751–759

    Article  PubMed  Google Scholar 

  • Heinze J, Hölldobler B, Peeters C (1994) Conflict and cooperation in ant societies. Naturwissenschaften 81:489–497

    Article  CAS  Google Scholar 

  • Heinze J, Trunzer B, Oliveira PS, Hölldobler B (1996) Regulation of reproduction in the neotropical ponerine ant, Pachycondyla villosa. J Insect Behav 9:441–450

    Article  Google Scholar 

  • Heinze J, Puchinger W, Hölldobler B (1997) Worker reproduction and social hierarchies in Leptothorax ants. Anim Behav 54:849–864

    Article  PubMed  Google Scholar 

  • Heinze J, Stengl B, Sledge MF (2002) Worker rank, reproductive status and cuticular hydrocarbon signature in the ant, Pachycondyla cf. inversa. Behav Ecol Sociobiol 52:59–65

    Article  Google Scholar 

  • Holman L, Jorgensen CG, Nielsen J, d'Ettorre P (2010) Identification of an ant queen pheromone regulating worker sterility. Proc R Soc B 277:3793–3800

    Article  PubMed  CAS  Google Scholar 

  • Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393

    Article  PubMed  CAS  Google Scholar 

  • Izzo A, Wells M, Huang Z, Tibbetts E (2010) Cuticular hydrocarbons correlate with fertility, not dominance, in a paper wasp, Polistes dominulus. Behav Ecol Sociobiol 64:857–864

    Article  Google Scholar 

  • Keller L, Nonacs P (1993) The role of queen pheromones in social insects—queen control or queen signal. Anim Behav 45:787–794

    Article  Google Scholar 

  • Kocher SD, Grozinger CM (2011) Cooperation, conflict, and the evolution of queen pheromones. J Chem Ecol 37:1263–1275

    Article  PubMed  CAS  Google Scholar 

  • Le Conte Y, Hefetz A (2008) Primer pheromones in social Hymenoptera. Annu Rev Entomol 53:523–542

    Article  PubMed  Google Scholar 

  • Liebig J (2010) Hydrocarbon profiles indicate fertility and dominance status in ant, bee, and wasp colonies. In: Blomquist GJ, Bagnères A-G (eds) Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press, Cambridge, pp 254–281

    Chapter  Google Scholar 

  • Liebig J, Peeters C, Oldham NJ, Markstadter 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 97:4124–4131

    Article  PubMed  CAS  Google Scholar 

  • Lockey KH (1988) Lipids of the insect cuticle—origin, composition and function. Comp Biochem Physiol B Biochem Mol Biol 89:595–645

    Google Scholar 

  • Martin S, Drijfhout F (2009a) A review of ant cuticular hydrocarbons. J Chem Ecol 35:1151–1161

    Article  PubMed  CAS  Google Scholar 

  • Martin SJ, Drijfhout FP (2009b) How reliable is the analysis of complex cuticular hydrocarbon profiles by multivariate statistical methods? J Chem Ecol 35:375–382

    Article  PubMed  CAS  Google Scholar 

  • Martin SJ, Drijfhout FP (2009c) Nestmate and task cues are influenced and encoded differently within ant cuticular hydrocarbon profiles. J Chem Ecol 35:368–374

    Article  PubMed  CAS  Google Scholar 

  • Medeiros FLN, Lopes NP, Moutinho PRS, Oliveira PS, Hölldobler B (1992) Functional polygyny, agonistic interactions and reproductive dominance in the neotropical ant Odontomachus chelifer (Hymenoptera, Formicidae, Ponerinae). Ethology 91:134–146

    Article  Google Scholar 

  • Millar JG (2010) Chemical synthesis of insect cuticular hydrocarbons. In: Blomquist GJ, Bagnères A-G (eds) Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press, Cambridge, pp 163–186

    Chapter  Google Scholar 

  • Monnin T (2006) Chemical recognition of reproductive status in social insects. Ann Zool Fenn 43:515–530

    Google Scholar 

  • Monnin T, Ratnieks FLW (2001) Policing in queenless ponerine ants. Behav Ecol Sociobiol 50:97–108

    Article  Google Scholar 

  • Nunes TM, Turatti ICC, Lopes NP, Zucchi R (2009) Chemical signals in the stingless bee, Frieseomelitta varia, indicate caste, gender, age, and reproductive status. J Chem Ecol 35:1172–1180

    Article  PubMed  CAS  Google Scholar 

  • Oliveira PS, Hölldobler B (1990) Dominance orders in the ponerine ant Pachycondyla apicalis (Hymenoptera, Formicidae). Behav Ecol Sociobiol 27:385–393

    Article  Google Scholar 

  • Peeters C, Monnin T, Malosse C (1999) Cuticular hydrocarbons correlated with reproductive status in a queenless ant. Proc R Soc Lond B 266:1323–1327

    Article  CAS  Google Scholar 

  • Powell S, Tschinkel WR (1999) Ritualized conflict in Odontomachus brunneus and the generation of interaction-based task allocation: a new organizational mechanism in ants. Anim Behav 58:965–972

    Article  PubMed  Google Scholar 

  • Ratnieks FLW, Foster KR, Wenseleers T (2006) Conflict resolution in insect societies. Annu Rev Entomol 51:581–608

    Article  PubMed  CAS  Google Scholar 

  • Seeley TD (1985) Honeybee ecology: a study of adaptation in social life. Princeton University Press, Princeton, New Jersey

    Google Scholar 

  • Sledge MF, Boscaro F, Turillazzi S (2001) Cuticular hydrocarbons and reproductive status in the social wasp Polistes dominulus. Behav Ecol Sociobiol 49:401–409

    Article  Google Scholar 

  • Smith AA, Hölldobler B, Liebig J (2008) Hydrocarbon signals explain the pattern of worker and egg policing in the ant Aphaenogaster cockerelli. J Chem Ecol 34:1275–1282

    Article  PubMed  CAS  Google Scholar 

  • Smith AA, Hölldobler B, Liebig J (2009) Cuticular hydrocarbons reliably identify cheaters and allow enforcement of altruism in a social insect. Curr Biol 19:78–81

    Article  PubMed  CAS  Google Scholar 

  • Smith AA, Hölldobler B, Liebig J (2011) Reclaiming the crown: queen to worker conflict over reproduction in Aphaenogaster cockerelli. Naturwissenschaften 98:237–240

    Article  PubMed  CAS  Google Scholar 

  • Smith AA, Hölldobler B, Liebig J (2012) Queen-specific signals and worker punishment in the ant Aphaenogaster cockerelli: the role of the Dufour's gland. Anim Behav 83:587–593

    Article  Google Scholar 

  • van Walsum E, Gobin B, Ito F, Billen J (1998) Worker reproduction in the ponerine ant Odontomachus simillimus (Hymenoptera: Formicidae). Sociobiology 32:427–440

    Google Scholar 

  • van Wilgenburg E, Sulc R, Shea KJ, Tsutsui ND (2010) Deciphering the chemical basis of nestmate recognition. J Chem Ecol 36:751–758

    Article  PubMed  Google Scholar 

  • van Zweden JS (2010) The evolution of honest queen pheromones in insect societies. Commun Integr Biol 3:50–52

    Article  PubMed  Google Scholar 

  • Wilson EO (1971) The Insect Societies. Belknap, Cambridge, MA

    Google Scholar 

Download references

Acknowledgments

We thank Walter R. Tschinkel for collection assistance and Fred Larabee for supplying additional colonies.

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Authors and Affiliations

  1. Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

    Adrian A. Smith, Lawrence M. Hanks & Andrew V. Suarez

  2. Department of Entomology, University of California, Riverside, CA, 92521, USA

    Jocelyn G. Millar

  3. Department of Animal Biology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

    Andrew V. Suarez

Authors
  1. Adrian A. Smith
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  2. Jocelyn G. Millar
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  3. Lawrence M. Hanks
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  4. Andrew V. Suarez
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Corresponding author

Correspondence to Adrian A. Smith.

Additional information

Communicated by J. Heinze

Electronic supplementary material

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Aggression of nestmate ants of the species Odontomachus brunneus to a newly established reproductive and dominant worker upon reintroduction to her original queenless colony. The ant with a red paint mark on her abdomen is the reintroduced reproductive. The lid of the colony was removed for clarity. Several bouts of rapid antennation can be seen as well as aggression elevating to multiple workers biting, holding, and pulling on the reintroduced worker (WMV 12,575 kb)

Response of nestmate ants of the species Odontomachus brunneus to workers treated with Z9:C29 (with yellow paint mark on thorax). Response by rapid antennation and submissive reactions can be seen multiple times (WMV 4,630 kb)

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Smith, A.A., Millar, J.G., Hanks, L.M. et al. Experimental evidence that workers recognize reproductives through cuticular hydrocarbons in the ant Odontomachus brunneus . Behav Ecol Sociobiol 66, 1267–1276 (2012). https://doi.org/10.1007/s00265-012-1380-x

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  • DOI: https://doi.org/10.1007/s00265-012-1380-x

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