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Queen fertility, egg marking and colony size in the ant Camponotus floridanus

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Abstract

In ant societies, workers do not usually reproduce but gain indirect fitness benefits from raising related offspring produced by the queen. One of the preconditions of this worker self-restraint is sufficient fertility of the queen. The queen is, therefore, expected to signal her fertility. In Camponotus floridanus, workers can recognize the presence of a highly fertile queen via her eggs, which are marked with the queen's specific hydrocarbon profile. If information on fertility is encoded in the hydrocarbon profile of eggs, we expect workers to be able to differentiate between eggs from highly and weakly fertile queens. We found that workers discriminate between these eggs solely on the basis of their hydrocarbon profiles which differ both qualitatively and quantitatively. This pattern is further supported by the similarity of the egg profiles of workers and weakly fertile queens and the similar treatment of both kinds of eggs. Profiles of queen eggs correspond to the cuticular hydrocarbon profiles of the respective queens. Changes in the cuticular profiles are associated with the size of the colony the queen originates from and her current egg-laying rate. However, partial correlation analysis indicates that only colony size predicts the cuticular profile. Colony size is a buffered indicator of queen fertility as it is a consequence of queen productivity within a certain period of time, whereas daily egg-laying rate varies due to cyclical oviposition. We conclude that surface hydrocarbons of eggs and the cuticular profiles of queens both signal queen fertility, suggesting a major role of fertility signals in the regulation of reproduction in social insects.

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References

  • Aitchison J (1986) The statistical analysis of compositional data: monographs in statistics and applied probability. Chapman & Hall, London

    Google Scholar 

  • Ayasse M, Maelovits T, Tengö J, Taghizadeh T, Francke W (1995) Are there pheromonal dominance signals in the bumblebee Bombus hypnorum L. (Hymenoptera, Apidae). Apidologie 26:163–180

    Article  CAS  Google Scholar 

  • Barron AB, Oldroyd BP, Ratnieks FLW (2001) Worker reproduction in honey-bees (Apis) and the anarchic syndrome: a review. Behav Ecol Sociobiol 50:199–208

    Article  Google Scholar 

  • Beekman M, Oldroyd BP (2005) Honey bee workers use cues other than egg viability for policing. Biol Lett 1:129–132

    Article  PubMed  Google Scholar 

  • Bonavita-Cougourdan A, Théraulaz G, Bagnéres AG, Roux M, Pratte M, Provost E, Clément JL (1991) Cuticular hydrocarbons, social organisation and ovarian development in a polistine wasp: Polistes dominulus Christ. Comp Biochem Physiol B Biochem Mol Biol 100:667–680

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Bourke AFG (1988b) Dominance orders, worker reproduction, and queen-worker conflict in the slave-making ant Harpagoxenus sublaevis. Behav Ecol Sociobiol 23:323–333

    Article  Google Scholar 

  • Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton

    Google Scholar 

  • Choe JC (1988) Worker reproduction and social evolution in ants (Hymenoptera: Formicidae). In: Trager JC (ed) Advances in myrmecology. E.J. Brill, Leiden, pp 163–187

    Google Scholar 

  • Cole BJ (1986) The social behavior of Leptothorax allardycei (Hymenoptera, Formicidae): time budgets and the evolution of worker reproduction. Behav Ecol Sociobiol 18:165–173

    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, Peeters C (2004a) Reproductive monopoly enforced by sterile police workers in a queenless ant. Behav Ecol 15:970–975

    Article  Google Scholar 

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

    Article  Google Scholar 

  • D'Ettorre P, Heinze J, Ratnieks FLW (2004a) Worker policing by egg eating in the ponerine ant Pachycondyla inversa. Proc R Soc Lond B 271:1427–1434

    Article  CAS  Google Scholar 

  • D'Ettorre P, Heinze J, Schulz C, Francke W, Ayasse M (2004b) 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  CAS  Google Scholar 

  • De Biseau J-C, Passera L, Daloze D, Aron S (2004) Ovarian activity correlates with extreme changes in cuticular hydrocarbon profile in the highly polygynous ant, Linepithema humile. J Insect Physiol 50:585–593

    Article  PubMed  CAS  Google Scholar 

  • Dietemann V, Hölldobler B, Peeters C (2002) Caste specialization and differentiation in reproductive potential in the phylogenetically primitive ant Myrmecia gulosa. Insectes Soc 49:289–298

    Article  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 U S A 100:10341–10346

    Article  PubMed  CAS  Google Scholar 

  • 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 U S A 101:2945–2950

    Article  PubMed  CAS  Google Scholar 

  • Fan Y, Zurek L, Dykstra MJ, Schal C (2003) Hydrocarbon synthesis by enzymatically dissociated oenocytes of the abdominal integument of the German cockroach, Blattella germanica. Naturwissenschaften 90:121–126

    PubMed  CAS  Google Scholar 

  • Foster KR (2004) Diminishing returns in social evolution: the not-so-tragic commons. J Evol Biol 17:1026–1034

    Article  Google Scholar 

  • Foster KR, Ratnieks FLW (2001) Convergent evolution of worker policing by egg eating in the honeybee and common wasp. Proc R Soc Lond B 268:169–174

    CAS  Google Scholar 

  • Frank SA (1995) Mutual policing and repression of competition in the evolution of cooperative groups. Nature 377:520–522

    Article  PubMed  CAS  Google Scholar 

  • Gadau J, Heinze J, Hölldobler B, Schmid M (1996) Population and colony structure of the carpenter ant Camponotus floridanus. Mol Ecol 5:785–792

    PubMed  CAS  Google Scholar 

  • Gobin B, Billen J, Peeters C (1999) Policing behaviour towards virgin egg layers in a polygynous ponerine ant. Anim Behav 58:1117–1122

    Article  PubMed  Google Scholar 

  • Halling LA, Oldroyd BP, Wattanachaiyingcharoen W, Baron AB, Nanork P, Wongsiri S (2001) Worker policing in the bee Apis florea. Behav Ecol Sociobiol 49:509–513

    Article  Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behavior I and II. J Theor Biol 7:1–52

    Article  PubMed  CAS  Google Scholar 

  • Hammond RL, Keller L (2004) Conflict over male parentage in social insects. PLoS Biol 2:1472–1482

    Article  CAS  Google Scholar 

  • Hannonen M, Sledge MF, Turillazzi S, Sundström L (2002) Queen reproduction, chemical signalling and worker bahaviour in polygyne colonies of the ant Formica fusca. Anim Behav 64:477–485

    Article  Google Scholar 

  • Hartmann A, Wantia J, Torres JA, Heinze J (2003) Worker policing without genetic conflicts in a clonal ant. Proc Natl Acad Sci U S A 100:12836–12840

    Article  PubMed  CAS  Google Scholar 

  • Heinze J, Keller L (2000) Alternative reproductive strategies: a queen perspective in ants. Trends Ecol Evol 15:508–512

    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 

  • Helanterä H, Sundström L (2005) Worker reproduction in the ant Formica fusca. J Evol Biol 18:162–171

    Article  PubMed  Google Scholar 

  • Hölldobler B, Carlin NF (1989) Colony founding, queen control and worker reproduction in the ant Aphaenogaster (=Novomessor) cockerelli (Hymenoptera: Formicidae). Psyche 96:131–151

    Article  Google Scholar 

  • Hölldobler B, Wilson EO (1983) Queen control in colonies of weaver ants (Hymenoptera: Formicidae). Ann Entomol Soc Am 76:235–238

    Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Hoover SER, Keeling CI, Winston ML, Slessor KN (2003) The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 90:477–480

    Article  PubMed  CAS  Google Scholar 

  • Iwanishi S, Hasegawa E, Ohkawara K (2003) Worker oviposition and policing behaviour in the myrmecine ant Aphaenogaster smythiesi japonica Forel. Anim Behav 66:513–519

    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 

  • Kikuta N, Tsuji K (1999) Queen and worker policing in monogynous and monandrous ant, Diacamma sp. Behav Ecol Sociobiol 46:180–189

    Article  Google Scholar 

  • Liebig J, Peeters C, Hölldobler B (1999) Worker policing limits the number of reproductives in a ponerine ant. Proc R Soc Lond B 266:1865–1870

    Article  Google Scholar 

  • 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 U S A 97:4124–4131

    Article  PubMed  CAS  Google Scholar 

  • Lucas C, Pho DB, Fresneau D, Jallon JM (2004) Hydrocarbon circulation and colonial signature in Pachycondyla villosa. J Insect Physiol 50:595–607

    Article  PubMed  CAS  Google Scholar 

  • Maynard Smith J, Szathmary E (1995) The major transitions in evolution. W.H. Freeman and Company, New York Oxford

    Google Scholar 

  • Monnin T, Peeters C (1997) Cannibalism of subordinates' eggs in the monogynous queenless ant Dinoponera quadriceps. Naturwissenschaften 84:499–502

    Article  CAS  Google Scholar 

  • Monnin T, Peeters C (1999) Dominance hierarchy and reproductive conflicts among subordinates in a monogynous queenless ant. Behav Ecol 10:323–332

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Monnin T, Malosse C, Peeters C (1998) Solid-phase microextraction and cuticular hydrocarbon differences related to reproductive activity in a queenless ant. J Chem Ecol 24:473–490

    Article  CAS  Google Scholar 

  • Naumann K, Winston ML, Slessor KN, Prestwich GD, Webster FX (1991) Production and transmission of honey bee queen (Apis mellifera L.) mandibular gland pheromone. Behav Ecol Sociobiol 29:321–332

    Article  Google Scholar 

  • 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 50:371–377

    Article  Google Scholar 

  • Ortius D, Heinze J (1999) Fertility signaling in queens of a North American ant. Behav Ecol Sociobiol 45:151–159

    Article  Google Scholar 

  • Pamilo P (1991) Evolution of colony characteristics in social insects. II. number of reproductive individuals. Am Nat 138:412–433

    Article  Google Scholar 

  • Pamilo P, Crozier RH (1996) Reproductive skew simplified. Oikos 75:533–535

    Article  Google Scholar 

  • Passera L (1980) La fonction inhibitrice des reines de la fourmi Plagiolepis pygmaea Latr.: role des pheromones. Insectes Soc 27:212–225

    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 

  • Pirk CWW, Neumann P, Hepburn R, Moritz RFA, Tautz J (2004) Egg viability and worker policing in honey bees. Proc Natl Acad Sci U S A 101:8649–8651

    Article  PubMed  CAS  Google Scholar 

  • Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat 132:217–236

    Article  Google Scholar 

  • Ratnieks FLW (1993) Egg-laying, egg-removal, and ovary development by workers in queenright honey bee colonies. Behav Ecol Sociobiol 32:191–198

    Article  Google Scholar 

  • Ratnieks FLW, Reeve HK (1992) Conflict in single queen hymenopteran societies: the structure of conflict and processes that reduce conflict in advanced eusocial species. J Theor Biol 158:33–65

    Article  Google Scholar 

  • Ratnieks FLW, Visscher PK (1989) Worker policing in the honeybee. Nature 342:796–797

    Article  Google Scholar 

  • Schal C, Sevala VL, Young HP, Bachmann JA (1998) Sites of synthesis and transport pathways of insect hydrocarbons: cuticle and ovary as target tissues. Am Zool 38:382–393

    CAS  Google Scholar 

  • Sanetra M, Crozier RH (2002) Daughters inherit colonies from mothers in the ‘living-fossil’ ant Nothomyrmecia macrops. Naturwissenschaften 89:71–74

    Article  PubMed  CAS  Google Scholar 

  • Seeley TD (1979) Queen substance dispersal by messenger workers in honeybee colonies. Behav Ecol Sociobiol 5:391–415

    Article  Google Scholar 

  • Seeley TD (1985) Honeybee ecology. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Siegel S, Castellan NJ Jr (1988) Nonparametric statistics for behavioral sciences. McGraw-Hill Book Co., New York

    Google Scholar 

  • Sledge M, 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 

  • Tentschert J, Bestmann HJ, Heinze J (2002) Cuticular compounds of workers and queens in two Leptothorax ant species—a comparison of results obtained by solvent extraction, solid sampling, and SPME. Chemoecology 12:15–21

    Article  CAS  Google Scholar 

  • Vargo EL (1988) A bioassay for a primer pheromone of queen fire ants (Solenopsis invicta) which inhibits the production of sexuals. Insectes Soc 35:382–392

    Article  Google Scholar 

  • Vargo EL, Hulsey CD (2000) Multiple glandular origins of queen pheromones in the fire ant Solenopsis invicta. J Insect Physiol 46:1151–1159

    Article  PubMed  CAS  Google Scholar 

  • Visscher PK (1989) A quantitative study of worker reproduction in honey bee colonies. Behav Ecol Sociobiol 25:247–254

    Article  Google Scholar 

  • Visscher PK (1996) Reproductive conflict in honey bees: a stalemate of worker egg-laying and policing. Behav Ecol Sociobiol 39:237–244

    Article  Google Scholar 

  • Walin L, Sundström L, Seppä P, Rosengren R (1998) Worker reproduction in ants—a genetic analysis. Heredity 81:604–612

    Article  Google Scholar 

  • Wenseleers T, Helanterä H, Hart A, Ratnieks FLW (2004) Worker reproduction and policing in insect societies: an ESS analysis. J Evol Biol 17:1035–1047

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Thibaud Monnin, Christian Peeters, Kazuki Tsuji, a referee, and especially Lotta Sundström for providing helpful comments on the manuscript; we also thank the German Science Foundation (SFB 554 TP C3), the European Union (INSECTS, Integrated Studies of the Economy of Insect Societies, HPRN-CT-2000-00052), and Aventis (travel grant to AE) for funding. The Social Insect Working Group of the Santa Fe Institute provided insightful discussions.

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Correspondence to Annett Endler.

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Communicated by L. Sundström

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Endler, A., Liebig, J. & Hölldobler, B. Queen fertility, egg marking and colony size in the ant Camponotus floridanus . Behav Ecol Sociobiol 59, 490–499 (2006). https://doi.org/10.1007/s00265-005-0073-0

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