Skip to main content
SpringerLink
Log in

Production of sexuals in a fission-performing ant: dual effects of queen pheromones and colony size

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Models based on the kin selection theory predict that in social hymenopterans, queens may favor a lower investment in the production of sexuals than workers. However, in perennial colonies, this conflict may be tuned down by colony-level selection because of the trade off between colony survival and reproductive allocation. In this study, we present a survey of sexual production in colonies of Aphaenogaster senilis, a common species of ant in the Iberian Peninsula. Similar to most species that reproduce by fission, males were found in large excess compared to gynes (172:1). Sexuals were more likely to be found in queenless than in queenright (QR) field colonies. However, we also found a few gynes and numerous males in very large QR colonies. We compared these data with those available in the literature for A. rudis, a congeneric species from North America that has independent colony founding. The sex ratio in this species was only five males for each female, and sexuals were mostly found in QR nests, irrespective of colony size. We confirmed queen inhibition of sexual production in A. senilis in laboratory experiments and provide evidence that this inhibition is mediated by a nonvolatile pheromone. To seek the potential source of such a queen pheromone, we analyzed the secretions of two conspicuous exocrine glands, the Dufour’s and postpharyngeal glands (DG and PPG, respectively) in both queens and workers. Both secretions were composed of hydrocarbons, but that of DG also contained small quantities of tetradecanal and hexadecanal. The hydrocarbon profile of the DG and PPG showed notable caste specificity suggesting a role in caste-related behavior. The PPG secretions also differed between colonies suggesting its role in colony-level recognition. We suggest that in A. senilis, there are two modes of colony fission: First, in very large colonies, gynes are produced, probably because of the dilution of the queen pheromone, and consequently one or more gynes leave the mother colony with workers and brood to found a new nest. This is beneficial at the colony level because it avoids the production of costly sexuals in small colonies. However, because the queen and workers have different optima for sexual production, we hypothesize that queens tend to overproduce the pheromone to delay their production. This in turn may drive workers to leave the mother colony during nest relocation and to produce sexuals once they are away from the queen’s influence, creating a second mode of colony fission.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alaux C, Jaisson P, Hefetz A (2005) Reproductive decision in semelparous social insects: a pace-maker queen in bumblebees colonies. Behav Ecol Sociobiol 59:270–277

    Article  Google Scholar 

  • Alaux C, Jaisson P, Hefetz A (2006) Regulation of worker reproduction in bumblebees: workers eavesdrop on a queen signal. Behav Ecol Sociobiol 60:439–446

    Article  Google Scholar 

  • Aron S, Keller L, Passera L (2001) Role of resource availability on sex, caste and reproductive allocation ratios in the Argentine ant Linepithema humile. J Anim Ecol 70:831–839

    Article  Google Scholar 

  • Backus VL (1995) Rules for allocation in a temperate forest ant—demography, natural selection, and queen–worker conflict. Am Nat 145:775–796

    Article  Google Scholar 

  • Bourke AFG, Chan GL (1999) Queen–worker conflict over sexual production and colony maintenance in perennial social insects. Am Nat 154:417–426

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Bourke AFG, Ratnieks FLW (1999) Kin conflict over caste determination in social Hymenoptera. Behav Ecol Sociobiol 46:287–297

    Article  Google Scholar 

  • Brian MV (1973) Caste control through worker attack in the ant Myrmica. Insectes Soc 20:87–102

    Article  Google Scholar 

  • Brian MV (1979) Habitat differences in sexual production by two co-existent ants Tetramorium caespitum, Lasius alienus, in southern England. J Anim Ecol 48:943–953

    Article  Google Scholar 

  • Bulmer MG (1983) Sex ratio theory in social insects with swarming. J Theor Biol 100:329–340

    Article  Google Scholar 

  • Butler CG (1959) The source of the substance produced by a queen honeybee (Apis mellifera) which inhibits development of the ovaries of the workers of its colony. Proc R Entomol Soc Lond 34:137–138

    Google Scholar 

  • Butler L (1961) The scent of queen honey bees (Apis mellifera) that causes partial inhibition of queen rearing. J Insect Physiol 7:258–264

    Article  CAS  Google Scholar 

  • Cerdá X, Dahbi A, Retana J (2002) Spatial patterns, temporal variability, and the role of multi-nest colonies in a monogynous Spanish desert ant. Ecol Entomol 27:7–15

    Article  Google Scholar 

  • Craig R (1980) Sex investment ratios in social Hymenoptera. Am Nat 116:311–323

    Article  Google Scholar 

  • 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 47:485–493

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • de Menten L, Fournier D, Brent C, Passera L, Vargo EL, Aron S (2005) Dual mechanism of queen influence over sex ratio in the ant Pheidole pallidula. Behav Ecol Sociobiol 58:527–533

    Article  Google Scholar 

  • Dietemann V, Peeters C, Liebig J, Thivet V, Hölldobler B (2003) Cuticular hydrocarbons mediate discrimination of reproductives and non reproductives in the ant Myrmecia gulosa. Proc Natl Acad Sci USA 100:10341–10346

    Article  PubMed  CAS  Google Scholar 

  • Dor R, Katzav-Gozansky T, Hefetz A (2005) Dufour’s gland pheromone as a reliable fertility signal among honeybee (Apis mellifera) workers. Behav Ecol Sociobiol 58:270–276

    Article  Google Scholar 

  • Elmes GW, Wardlaw JC (1982) A population study of the ants Myrmica sabuleti and Myrmica scabrinodis living at two sites in the south of England. II. Effect of above-nest vegetation. J Anim Ecol 51:665–680

    Article  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 

  • Gotwald WH Jr (1995) Army ants: the biology of social predation. Cornell Univ. Press, Ithaca, NY

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Headley AE (1949) A population study of the ant Aphaenogaster fulva ssp. aquia Buckley (Hymenoptera, Formicidae). Ann Entomol Soc Am, 42:265–272

    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 

  • Herbers JM, Banschbach VS (1998) Food supply and reproductive allocation in forest ants: repeated experiments give different results. Oikos 83:145–151

    Article  Google Scholar 

  • Herbers JM, Banschbach VS (1999) Plasticity of social organization in a forest ant species. Behav Ecol Sociobiol 45:451–465

    Article  Google Scholar 

  • Herbers JM, DeHeer CJ, Foitzik S (2001) Conflict over sex allocation drives conflict over reproduction in perennial social insects. Am Nat 158:178–192

    Article  PubMed  CAS  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 

  • 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, Ohkawara K (2005) The mechanism of the queen signal in regulation of worker reproduction in the myrmicine ant Aphaenogaster smythiesi japonica. Ethol Ecol Evol 17:27–39

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Julian GE, Fewell JH, Gadau J, Johnson RA, Larrabee D (2002) Genetic determination of the queen caste in an ant hybrid zone. Proc Natl Acad Sci USA 99:8157–8160

    Article  PubMed  CAS  Google Scholar 

  • Katzav-Gozansky T, Boulay R, Soroker V, Hefetz A (2004) Queen-signal modulation of worker pheromonal composition in honeybees. Proc R Soc Lond B 271:2065–2069

    Article  Google Scholar 

  • Katzav-Gozansky T, Boulay R, Soroker V, Hefetz A (2006) Queen pheromones affecting the production of queen-like secretion in workers. J Comp Physiol A 192:737–742

    Article  CAS  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 

  • Lahav S, Soroker V, Hefetz A, Vander Meer RK (1999) Direct behavioral evidence for hydrocarbons as ant recognition discriminators. Naturwissenschaften 86:246–249

    Article  CAS  Google Scholar 

  • Ledoux A (1971) Un nouveau mode de bouturage de société chez la fourmi Aphaenogaster senilis Mayr. C R Acad Sci Ser D Sci Nat 273:83–85

    Google Scholar 

  • Ledoux A (1976a) Bouturage expérimental de colonie chez la fourmi Aphaenogaster senilis Mayr. C R Acad Sci Ser D Sci Nat 283:1061–1063

    Google Scholar 

  • Ledoux A (1976b) Inhibition exercée sur l’apparition de nouvelles femelles ailées, par le femelle reine pondeuse chez Aphaenogaster senilis (Hyméoptère Formicoidea). C R Acad Sci Ser D Sci Nat 283:1197–200

    Google Scholar 

  • Ledoux A (1984) Sur la présence d’ouvrières à parthénogenèse thélytoque observée chez Aphaenogaster senilis (Mayr.) (Hyménoptère Formicoidea). C R Acad Sci Ser III Sci Vie 299:859–861

    Google Scholar 

  • Lenoir A, Fresneau D, Errard C, Hefetz A (1999) Individuality and colonial identity in ants. In: Detrain C, Deneubourg JL, Pasteels J (eds) Information processing in social insects. Birkhauser, Basel, pp 219–237

    Google Scholar 

  • Lenoir A, Hefetz A, Simon T, Soroker V (2001) Comparative dynamics of gestalt odour formation in two ant species Camponotus fellah and Aphaenogaster senilis (Hymenoptera: Formicidae). Physiol Entomol 26:275–283

    Article  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 

  • Lim SP, Lee CY (2005) Effects of queen body parts on the production of new sexuals in the Pharaoh’s ant, Monomorium pharaonis (Hymenoptera: Formicidae). Sociobiology 46:677–688

    Google Scholar 

  • Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS system for mixed models. SAS Institute, Cary

    Google Scholar 

  • Mehdiabadi N, Reeve HK, Mueller UG (2003) Queens versus workers: sex-ratio conflicts in eusocial insects. Trends Ecol Evol 18:88–93

    Article  Google Scholar 

  • Monnin T, Ratnieks FL, Jones GR, Beard R (2002) Pretender punishment induced by chemical signaling in a queenless ant. Nature 419:61–65

    Article  PubMed  CAS  Google Scholar 

  • Oster G, Wilson EO (1978) Caste and ecology in the social insects. Princeton Univ. Press, Princeton, NJ

    Google Scholar 

  • Pamilo P (1991) Evolution of colony characteristics in social insects. I. Sex allocation. Am Nat 137:83–107

    Article  Google Scholar 

  • Pearcy M, Aron S (2006) Local resource competition and sex ratio in the ant Cataglyphis cursor. Behav Ecol:569–574

  • 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 

  • Pettis JS, Winston ML, Collins AM (1995) Suppression of queen rearing in European and Africanized honey bees Apis mellifera L. by synthetic queen mandibular pheromone. Insectes Soc 42:113–121

    Article  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge Univ. Press, Cambridge

    Google Scholar 

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

    Article  Google Scholar 

  • Seeley TD (1995) The wisdom of the hive: the social physiology of honey bee colonies. Harvard Univ. Press, London

    Google Scholar 

  • Sundström L (1995) Sex allocation and colony maintenance in monogyne and polygyne colonies of Formica truncorum (Hymenoptera: Formicidae): the impact of kinship and mating structure. Am Nat 146:182–201

    Article  Google Scholar 

  • Talbot M (1951) Populations and hibernating conditions of the ant Aphaenogaster (Attomyrma) rudis Emery (Hymenoptera: Formicidae). Ann Entomol Soc Am 44:302–307

    Google Scholar 

  • Thomas ML, Parry LJ, Allan RA, Elgar MA (1999) Geographic affinity, cuticular hydrocarbons and colony recognition in the Australian meat ant Iridomyrmex purpureus. Naturwissenschaften 86:87–92

    Article  CAS  Google Scholar 

  • Vander Meer RK, Glancey BM, Lofgren CS, Glover A, Tumlinson JH, Rocca J (1980) The poison sac of red imported fire ant queens: source of a pheromone attractant. Ann Entomol Soc Am 73:609–612

    Google Scholar 

  • Vander Meer RK, Morel L (1998) Nestmate recognition in ants. In: Vander Meer RK, Breed M, Winston M, Espelie KE (eds) Pheromone communication in social insects. Westview, Boulder, CO, pp 79–103

    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 (1997) Poison gland of queen fire ants (Solenopsis invicta) is the source of a primer pheromone. Naturwissenschaften 84:507–510

    Article  CAS  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 

  • Vargo EL, Passera L (1991) Pheromonal and behavioral queen control over the production of gynes in the Argentine ant Iridomyrmex humilis (Mayr). Behav Ecol Sociobiol 28:161–169

    Article  Google Scholar 

  • Vargo EL, Passera L (1992) Gyne development in the Argentine ant Iridomyrmex humilis role of overwintering and queen control. Physiol Entomol 17:193–201

    Google Scholar 

  • Volny VP, Gordon DM (2002) Genetic basis for queen–worker dimorphism in a social insect. Proc Natl Acad Sci USA 99:6108–6111

    Article  PubMed  CAS  Google Scholar 

  • Wagner D, Tissot M, Cuevas W, Gordon DM (2000) Harvester ants utilize cuticular hydrocarbons in nestmate recognition. J Chem Ecol 26:2245–2257

    Article  CAS  Google Scholar 

  • Walin L, Seppä P (2001) Resource allocation in the red ant Myrmica ruginodis—an interplay of genetics and ecology. J Evol Biol 14:694–707

    Article  Google Scholar 

  • Wheeler DE (1994) Nourishment in ants: patterns in individuals and societies. In: Hunt JH, Nalepa CA (eds) Nourishment and evolution in insect societies. Westview, Boulder, CO, pp 245–278

    Google Scholar 

  • Wilson EO (1971) The insect societies. Harvard Univ. Press, Cambridge.

    Google Scholar 

  • Winston M, Higo HA, Slessor KN (1990) Effects of various dosages of queens mandibular gland pheromone on the inhibition of queen rearing in the honey bee (Hymenoptera: Apidae). Ann Entomol Soc Am 83:234–238

    Google Scholar 

  • Woyciechowski M, Łomnicki A (1987) Multiple mating of queens and the sterility of workers among eusocial Hymenoptera. J Theor Biol 128:317–327

    Google Scholar 

  • Zar JH (1984) Biostatistical analyses. Princeton Hall, London

    Google Scholar 

Download references

Acknowledgments

This work was supported by “Ecodoca” (European Community—Access to Research Infrastructure action of the Improving Human Potential Program at Doñana Biological Station) to AL and AH and “Picasso” no. 09137XM to AL and XC. RB and XC were supported by grant CGL2006-04968/BOS. Jean-Philippe Christides helped in the chemical analyses. Colony collection and demographic data were obtained with the help of Fernando Amor, Angel Barroso, Ana Carvajal, Raymond Jegat, Isabel Luque, Thibaut Monnin, and Javier Retana. We thank Ray Heithaus and David Lubertazzi for valuable information on A. rudis and Saturo Iwanishi for interesting comments on the manuscript. We thank Naomi Paz for editorial assistance.

Author information

Authors and Affiliations

  1. Estación Biológica de Doñana, Consejo Superior de Investigaciones Científicas, Avenida María Luisa s/n, 41013, Sevilla, Spain

    Raphaël Boulay & Xim Cerdá

  2. Department of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Ramat Aviv, 69978, Tel Aviv, Israel

    Abraham Hefetz

  3. Institut de Recherches sur la Biologie de l’Insecte, CNRS UMR 6035, Faculté des Sciences, Université François Rabelais, Parc de Grandmont, 37200, Tours, France

    Séverine Devers & Alain Lenoir

  4. Institut für Organische Chemie, Universität Hamburg, Martin Luther King Platz 6, 20146, Hamburg, Germany

    Wittko Francke & Robert Twele

Authors
  1. Raphaël Boulay
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Abraham Hefetz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xim Cerdá
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Séverine Devers
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wittko Francke
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Robert Twele
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alain Lenoir
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Raphaël Boulay.

Additional information

Communicated by J. Heinze

Rights and permissions

Reprints and permissions

About this article

Cite this article

Boulay, R., Hefetz, A., Cerdá, X. et al. Production of sexuals in a fission-performing ant: dual effects of queen pheromones and colony size. Behav Ecol Sociobiol 61, 1531–1541 (2007). https://doi.org/10.1007/s00265-007-0385-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-007-0385-3

Keywords

Search

Navigation