Skip to main content
Log in

Worker self-restraint and policing maintain the queen’s reproductive monopoly in a pseudomyrmecine ant

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

Abstract

Division of reproductive labor in insect societies is often based on worker self-restraint and both queen and worker policing. Workers of many hitherto studied wasps, bees and ants do not lay eggs in the presence of a queen. However, it is presently unclear how far these observations in a few select clades can be generalized. We investigated if and how queens maintain a reproductive monopoly in colonies of the elongate twig ant, Pseudomyrmex gracilis, a member of the previously unstudied ant subfamily Pseudomyrmecinae. Colonies are usually headed by a single, singly mated queen (monogyny, monandry). Workers therefore would be more closely related to males produced by other workers (r = 0.375) than to the sons of queens (r = 0.25). Nevertheless, workers appear to refrain from laying male-destined eggs in the presence of the queen. In queenless conditions, workers form dominance hierarchies by antennal boxing, and only one or a few high-ranking individuals readily begin to lay eggs. When returned into a queenright colony, egg-laying workers are immediately bitten, stung and expelled or killed by other workers. While the composition of cuticular hydrocarbons clearly differed between castes, it less clearly reflected worker ovarian development. An association with worker ovarian development that would allow workers to monitor the reproductive status of nestmates could only be tentatively postulated for certain substances. Our study broadens our knowledge about reproductive conflict in social Hymenoptera and shows that worker sterility in the presence of a queen is more common in monogynous, monandrous ants than expected from relatedness alone.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aitchison J (1986) The statistical analysis of compositional data. Chapman and Hall, London

    Book  Google Scholar 

  • Bang A, Deshpande S, Sumana A, Gadagkar R (2010) Choosing an appropriate index to construct dominance hierarchies in animal societies: a comparison of three indices. Anim Behav 79:631–636

    Article  Google Scholar 

  • Barth MB, Kellner K, Heinze J (2010) The police are not the army: context-dependent aggressiveness in a clonal ant. Biol Lett 6:329–332

    Article  PubMed  Google Scholar 

  • Bourke AFG (1988) 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 

  • Brady SG, Schultz TR, Fisher BL, Ward PS (2006) Evaluating alternative hypotheses for the early evolution and diversification of ants. Proc Natl Acad Sci USA 103:18172–18177

    Article  PubMed  CAS  Google Scholar 

  • Brunner E, Heinze J (2009) Worker dominance and policing in the ant Temnothorax unifasciatus. Insectes Soc 56:397–404

    Article  Google Scholar 

  • Carlson DA, Bernier UR, Sutton BD (1998) Elution parameters from capillary GC for methyl-branched alkanes. J Chem Ecol 24:1845–1865

    Article  CAS  Google Scholar 

  • Clement LW, Köppen SCW, Brand WA, Heil M (2008) Strategies of a parasite of the ant–Acacia mutualism. Behav Ecol Sociobiol 62:953–962

    Article  PubMed  Google Scholar 

  • Cole BJ (1981) Dominance hierarchies in Leptothorax ants. Science 212:83–84

    Article  PubMed  CAS  Google Scholar 

  • Crozier RH, Pamilo P (1996) Evolution of social insect colonies. Sex allocation and kin selection. Oxford University Press, Oxford

    Google Scholar 

  • Dietemann V, Liebig J, Hölldobler B, Peeters C (2005) Changes in the cuticular hydrocarbons of incipient reproductives correlate with triggering of worker policing in the bulldog ant Myrmecia gulosa. Behav Ecol Sociobiol 58:486–496

    Article  Google Scholar 

  • Franks NR, Scovell E (1983) Dominance and reproductive success among slave-making worker ants. Nature 304:724–725

    Article  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 

  • Goodnight KF, Queller DC (2001) Relatedness 5.0.8. Available online at www.gsoftnet.us/GSoft.html, Rice University.

  • Hammond RL, Keller L (2004) Conflict over male parentage in social insects. PLoS Biol 2:e248. doi:10.1371/journal.pbio.0020248

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Heil M, González-Teuber M, Clement LW, Kautz S, Verhaagh M, Bueno JCS (2009) Divergent investment strategies of Acacia myrmecophytes and the coexistence of mutualists and exploiters. Proc Natl Acad Sci USA 106:18091–18096

    Article  PubMed  CAS  Google Scholar 

  • Heinze J (2004) Reproductive conflict in insect societies. Adv Stud Behav 34:1–57

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

    Article  PubMed  Google Scholar 

  • Helanterä H, Sundström L (2007) Worker reproduction in Formica ants. Am Nat 170:E14–E25

    Article  PubMed  Google Scholar 

  • Hölldobler B, Wilson EO (2008) The superorganism: the beauty, elegance, and strangeness of insect societies. WW Norton, New York

    Google Scholar 

  • Holm S (1979) A simple sequential rejective multiple test procedure. Scand J Statistics 6:65–70

    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 

  • Janzen DH (1966) Coevolution of mutualism between ants and acacias in Central America. Evolution 20:249–275

    Article  Google Scholar 

  • Janzen DH (1975) Pseudomyrmex nigropilosa: a parasite of a mutualism. Science 188:936–937

    Article  PubMed  CAS  Google Scholar 

  • Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Res 10:551–555

    Article  Google Scholar 

  • Kautz S, Pauls SU, Ballhorn DJ, Lumbsch HT, Heil M (2009) Polygynous supercolonies of the acacia–ant Pseudomyrmex peperi, an inferior colony founder. Mol Ecol 18:5180–5194

    Article  PubMed  CAS  Google Scholar 

  • Kawabata S, Tsuji K (2005) The policing behavior ‘immobilization’ towards ovary-developed workers in the ant, Diacamma sp. from Japan. Insect Soc 52:89–95

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Larsen A, Philpott SM (2010) Twig-nesting ants: the hidden predators of the Coffee Berry Borer in Chiapas, Mexico. Biotropica 42:342–347

    Article  Google Scholar 

  • Lewis PO, Zaykin D (2001) Genetic Data Analysis: computer program for the analysis of allelic data. Version 1.0 (d16c). Free program distributed by the authors over the internet from http://lewis.eeb.uconn.edu/lewishome/software.html

  • 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 282–324

    Google Scholar 

  • MacCallum RC, Widaman KF, Zhang S, Hong S (1999) Sample size in factor analysis. Psychol Methods 4:84–89

    Article  Google Scholar 

  • MacGown JA, Hill JG (2010) Two new exotic pest ants, Pseudomyrmex gracilis and Monomorium floricola (Hymenoptera: Formicidae) collected in Mississippi. Midsouth Entomol 3:106–109

    Google Scholar 

  • Martin P, Bateson P (1993) Measuring behaviour, 2nd edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Mintzer A (1982) Nestmate recognition and incompatibility between colonies of the acacia–ant Pseudomyrmex ferruginea. Behav Ecol Sociobiol 10:165–168

    Article  Google Scholar 

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

    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 ponerine ants. Behav Ecol Sociobiol 50:97–102

    Article  Google Scholar 

  • Nelson DR (1993) Methyl-branched lipids in insects. In: Stanley-Samuelson DW, Nelson DR (eds) Insect lipids: chemistry, biochemistry, and biology. University of Nebraska Press, Lincoln, pp 271–316

    Google Scholar 

  • Ohtsuki H, Tsuji K (2009) Adaptive reproduction schedule as a cause of worker policing in social Hymenoptera: a dynamic game analysis. Am Nat 173:747–758

    Article  PubMed  Google Scholar 

  • Paxton RJ, Thorén PA, Estoup A, Tengö J (2001) Queen–worker conflict over male production and the sex ratio in a facultatively polyandrous bumblebee, Bombus hypnorum: the consequences of nest usurpation. Mol Ecol 10:2489–2498

    PubMed  CAS  Google Scholar 

  • Raine NE, Gammans N, Macfayden IJ, Scrivner GK, Stone GN (2004) Guards and thieves: antagonistic interactions between two ant species coexisting on the same ant–plant. Ecol Entomol 29:345–352

    Article  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, 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 honeybees. Nature 342:796–797

    Article  Google Scholar 

  • Ratnieks FLW, Wenseleers T (2005) Policing insect societies. Science 307:54–56

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Saigo T, Tsuchida K (2004) Queen and worker policing in monogynous and monandrous colonies of a primitively eusocial wasp. Proc R Soc Lond B 271:S509–S512

    Article  Google Scholar 

  • Schmid VS, Kautz S, Trindl A, Heinze J (2009) Polymerase chain reaction primers for polymorphic microsatellite loci in the ant Pseudomyrmex gracilis (Formicidae: Pseudomyrmecinae). Mol Ecol Res 9:1150–1152

    Article  CAS  Google Scholar 

  • Sommer K, Hölldobler B (1992) Coexistence and dominance among queens and mated workers in the ant Pachycondyla tridentate. Naturwissenschaften 79:470–472

    Article  Google Scholar 

  • Stroeymeyt N, Brunner E, Heinze J (2007) “Selfish worker policing” controls reproduction in a Temnothorax ant. Behav Evol Sociobiol 61:1449–1457

    Article  Google Scholar 

  • Tsuchida K, Saigo T, Nagata N, Tsujita S, Takeuchi K, Miyano S (2003) Queen–worker conflicts over male production and sex allocation in a primitively eusocial wasp. Evolution 57:2365–2373

    PubMed  Google Scholar 

  • Tsuji K, Kikuta N, Kikuchi T (2012) Determination of the cost of worker reproduction via diminished life span in the ant Diacamma sp. Evolution 66:1322–1331

    Article  PubMed  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 S, Seppä P, Rosengren R (1998) Worker reproduction in ants – a genetic analysis. Heredity 81:604–612

    Article  Google Scholar 

  • Walter B, Brunner E, Heinze J (2011) Policing effectiveness depends on relatedness and group size. Am Nat 177:368–376

    Article  PubMed  Google Scholar 

  • Ward PS, Downie DA (2005) The ant subfamily Pseudomyrmecinae (Hymenoptera: Formicidae): phylogeny and evolution of big-eyed arboreal ants. Syst Entomol 30:310–335

    Article  Google Scholar 

  • Wenseleers T, Ratnieks FLW (2006) Comparative analysis of worker reproduction and policing in eusocial Hymenoptera supports relatedness theory. Am Nat 168:E163–E179

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wenseleers T, Tofilski A, Ratnieks FLW (2005) Queen and worker policing in the tree wasp Dolichovespula sylvestris. Behav Ecol Sociobiol 58:80–86

    Article  Google Scholar 

  • Wetterer JK (2010) Worldwide spread of the graceful twig ant, Pseudomyrmex gracilis (Hymenoptera: Formicidae). Fla Entomol 93:535–540

    Article  Google Scholar 

Download references

Acknowledgements

The study would not have been possible without the great logistic support of Dr. Josefina Steiner, Universidade Federal de Santa Catarina, who also provided the opportunity to conduct the investigations in the framework of a project on the interaction among bromeliads and the associated fauna. We also thank Phil Ward for ant identification. The study was authorized by IBAMA, permit 12826, in 2008 and material transfer agreement 003/2005/DZUP between Dr. M.A. Navarro da Silva, Departamento de Zoologia da Universidade Federal do Parana, and University of Regensburg. V.S.S. was supported by scholarships of Universität Bayern e.V. and DAAD. M.K. gratefully acknowledges financial support from the Volkswagen Foundation and the Max Planck Society.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Volker S. Schmid.

Additional information

Communicated by L. Sundström

Electronic supplementary material

Below is the link to the electronic supplementary material.

Video file showing two instances of antennal boxing (indicated by yellow arrows) (MPG 13792 kb)

Video file showing one instance of antennal boxing (indicated by a yellow arrow) (MPG 7860 kb)

Video file showing one instance of antennal boxing (indicated by a yellow arrow) (MPG 3416 kb)

Online Resource 4

PDF file containing Tables S1–S4 and Fig. S1 (PDF 156 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schmid, V.S., Kaltenpoth, M., Strohm, E. et al. Worker self-restraint and policing maintain the queen’s reproductive monopoly in a pseudomyrmecine ant. Behav Ecol Sociobiol 67, 571–581 (2013). https://doi.org/10.1007/s00265-013-1476-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-013-1476-y

Keywords

Navigation