Behavioral Ecology and Sociobiology

, Volume 68, Issue 3, pp 363–371 | Cite as

Context-dependent acceptance of non-nestmates in a primitively eusocial insect

Original Paper


The benefits of cooperation are essential in driving group formation. However, an individual can gain significant benefits by acting selfishly at a substantial cost to others in the group. Thus, group members must find a balance between accepting and rejecting potential new members. Here, I explore the factors that mediate acceptance of non-related individuals during the period of group establishment in the primitively eusocial wasp Mischocyttarus mexicanus. In this species, group composition changes during establishment, with non-related females (non-nestmates) sometimes accepted into a foreign colony. By experimentally introducing non-nestmates to newly established colonies, I test the hypothesis that acceptance threshold of nestmates towards non-nestmates shifts depending on the ecological context, as predicted by the Optimal Acceptance Threshold Model. I explored how non-nestmate age (young vs. old), stage of colony establishment (early vs. late), initial behavior of the non-nestmates (non-aggressive vs. aggressive), and the behavioral response by nestmates (non-aggressive vs. aggressive) affected the rates of acceptance. My results show an effect of both non-nestmate age and stage of colony development on non-nestmate acceptance. Young non-nestmates were more frequently accepted in early than in late colonies. Late colonies more frequently rejected both young and old non-nestmates, suggesting a cost of accepting potential usurpers into late colonies. Surprisingly, non-nestmate aggressive behavior did not have a direct effect on their acceptance, but it triggered an aggressive response from nestmates. These findings reveal a shift in the acceptance threshold, suggesting an effect of the social context and the specific needs of a colony on non-nestmate acceptance.


Acceptance threshold Context-dependent Non-nestmate Plasticity Primitively eusocial wasp 



I thank N. Tucci, C. Muniz, A. Murfin, Z. Buckley, F. Brand, and C. Beers for assistance in field experiments and the staff of Kendall Indian Hammocks Park for logistic support. O. Gaoue provided advice for GLM analysis. K. Waddington, W. Searcy, S. O'Donnell, A. Dubois, A. Uy, and members of the Uy and Searcy labs gave helpful comments to improve earlier versions of the manuscript. This study was funded by a Sigma Xi Grant in-Aid of Research, a GAFAC Funding Award, and the William H. Evoy Research Support Fund and complied with the regulations of the Miami-Dade County Parks & Recreation Department, with special thanks to Alicie Warren and Eduardo Salzedo for permit logistics.


  1. Akaike H (1973) Information theory as an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Second international symposium on information theory. Akademiai Kiado, Budapest, pp 267–281Google Scholar
  2. Arathi HS, Shakarad M, Gadagkar R (1997) Factors influencing the acceptance of alien conspecifics onto established nests of the primitively eusocial wasp, Ropadilia marginata. J Ins Behav 10:343–351CrossRefGoogle Scholar
  3. Brown JL (1987) Helping and communal breeding in birds: ecology and evolution. Princeton University Press, PrincetonGoogle Scholar
  4. Buczkowski G, Silverman J (2005) Context-dependent nestmate discrimination and the effect of action thresholds on exogenous cue recognition in the Argentine ant. Anim Beh 69:741–949CrossRefGoogle Scholar
  5. Burnham KP, Anderson DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Soc Method Res 33:261–305CrossRefGoogle Scholar
  6. Cant MA, Field J (2001) Helping effort and future fitness in cooperative animal societies. Proc R Soc Lond B 268:1959–1964CrossRefGoogle Scholar
  7. Carpenter JM, Hunt JH, Strassmann JE (2009) Mischocyttarus mexicanus cubicola: major extension of its range to Texas (Hymenoptera: Vespidae). Entomol Am 115:95–96Google Scholar
  8. Caswell H (2001) Matrix population models. Construction, analysis and interpretation. Sinauer, Sunderland, pp 333–334Google Scholar
  9. Cervo R, Lorenzi MC (1996) Behaviour in usurpers and late joiners of Polistes biglumis bimaculatus (Hymenoptera, Vespidae). Ins Soc 43:255–266CrossRefGoogle Scholar
  10. Clouse R (1995) Nest usurpation and intercolonial cannibalism in Mischocyttarus mexicanus (Hymenoptera: Vespidae). J Kansas Entomol Soc 68:67–73Google Scholar
  11. Clouse R (2001) Some effects of group size on the output of beginning nests of Mischocyttarus mexicanus (Hymenoptera: Vespidae). Fla Entomol 84:418–425CrossRefGoogle Scholar
  12. Couvillon MJ, Roy GF, Ratnieks FLW (2009) Recognition errors by honey bee (Apis mellifera) guards demonstrate overlapping cues in conspecific recognition. J Apicult Res 48:225–232CrossRefGoogle Scholar
  13. Couvillon MJ, Zweden JS, Ratnieks FLW (2012) Model of collective decision-making in nestmate recognition fails to account for individual discriminator responses and non-independent discriminator errors. Behav Ecol Sociobiol 66:339–341CrossRefGoogle Scholar
  14. Couvillon MJ, Segers FHID, Cooper-Bownan R, Truslove G, Nascimiento FS, Nascimiento FS, Ratnieks FSL (2013) Context affects nestmate recognition errors in honey bees and stingless bees. J Exp Biol 216:3055–3061PubMedCrossRefGoogle Scholar
  15. Crozier RH, Pamilo P (1996) Evolution of social insect colonies: sex allocation and kin selection. Oxford University Press, OxfordGoogle Scholar
  16. Downs SG, Ratnieks FLW (2000) Adaptive shifts in honey bee (Apis mellifera L.) guarding behavior support predictions of the acceptance threshold model. Beh Ecol 11:326–333CrossRefGoogle Scholar
  17. Dugatkin LA (1997) Cooperation among animals. Oxford University Press, OxfordGoogle Scholar
  18. Field J, Cronin A, Bridge C (2006) Future fitness and helping in social queues. Nature 441:214–217. doi: 10.1038/nature04560 PubMedCrossRefGoogle Scholar
  19. Foster KR (2009) A defense of sociobiology. Cold Spring Harbor Symp Quant Biol 74:403–418. doi: 10.1101/sqb.2009.74.041 PubMedCrossRefGoogle Scholar
  20. Gadagkar R (1985) Kin recognition in social insects and other animals—a review of recent findings and a consideration of their relevance for the theory of kin selection. Proc Indian Acad Sci (Anim Sci) 94:587–621CrossRefGoogle Scholar
  21. Gamboa GJ, Reeve HK, Ferguson ID, Wacker TL (1986a) Nestmate recognition in social wasps: the origin and acquisition of recognition odours. Anim Behav 34:685–695CrossRefGoogle Scholar
  22. Gamboa GJ, Reeve HK, Pfenning DW (1986b) The evolution and ontogeny of nestmate recognition in social wasps. Annu Rev Entomol 31:431–454CrossRefGoogle Scholar
  23. Gamboa GJ, Reeves HK, Holmes WG (1991a) Conceptual issues and methodology in kin-recognition research: a critical discussion. Ethol 88:109–127CrossRefGoogle Scholar
  24. Gamboa GJ, Foster RL, Scope JA, Bitterman AM (1991b) Effects of stage of colony cycle, context, and intercolony distance on conspecific tolerance by paper wasps (Polistes fuscatus). Behav Ecol Sociobiol 29:87–94CrossRefGoogle Scholar
  25. Gamboa GJ (1996) Kin recognition in social wasps. In: Turillazzi S, West-Eberhard MJ (eds) Natural history and the evolution of paper wasps. Oxford University Press, Oxford, pp 161–177Google Scholar
  26. Gamboa GJ (2004) Kin recognition in eusocial wasps. Ann Zool Fennici 41:789–808Google Scholar
  27. Gunnels CW (2007) Seasonally variable eusocially selected traits in the paper wasp, Mischocyttarus mexicanus. Ethol 113:648–660CrossRefGoogle Scholar
  28. Gunnels CW, Dubrovski A, Avalos A (2008) Social interactions as an ecological constrain in a eusocial insect. Anim Behav 75:681–691CrossRefGoogle Scholar
  29. Hamilton WD (1964) The evolution of social behavior. J Theor Biol 7:1–52PubMedCrossRefGoogle Scholar
  30. Heinze J (2010) Conflict and conflict resolution in social insects. In: Kappeler, P (ed) Animal behavior: evolution and mechanisms. Springer, HeidelbergGoogle Scholar
  31. Hermann HR, Gonzalas JM, Hermann BS (1985) Mischocyttarus mexicanus cubicola (Hymenoptera), distribution and nesting plants. Fla Entomol 68:609–614CrossRefGoogle Scholar
  32. Hsu YY, Early RL, Wolf LL (2006) Modulation of aggressive behavior by fighting experience: mechanisms and contest outcomes. Biol Rev 81:33–74PubMedGoogle Scholar
  33. Itô Y (1993) Behaviour and social evolution of wasps. Oxford University Press, Oxford, pp 53–65Google Scholar
  34. Johnson BR, van Wilgenburg E, Tsutsui ND (2011) Nestmate recognition in social insects: overcoming physiological constraints with collective decision making. Behav Ecol Sociobiol 65:935–944PubMedCentralPubMedCrossRefGoogle Scholar
  35. Judd TM (1998) Defensive behavior of colonies of the paper wasp, Polistes fuscatus, against vertebrate predators over the colony cycle. Ins Soc 45:197–208CrossRefGoogle Scholar
  36. Klahn JE (1988) Instraspecific comb usurpation in the social wasp Polistes fuscatus. Behav Ecol Sociobiol 23:1–8CrossRefGoogle Scholar
  37. Koenig WD, Dickinson JL (2004) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  38. Kûdo K, Tsuchida K, Mateus S, Zucchi R (2007) Nestmate recognition in a neotropical polygynous wasp. Insect Soc 54:29–33CrossRefGoogle Scholar
  39. Leadbeater E, Carruthers JM, Green JP, Field J (2010) Unrelated helpers in a primitively eusocial wasp: is helping tailored towards direct fitness? PLoS ONE 5(8):e11997. doi: 10.1371/journal.pone.0011997 PubMedCentralPubMedCrossRefGoogle Scholar
  40. Leadbeater E, Carruthers JM, Green JP, Rosser NS, Field J (2011) Nest inheritance is the missing source of direct fitness in a primitively eusocial insect. Science 333:874–876. doi: 10.1126/science.1205140 PubMedCrossRefGoogle Scholar
  41. Litte M (1977) Behavioral ecology of the social wasp, Mischocyttarus mexicanus. Behav Ecol Sociobiol 2:229–246CrossRefGoogle Scholar
  42. Lorenzi MC, Bagnères AG, Clément JL (1996) The role of cuticular hydrocarbons in insect societies: is it the same in paper wasps? In: Turillazzi S, West-Eberhard MJ (eds) Natural history and the evolution of paper wasps. Oxford University Press, Oxford, pp 178–189Google Scholar
  43. Lorenzi MC, Sledge MF, Laiolo P, Sturlini E, Turillazi S (2004) Cuticular hydrocarbon dynamics in young adult Polistes dominulus (Hymenoptera: Vespidae) and the role of linear hydrocarbons in nestmate recognition systems. J Insect Physiol 50:935–941PubMedCrossRefGoogle Scholar
  44. Mateo JM (2004) Recognition systems and biological organization: the perception component of social recognition. Ann Zool Fen 41:729–745Google Scholar
  45. McCulloch CE (2000) Generalized linear models. J Am Stat Assoc 95:1320–1324CrossRefGoogle Scholar
  46. Molina Y, O'Donnell S (2008) A developmental test of the dominance-nutrition hypothesis: linking adult feeding, aggression and reproductive potential in the paperwasp Mischocyttarus mastigophorus. Ethol Ecol Evol 20:125–139CrossRefGoogle Scholar
  47. Mora-Kepfer F (2011) Context-dependent behavior, reproduction and brain structure in newly-established colonies of the primitively eusocial wasp, Mischocyttarus mexicanus. Dissertation, University of MiamiGoogle Scholar
  48. Nelder JA, Wedderburn RWM (1972) Generalized Linear Models. J Roy Stat Soc A 135:370–384CrossRefGoogle Scholar
  49. Nonacs P, Reeve HK (1995) The ecology of cooperation in wasps: causes and consequences of alternative reproductive decisions. Ecology 76:953–996CrossRefGoogle Scholar
  50. O'Donnell S (1998) Dominance and polyethism in the eusocial paper wasp Mischocyttarus mastigophorus (Hymenoptera: Vespidae). Behav Ecol Sociobiol 43:327–331CrossRefGoogle Scholar
  51. Panek LM, Gamboa G, Espelie KE (2001) The effect of a wasp's age on its cuticular hydrocarbon profile and its tolerance by nestmate and non-nestmate conspecifics (Polistes fuscatus,Hymenoptera: Vespidae). Ethol 107:55–63CrossRefGoogle Scholar
  52. Penn DJ, Frommen JG (2010) Kin recognition: an overview of conceptual issues, mechanisms and evolutionary theory. In: Kappeler, P (ed) Animal behavior: evolution and mechanisms. Springer, HeidelbergGoogle Scholar
  53. Queller DC, Zacchi F, Cervo R, Turillazi S, Henshaw MT, Santorelli LA, Strassman JE (2000) Unrelated helpers in a social insect. Nature 405:784–787PubMedCrossRefGoogle Scholar
  54. R Development Core Team (2009). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL
  55. Reeve HK (1989) The evolution of conspecific acceptance thresholds. Am Nat 133:407–435CrossRefGoogle Scholar
  56. Reeve HK (1991) Polistes. In: Ross KG, Mathews RW (eds) The social biology of wasps. Comstock, London, pp 99–148Google Scholar
  57. Röseler PF (1991) Reproductive competition during colony establishment. In: Ross KG, Mathews RW (eds) The social biology of wasps. Comstock, London, pp 309–335Google Scholar
  58. Sherman PW, Reeve HK, Fenning DW (1997) Recognition systems. In: Krebs JR, Davies NB (eds) Behavioural ecology. An evolutionary approach. Blackwell, Oxford, pp 69–96Google Scholar
  59. Singer TL, Espelie KE (1992) Social wasps use nest paper hydrocarbons for nestmate recognition. Anim Behav 44:63–68CrossRefGoogle Scholar
  60. Sokal R, Rohlf FJ (1995) Biometry. W.H. Freeman, New York, pp 715–724Google Scholar
  61. Solomon NG, French JA (1997) Cooperative breeding in mammals. Cambridge University Press, CambridgeGoogle Scholar
  62. Soro A, Ayasse M, Zobel MU, Paxton RJ (2009) Complex sociogenetic organization and the origin of unrelated workers in a eusocial sweat bee, Lasioglossum malachurum. Insect Soc 56:55–63CrossRefGoogle Scholar
  63. SPSS, Inc (2008) SPSS Graduate Pack for Windows. SPSS, ChicagoGoogle Scholar
  64. Starks PT (1998) A novel ‘Sit and wait’ reproductive strategy in social wasps. Proc R Soc Lond B 265:1407–1410CrossRefGoogle Scholar
  65. Starks PT, Fischer DJ, Watson RE, Melikian GL, Nath SD (1998) Context-dependent nestmate discrimination in the paper wasp, Polistes dominulus: a critical test of the optimal acceptance threshold model. Anim Beh 56:449–458CrossRefGoogle Scholar
  66. Stuart RJ, Herbers JM (2000) Nest mate recognition in ants with complex colonies: within- and between-population variation. Behav Ecol 11:676–685CrossRefGoogle Scholar
  67. Sumner S, Lucas E, Barker J, Isaac NJB (2007) Radio-tagging technology reveals extreme nest drifting in a eusocial insect. Curr Bio 17:140–145CrossRefGoogle Scholar
  68. Trivers RL, Hare H (1976) Haplodiploidy and the evolution of social insects. Science 191:249–263PubMedCrossRefGoogle Scholar
  69. Waldman B (1987) Mechanisms of kin recognition. J Theor Biol 128:159–185CrossRefGoogle Scholar
  70. Van Wilgenburg E, Clémencet J, Tsutsui ND (2010) Experience influences aggressive behavior in the Argentine ant. Biol Lett 6:152–155PubMedCentralPubMedCrossRefGoogle Scholar
  71. Vander Meer RK, Saliwanchik D, Lavine (1989) Temporal changes in cuticular hydrocarbon patterns of Solenopsis invicta: implications for nestmate recognition. J Chem Ecol 15:2115–2125PubMedCrossRefGoogle Scholar
  72. Vásquez G, Silverman J (2010) Queen acceptance and the complexity of nestmate discrimination in the Argentine ant. Behav Ecol Sociobiol 62:537–548CrossRefGoogle Scholar
  73. West MJ (1967) Foundress associations in Polistinae wasps: dominance hierarchies and the evolution of social behavior. Science 157:1584–1585PubMedCrossRefGoogle Scholar
  74. West SA, Griffin AS, Gardner A (2007) Evolutionary explanations for cooperation. Curr Bio 17:R661–R672. doi: 10.1016/j.cub.2007.06.004 CrossRefGoogle Scholar
  75. Wilson EO (1971) The insect societies. Harvard University Press, Cambridge, 650 ppGoogle Scholar
  76. Zanette LR, Field J (2008) Genetic relatedness in early association of Polistes dominulus: from related to unrelated helpers. Mol Ecol 17:2590–2597PubMedCrossRefGoogle Scholar
  77. Zanette LR, Field J (2011) Founders versus joiners: group formation in the paper wasp Polistes dominulus. Anim Beh 82:699–705CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of BiologyUniversity of MiamiCoral GablesUSA

Personalised recommendations