Abstract
In insect societies, workers often try to challenge the reproductive monopoly of the queen by laying their own eggs. Successful worker reproduction, however, is frequently prevented by queen policing or worker policing, whereby either the mother queen or non-reproductive workers selectively kill worker-laid eggs. Recently, a third mechanism—“selfish” worker policing—has also been described in which the workers selectively police worker-laid eggs but also lay eggs themselves. Here, we present results from the monogynous wasp Dolichovespula norwegica, which show that all three kinds of policing—queen policing, worker policing and “selfish” worker policing—co-occur. The net effect of these three kinds of policing collectively favoured the queen’s reproduction, as within 1 day 44% of the worker-laid eggs versus only 8% of the queen-laid eggs were eaten. Of the worker-laid eggs that were killed by workers, approximately two thirds were eaten by the reproductive workers even though these made up only a small proportion, 8%, of the work force. This means that policing workers obtained both direct fitness benefits as well as indirect (inclusive) fitness. In addition, we show that worker policing was carried out by a limited, specialised set of workers that was estimated to constitute approximately one quarter of the whole colony and of which 66% were non-reproductive.
References
Bonckaert W, Vuerinckx K, Billen J, Hammond RL, Keller L, Wenseleers T (2008) Worker policing in the German wasp Vespula germanica. Behav Ecol 19:272–278
Boomsma JJ, Ratnieks FLW (1996) Paternity in eusocial Hymenoptera. Philos Trans R Soc Lond B Biol Sci 351:947–975
Bourke AFG (1988) Worker reproduction in the higher eusocial Hymenoptera. Q Rev Biol 63:291–311
Bourke AFG (1999) Colony size, social complexity and reproductive conflict in social insects. J Evol Biol 12:245–257
Bourke AFG (2005) Genetics, relatedness and social behaviour in insect societies. In: Fellowes MDE, Holloway GJ, Rolff J (eds) Insect evolutionary ecology. CABI, Wallingford, pp 1–30
Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton
Brunner E, Heinze E (2009) Worker dominance and policing in the ant Temnothorax unifasciatus. Insect Soc 56:397–404
Crozier RH, Pamilo P (1996) Evolution of social insect colonies. Sex allocation and kin selection. Oxford University Press, Oxford
D’Ettorre P, Heinze J, Ratnieks FLW (2004) Worker policing by egg-eating in the ponerine ant Pachycondyla inversa. Proc R Soc Lond B Biol Sci 271:1427–1434
Daly D, Archer ME, Watts PC, Speed MP, Hughes MR, Barker FS, Jones J, Odgaard K, Kemp SJ (2002) Polymorphic microsatellite loci for eusocial wasps (Hymenoptera: Vespidae). Mol Ecol Notes 2:273–275
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
Foster K, Ratnieks F (2000) Facultative worker policing in a wasp. Nature 407:692–693
Foster KR, Ratnieks FLW (2001a) Paternity, reproduction and conflict in vespine wasps: a model system for testing kin selection predictions. Behav Ecol Sociobiol 50:1–8
Foster KR, Ratnieks FLW (2001b) The effect of sex-allocation biasing on the evolution of worker policing in hymenopteran societies. Am Nat 158:615–624
Foster KR, Ratnieks FLW (2001c) Convergent evolution of worker policing by egg eating in the honeybee and common wasp. Proc R Soc Lond B 268:169–174
Foster KR, Ratnieks FLW, Gyllenstrand N, Thoren PA (2001) Colony kin structure and male production in Dolichovespula wasps. Mol Ecol 10:1003–1010
Foster KR, Gulliver J, Ratnieks FLW (2002) Worker policing in the European hornet Vespa crabro. Insect Soc 49:41–44
Halling LA, Oldroyd BP, Wattanachaiyingcharoen W, Barron AB, Nanork P, Wongsiri S (2001) Worker policing in the bee Apis florea. Behav Ecol Sociobiol 49:509–513
Hamilton WD (1964) The genetical evolution of social behaviour I & II. J Theor Biol 7:1–52
Hammond RL, Keller L (2004) Conflict over male parentage in social insects. PLoS Biol 2:1–11
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
Helanterä H, Tofilski A, Wenseleers T, Ratnieks FLW (2006) Worker policing in the common wasp Vespula vulgaris is not aimed at improving colony hygiene. Insect Soc 53:399–402
Hughes WOH, Oldroyd BP, Beekman M, Ratnieks FLW (2008) Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320:1213–1216
Kellner K, Trindl A, Heinze J, D’Ettorre P (2007) Polygyny and polyandry in small ant societies. Mol Ecol 16:2363–2369
Lee ET, Wang JW (2003) Statistical methods for survival data analysis, 3rd edn. Wiley-Interscience, Hoboken
Liebig J, Monnin T, Turillazzi S (2005) Direct assessment of queen quality and lack of worker suppression in a paper wasp. Proc R Soc Lond B Biol Sci 272:1339–1344
Michener CD, Brothers DJ (1974) Were workers of eusocial Hymenoptera initially altruistic or oppressed. Proc Natl Acad Sci U S A 71:671–674
Monnin T, Peeters C (1997) Cannibalism of subordinates’ eggs in the monogynous queenless ant Dinoponera quadriceps. Naturwissenschaften 84:499–502
Nielsen R, Tarpy DR, Reeve HK (2003) Estimating effective paternity number in social insects and the effective number of alleles in a population. Mol Ecol 12:3157–3164
Nonacs P (2006) Nepotism and brood reliability in the suppression of worker reproduction in the eusocial Hymenoptera. Biol Lett 2:577–579
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
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
Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, Princeton
Pamilo P (1991) Evolution of colony characteristics in social insects 1. Sex allocation. Am Nat 137:83–107
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
Queller DC (2000) Relatedness and the fraternal major transitions. Phil Trans R Soc Lond B 355:1647–1655
Queller DC, Strassmann JE (1998) Kin selection and social insects. Bioscience 48:165–175
Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat 132:217–236
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
Ratnieks FLW, Visscher PK (1989) Worker policing in the honeybee. Nature 342:796–797
Ratnieks FLW, Foster KR, Wenseleers T (2006) Conflict resolution in insect societies. Annu Rev Entomol 51:581–608
Robinson GE (1992) Regulation of division of labor in insect societies. Annu Rev Entomol 37:637–665
Saigo T, Tsuchida K (2004) Queen and worker policing in monogynous and monandrous colonies of a primitively eusocial wasp. Proc R Soc Lond B Biol Sci (Suppl) 271:S509–S512
Starr CK (1984) Sperm competition, kinship, and sociality: a review of modern theory. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic, Orlando, pp 427–464
Stroeymeyt N, Brunner E, Heinze J (2007) “Selfish worker policing” controls reproduction in a Temnothorax ant. Behav Ecol Sociobiol 61:1449–1457
Thorén PA, Paxton RJ, Estoup A (1995) Unusually high frequency of (CT)n and (GT)n microsatellite loci in a yellow jacket wasp, Vespula rufa (L.) (Hymenoptera: Vespidae). Insect Mol Biol 5:141–148
Trivers RL, Hare H (1976) Haplodiploidy and the evolution of the social insects. Science 191:249–263
van Zweden JS, Furst MA, Heinze J, D’Ettorre P (2007) Specialization in policing behaviour among workers in the ant Pachycondyla inversa. Proc R Soc B Biol Sci 274:1421–1428
Velthuis HHW, Araujo Alves D de, Imperatriz-Fonseca VL, Duchateau MJ (2002) Worker bees and the fate of their eggs. Proc Exp Appl Entomol NEV Amsterdam 13:97–102
Wang J (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166:1963–1979
Wang J, Santure AW (2009) Parentage and sibship inference from multilocus genotype data under polygamy. Genetics 181:1579–1594
Wenseleers T, Ratnieks FLW (2006a) Comparative analysis of worker reproduction and policing in eusocial Hymenoptera supports relatedness theory. Am Nat 168:E163–E179
Wenseleers T, Ratnieks FLW (2006b) Enforced altruism in insect societies. Nature 444:50–50
Wenseleers T, Tofilski A, Ratnieks FLW (2005a) Queen and worker policing in the tree wasp Dolichovespula sylvestris. Behav Ecol Sociobiol 58:80–86
Wenseleers T, Badcock NS, Erven K, Tofilski A, Nascimento FS, Hart AG, Burke TA, Archer ME, Ratnieks FLW (2005b) A test of worker policing theory in an advanced eusocial wasp, Vespula rufa. Evolution 59:1306–1314
Wilson EO (1971) The insect societies. Harvard University Press, Cambridge
Acknowledgements
We would like to thank the Institute for the Promotion of Innovation through Science and Technology in Flanders (IWT-Vlaanderen) and the Research Foundation Flanders (grant no. GNM-B5996-KAN2006) for funding. We are also very grateful to Kristel Vuerinckx and Tom Vanhove for help with video analysis and to Kristien Erven for help with the genotyping.
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Bonckaert, W., Tofilski, A., Nascimento, F.S. et al. Co-occurrence of three types of egg policing in the Norwegian wasp Dolichovespula norwegica . Behav Ecol Sociobiol 65, 633–640 (2011). https://doi.org/10.1007/s00265-010-1064-3
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DOI: https://doi.org/10.1007/s00265-010-1064-3