Skip to main content
SpringerLink
Log in

When does cheating pay? Worker reproductive parasitism in honeybees

  • Review Article
  • Published:
Insectes Sociaux Aims and scope Submit manuscript

Abstract

The notion that honeybee colonies are harmonious, isolated societies in which workers selflessly sacrifice their reproductive opportunities to serve their queen has long been debunked. Like any society, honeybee colonies contain selfish individuals that pursue their own interests, or cheat, at the expense of the colony, and these individuals need to be controlled. There are numerous studies detailing the myriad ways in which selfish workers may subvert the typical dominance hierarchy of a haplo-diploid insect society. Recent studies have focussed on thelytoky, the ability to produce diploid offspring without mating, as the most significant attribute of a successful reproductive parasite. However, we argue that thelytoky is not necessary for successful parasitism, and that even arrhenotokous societies contain specialized reproductive parasites. Using A. mellifera and A. cerana as examples, we show that the most important aspects of a would-be reproductive cheat’s success are an ability to escape policing and the timing of the reproductive attempt. Finally, we show that thelytoky, while not necessary for the evolution of successful reproductive parasites, can give rise to specialized parasitic lineages and that such lineages are likely to be far more common than previously assumed.

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

Figure adapted from Beekman and Oldroyd (2008)

Fig. 2

Figure adapted from Beekman and Oldroyd (2008)

Similar content being viewed by others

References

  • Allsopp M (1992) The capensis calamity. South Afr Bee J 64:52–57

    Google Scholar 

  • Allsopp MH (1993) Summarised overview of the capensis problem. South Afr Bee J 65:127–136

    Google Scholar 

  • Allsopp MH, Beekman M, Gloag RS, Oldroyd BP (2010) Maternity of replacement queens in the thelytokous Cape honey bee Apis mellifera capensis. Behav Ecol Sociobiol 64:567–574. doi:10.1007/s00265-009-0872-9

    Article  Google Scholar 

  • Alves DA, Imperatriz-Fonseca VL, Francoy TM, Santos PS, Nogueira-Neto P, Billen J, Wenseleers T (2009) The queen is dead-long live the workers: intraspecific parasitism by workers in the stingless bee Melipona scutellaris. Mol Ecol 18:4102–4111. doi:10.1111/j.1365-294X.2009.04323.x

    Article  CAS  PubMed  Google Scholar 

  • Anderson RH (1963) The laying worker in the Cape honeybee, Apis mellifera capensis. J Apic Res 2:85–92

    Article  Google Scholar 

  • Arias MC, Sheppard WS (2005) Phylogenetic relationships of honey bees (Hymenoptera: Apinae: Apini) inferred from nuclear and mitochondrial DNA sequence data. Mol Phylogenet Evol 37:25–35. doi:10.1016/j.ympev.2005.02.017

    Article  CAS  PubMed  Google Scholar 

  • Bai ARK, Reddy CC (1975) Ovary development and egg laying in Apis cerana indica workers. J Apic Res 14:149–152

    Article  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 

  • Baudry E et al (2004) Whole-genome scan in thelytokous-laying workers of the Cape honeybee (Apis mellifera capensis): central fusion, reduced recombination rates and centromere mapping using half-tetrad analysis. Genetics 167:243–252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beekman M, Oldroyd BP (2008) When workers disunite: intraspecific parasitism by eusocial bees. Annu Rev Entomol 53:19–37

    Article  CAS  PubMed  Google Scholar 

  • Beekman M, Ratnieks FLW (2003) Power over reproduction in social Hymenoptera. Philos Trans R Soc B 358:1741–1754

    Article  Google Scholar 

  • Beekman M, Calis JNM, Boot WJ (2000) Parasitic honeybees get royal treatment. Nature 404:723

    Article  CAS  PubMed  Google Scholar 

  • Beekman M, Good G, Allsopp MH, Radloff S, Pirk CWW, Ratnieks FLW (2002) A non-policing honey bee colony (Apis mellifera capensis). Naturwissenschaften 89:479–482. doi:10.1007/s00114-002-0365-4

    Article  CAS  PubMed  Google Scholar 

  • Beekman M, Allsopp MH, Wossler TC, Oldroyd BP (2008) Factors affecting the dynamics of the honeybee (Apis mellifera) hybrid zone of South Africa. Heredity 100:13–18

    Article  CAS  PubMed  Google Scholar 

  • Beekman M, Allsopp MH, Jordan LA, Lim J, Oldroyd BP (2009) A quantitative study of worker reproduction in queenright colonies of the Cape honey bee, Apis mellifera capensis. Mol Ecol 18:2722–2727. doi:10.1111/j.1365-294X.2009.04224.x

    Article  PubMed  Google Scholar 

  • Beetsma J (1979) The process of queen-worker differentiation in the honey-bee. Bee World 60:24–39

    Article  CAS  Google Scholar 

  • Birmingham AL, Hoover SE, Winston ML, Ydenberg RC (2004) Drifting bumble bee (Hymenoptera: Apidae) workers in commercial greenhouses may be social parasites. Can J Zool Rev Can Zool 82:1843–1853. doi:10.1139/z04-181

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Bourke AFG (2011) Principles of Social Evolution. Oxford University Press, Oxford

    Book  Google Scholar 

  • Chaline N, Ratnieks FLW, Burke T (2002) Anarchy in the UK: detailed genetic analysis of worker reproduction in a naturally occurring British anarchistic honeybee, Apis mellifera, colony using DNA microsatellites. Mol Ecol 11:1795–1803. doi:10.1046/j.1365-294X.2000.01569.x

    Article  CAS  PubMed  Google Scholar 

  • Chapman NC, Nanork P, Reddy MS, Bhat NS, Beekman M, Oldroyd BP (2008) Nestmate recognition by guards of the Asian hive bee Apis cerana. Insect Soc 55:382–386

    Article  Google Scholar 

  • Chapman NC, Makinson J, Beekman M, Oldroyd BP (2009a) Honeybee, Apis mellifera, guards use adaptive acceptance thresholds to limit worker reproductive parasitism. Anim Behav 78:1205–1211

    Article  Google Scholar 

  • Chapman NC, Nanork P, Gloag RS, Wattanachaiyingcharoen W, Beekman M, Oldroyd BP (2009b) Queenless colonies of the Asian red dwarf honey bee (Apis florea) are infiltrated by workers from other queenless colonies. Behav Ecol 20:817–820. doi:10.1093/beheco/arp065

    Article  Google Scholar 

  • Chapman NC, Beekman M, Oldroyd BP (2010a) Worker reproductive parasitism and drift in the western honeybee Apis mellifera. Behav Ecol Sociobiol 64:419–427

    Article  Google Scholar 

  • Chapman NC, Higgs JS, Wattanachaiyingcharoen W, Beekman M, Oldroyd BP (2010b) Worker reproductive parasitism in naturally orphaned colonies of the Asian red dwarf honey bee, Apis florea. Insect Soc 57:163–167. doi:10.1007/s00040-009-0061-x

    Article  Google Scholar 

  • Dampney JR, Barron AB, Oldroyd BP (2002) Policing of adult honey bees with activated ovaries is error prone. Insect Soc 49:270–274. doi:10.1007/s00040-002-8313-z

    Article  Google Scholar 

  • Darwin C (1859) On the Origin of Species by Means of Natural Selection. John Murray, London

    Google Scholar 

  • Dietemann V, Neumann P, Härtel S, Pirk CWW, Crewe RM (2007) Pheromonal dominance and the selection of a socially parasitic honeybee worker lineage (Apis mellifera capensis Esch.). J Evol Biol 20:997–1007

    Article  CAS  PubMed  Google Scholar 

  • Dobata S, Sasaki T, Mori H, Hasegawa E, Shimada M, Tsuji K (2009) Cheater genotypes in the parthenogenetic ant Pristomyrmex punctatus. Proc R Soc B 276:567–574

    Article  CAS  PubMed  Google Scholar 

  • Dobata S, Sasaki T, Mori H, Hasegawa E, Shimada M, Tsuji K (2011) Persistence of the single lineage of transmissible ‘social cancer’ in an asexual ant. Mol Ecol 20:441–455. doi:10.1111/j.1365-294X.2010.04954.x

    Article  PubMed  Google Scholar 

  • Downs SG, Ratnieks FLW (1999) Recognition of conspecifics by honeybee guards uses nonheritable cues acquired in the adult stage. Anim Behav 58:643–648. doi:10.1006/anbe.1999.1177

    Article  CAS  PubMed  Google Scholar 

  • Downs SG, Ratnieks FLW (2000) Adaptive shifts in honey bee (Apis mellifera L.) guarding behavior support predictions of the acceptance threshold model. Behav Ecol 11:326–333. doi:10.1093/beheco/11.3.326

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Engel MS, Schultz TR (1997) Phylogeny and behavior in honey bees (Hymenoptera: Apidae). Ann Entomol Soc Am 90:43–53

    Article  Google Scholar 

  • Engelstädter J, Sandrock C, Vorburger C (2011) Contagious parthenogenesis, automixis, and a sex determination meltdown. Evolution 65:501–511

    Article  PubMed  Google Scholar 

  • Foret S, Kucharski R, Pellegrini M, Feng S, Jacobsen SE, Robinson GE, Maleszka R (2012) DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees. Proc Natl Acad Sci 109:4968–4973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fournier D, Estoup A, Orivel J, Foucaud J, Jourdan H, Le Breton J, Keller L (2005) Clonal reproduction by males and females in the little fire ant. Nature 435:1230–1234

    Article  CAS  PubMed  Google Scholar 

  • Free JB (1958) The drifting of honey bees. J Agric Sci 51:294–306. doi:10.1017/S0021859600035103

    Article  Google Scholar 

  • Ghoul M, Griffin AS, West SA (2014) Toward an evolutionary definition of cheating. Evolution 68:318–331. doi:10.1111/evo.12266

    Article  PubMed  Google Scholar 

  • Goudie F, Oldroyd BP (2014) Thelytoky in the honey bee. Apidologie 45:306–326. doi:10.1007/s13592-013-0261-2

    Article  Google Scholar 

  • Goudie F, Allsopp MH, Beekman M, Oxley PR, Lim J, Oldroyd BP (2012) Maintenance and loss of heterozygosity in a thelytokous lineage of honey bees (Apis mellifera capensis). Evolution 66:1897–1906. doi:10.1111/j.1558-5646.2011.01543.x

    Article  PubMed  Google Scholar 

  • Greeff JM (1996) Effects of thelytokous worker reproduction on kin-selection and conflict in the Cape honeybee, Apis mellifera capensis. Phil Trans R Soc Lond B 351:617–625

    Article  Google Scholar 

  • Hamilton WD (1964a) The genetical evolution of social behaviour I. J Theor Biol 7:1–16

    Article  CAS  PubMed  Google Scholar 

  • Hamilton WD (1964b) The genetical evolution of social behaviour II. J Theor Biol 7:17–52

    Article  CAS  PubMed  Google Scholar 

  • Hardin G (1968) The tragedy of the commons. Science 162:1243–1248

    Article  CAS  PubMed  Google Scholar 

  • Härtel S, Neumann P, Raassen FS, Moritz RFA, Hepburn HR (2006) Social parasitism by Cape honeybee workers in colonies of their own subspecies (Apis mellifera capensis Esch.). Insect Soc 53:183–193

    Article  Google Scholar 

  • Hepburn HR (1992) Pheromonal and ovarial development covary in Cape worker honeybees, Apis mellifera capensis. Naturwissenschaften 79:523–524

    Article  Google Scholar 

  • Holmes MJ, Oldroyd BP, Allsopp MH, Lim J, Wossler TC, Beekman M (2010) Maternity of emergency queens in the Cape honey bee, Apis mellifera capensis. Mol Ecol 19:2792–2799. doi:10.1111/j.1365-294X.2010.04683.x

    Article  CAS  PubMed  Google Scholar 

  • Holmes MJ, Oldroyd BP, Duncan M, Allsopp MH, Beekman M (2013a) Cheaters sometimes prosper: targeted worker reproduction in honeybee (Apis mellifera) colonies during swarming. Mol Ecol 22:4298–4306. doi:10.1111/mec.12387

    Article  PubMed  Google Scholar 

  • Holmes MJ, Tan K, Wang Z, Oldroyd BP, Beekman M (2013b) Honeybee (Apis cerana) guards do not discriminate between robbers and reproductive parasites. Insect Soc 60:265–271. doi:10.1007/s00040-013-0292-8

    Article  Google Scholar 

  • Holmes MJ, Tan K, Wang Z, Oldroyd BP, Beekman M (2014a) Effect of queen excluders on ovary activation in workers of the Eastern honeybee Apis cerana. Insect Soc 61:191–196. doi:10.1007/s00040-014-0344-8

    Article  Google Scholar 

  • Holmes MJ, Tan K, Wang Z, Oldroyd BP, Beekman M (2014b) Why acquiesce? Worker reproductive parasitism in the Eastern honeybee (Apis cerana). J Evol Biol 27:939–949. doi:10.1111/jeb.12366

    Article  CAS  PubMed  Google Scholar 

  • Holmes MJ, Tan K, Wang Z, Oldroyd BP, Beekman M (2015) Genetic reincarnation of workers as queens in the Eastern honeybee Apis cerana. Heredity 114:65–68. doi:10.1038/hdy.2014.70

    Article  CAS  PubMed  Google Scholar 

  • Imperatiz-Fonseca VL, Zucchi R (1995) Virgin queens in stingless bee (Apidae, Meliponinae) colonies: a review. Apidologie 26:231–244

    Article  Google Scholar 

  • Jordan LA, Allsopp MH, Oldroyd BP, Wossler TC, Beekman M (2008) Cheating honeybee workers produce royal offspring. Proc R Soc B 275:345–351. doi:10.1098/rspb.2007.1422

    Article  PubMed  Google Scholar 

  • Katzav-Gozansky T, Soroker V, Kamer J, Schulz CM, Francke W, Hefetz A (2003) Ultrastructural and chemical characterization of egg surface of honeybee worker and queen-laid eggs. Chemoecology 13:129–134

    Article  CAS  Google Scholar 

  • Kropacova S, Haslbachova H (1969) The development of ovaries in worker honeybees in a queenright colony. J Apic Res 8:57–64

    Article  Google Scholar 

  • Lo N, Gloag RS, Anderson DL, Oldroyd BP (2010) A molecular phylogeny of the genus Apis suggests that the Giant Honey Bee of the Philippines, A. breviligula Maa, and the Plains Honey Bee of southern India, A. indica Fabricius, are valid species. Syst Entomol 35:226–233. doi:10.1111/j.1365-3113.2009.00504.x

    Article  Google Scholar 

  • Lopez-Vaamonde C, Koning JW, Brown RM, Jordan WC, Bourke AFG (2004) Social parasitism by male-producing reproductive workers in a eusocial insect. Nature 430:557–560. doi:10.1038/nature02769

    Article  CAS  PubMed  Google Scholar 

  • Makert GR, Paxton RJ, Hartfelder K (2006) Ovariole number—a predictor of differential reproductive success among worker subfamilies in queenless honeybee (Apis mellifera L.) colonies. Behav Ecol Sociobiol 60:815–825. doi:10.1007/s00265-006-0225-x

    Article  Google Scholar 

  • Martin SJ, Chaline N, Ratnieks FLW, Jones GR (2005) Searching for the egg-marking signal in honeybees. J Negative Res Ecol Evol Biol 2:1–9

    Google Scholar 

  • Miller DG, Ratnieks FLW (2001) The timing of worker reproduction and breakdown of policing behaviour in queenless honey bee (Apis mellifera L.) societies. Insect Soc 48:178–184. doi:10.1007/pl00001762

    Article  Google Scholar 

  • Monnin T, Ratnieks FLW (2001) Policing in queenless ponerine ants. Behav Ecol Sociobiol 50:97–108. doi:10.1007/s002650100351

    Article  Google Scholar 

  • Monnin T, Ratnieks FLW, Jones GR, Beard R (2002) Pretender punishment induced by chemical signalling in a queenless ant. Nature 419:61–65. doi:10.1038/nature00932

    Article  CAS  PubMed  Google Scholar 

  • Montague CE, Oldroyd BP (1998) The evolution of worker sterility in honey bees: an investigation into a behavioral mutant causing failure of worker policing. Evolution 52:1408–1415. doi:10.2307/2411310

    Article  Google Scholar 

  • Moritz RFA, Kryger P, Allsopp MH (1996) Competition for royalty in bees. Nature 384:31. doi:10.1038/384031a0

    Article  CAS  Google Scholar 

  • Moritz RFA, Kryger P, Allsopp MH (1999) Lack of worker policing in the Cape honeybee (Apis mellifera capensis). Behaviour 136:1079–1092. doi:10.1163/156853999501766

    Article  Google Scholar 

  • Moritz RFA, Lattorff HMG, Neumann P, Kraus FB, Radloff SE, Hepburn HR (2005) Rare royal families in honeybees, Apis mellifera. Naturwissenschaften 92:488–491

    Article  CAS  PubMed  Google Scholar 

  • Moritz RFA, Pirk CWW, Hepburn HR, Neumann P (2008) Short-sighted evolution of virulence in parasitic honeybee workers (Apis mellifera capensis Esch.). Naturwissenschaften 95:507–513. doi:10.1007/s00114-008-0351-6

    Article  CAS  PubMed  Google Scholar 

  • Nanork P, Paar J, Chapman NC, Wongsiri S, Oldroyd BP (2005) Asian honeybees parasitize the future dead. Nature 437:829

    Article  CAS  PubMed  Google Scholar 

  • Nanork P, Chapman NC, Wongsiri S, Lim J, Gloag RS, Oldroyd BP (2007a) Social parasitism by workers in queenless and queenright Apis cerana colonies. Mol Ecol 16:1107–1114

    Article  CAS  PubMed  Google Scholar 

  • Nanork P, Wongsiri S, Oldroyd BP (2007b) Preservation and loss of the honey bee (Apis) egg-marking signal across evolutionary time. Behav Ecol Sociobiol 61:1509–1514. doi:10.1007/s00265-007-0382-6

    Article  Google Scholar 

  • Neumann P, Hepburn R (2002) Behavioural basis for social parasitism of Cape honeybees (Apis mellifera capensis). Apidologie 33:165–192

    Article  Google Scholar 

  • Neumann P, Radloff S, Pirk C, Hepburn R (2003) The behaviour of drifted Cape honeybee workers (Apis mellifera capensis): predisposition for social parasitism? Apidologie 34:585–590

    Article  Google Scholar 

  • Niu D-F, Pirk CWW, Zheng H-Q, Ping S, Shi J-H, Cao L-F, Hu F-L (2016) Reproductive traits and mandibular gland pheromone of anarchistic honey bee workers Apis mellifera occurring in China. Apidologie 47:515–526

    Article  CAS  Google Scholar 

  • Oldroyd BP, Osborne KE (1999) The evolution of worker sterility in honeybees: the genetic basis of failure of worker policing. Proc R Soc Lond Ser B Biol Sci 266:1335–1339

    Article  Google Scholar 

  • Oldroyd BP, Wongsiri S (2006) Asian Honey Bees: Biology, Conservation and Human Interactions. Harvard University Press, Cambridge

    Google Scholar 

  • Oldroyd BP, Smolenski AJ, Cornuet JM, Crozier RH (1994) Anarchy in the beehive. Nature 371:749. doi:10.1038/371749a0

    Article  CAS  Google Scholar 

  • Oldroyd BP et al (2001) Worker policing and worker reproduction in Apis cerana. Behav Ecol Sociobiol 50:371–377. doi:10.1007/s002650100376

    Article  Google Scholar 

  • Oldroyd BP, Allsopp MH, Gloag RS, Lim J, Jordan LA, Beekman M (2008) Thelytokous parthenogenesis in unmated queen honeybees (Apis mellifera capensis): central fusion and high recombination rates. Genetics 180:359–366

    Article  PubMed  PubMed Central  Google Scholar 

  • Oldroyd BP, Allsopp MH, Lim J, Beekman M (2011) A thelytokous lineage of socially parasitic honey bees has retained heterozygosity despite at least 10 years of inbreeding. Evolution 65:860–868. doi:10.1111/j.1558-5646.2010.01164.x

    Article  PubMed  Google Scholar 

  • Oldroyd BP, Allsopp MH, Roth KM, Remnant EJ, Drewell RA, Beekman M (2014) A parent-of-origin effect on honeybee worker ovary size. Proc R Soc Lond B Biol Sci 281:20132388

    Article  Google Scholar 

  • Onions GW (1912) South African ‘fertile’ worker bees. South Afr Bee J 1:720–728

    Google Scholar 

  • Page RE, Erickson EH (1988) Reproduction by worker honey bees (Apis mellifera L.). Behav Ecol Sociobiol 23:117–126. doi:10.1007/bf00299895

    Article  Google Scholar 

  • Pearcy M, Hardy O, Aron S (2006) Thelytokous parthenogenesis and its consequences on inbreeding in an ant. Heredity 96:377–382

    Article  CAS  PubMed  Google Scholar 

  • Perepelova LI (1929) Laying workers, the oviposition of the queen, and swarming. Bee World 10:69–71

    Article  Google Scholar 

  • Pfeiffer KJ, Crailsheim K (1998) Drifting of honeybees. Insect Soc 45:151–167. doi:10.1007/s000400050076

    Article  Google Scholar 

  • Pirk CWW, Neumann P, Hepburn HR (2002) Egg laying and egg removal by workers are positively correlated in queenright Cape honeybee colonies (Apis mellifera capensis). Apidologie 33:203–211. doi:10.1051/apido:2002004

    Article  Google Scholar 

  • Pirk CWW, Neumann P, Ratnieks FLW (2003) Cape honeybees, Apis mellifera capensis, police worker-laid eggs despite the absence of relatedness benefits. Behav Ecol 14:347–352. doi:10.1093/beheco/14.3.347

    Article  Google Scholar 

  • Rabeling C, Kronauer DJC (2013) Thelytokous parthenogenesis in eusocial Hymenoptera. Annu Rev Entomol 58:273–292

    Article  CAS  Google Scholar 

  • Raffiudin R, Crozier RH (2007) Phylogenetic analysis of honey bee behavioral evolution. Mol Phylogenet Evol 43:543–552. doi:10.1016/j.ympev.2006.10.013

    Article  CAS  PubMed  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 (1995) Evidence for a queen-produced egg-marking pheromone and its use in worker policing in the honey-bee. J Apic Res 34:31–37

    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. doi:10.1016/s0022-5193(05)80647-2

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ratnieks FLW, Foster KR, Wenseleers T (2006) Conflict resolution in insect societies. Annu Rev Entomol 51:581–608. doi:10.1146/annurev.ento.51.110104.151003

    Article  CAS  PubMed  Google Scholar 

  • Remnant EJ et al (2016) Parent-of-origin effects on genome-wide DNA methylation in the Cape honey bee (Apis mellifera capensis) may be confounded by allele-specific methylation. BMC Genom 17:226

    Article  CAS  Google Scholar 

  • Riehl C, Frederickson ME (2016) Cheating and punishment in cooperative animal societies. Philos Trans R Soc Lond B Biol Sci. doi:10.1098/rstb.2015.0090

    Google Scholar 

  • Sakagami SF (1954) Occurrence of an aggressive behaviour in queenless hives, with considerations on the social organisation of honeybee. Insect Soc 1:331–343

    Article  Google Scholar 

  • Santos PD, Alves DD, Eterovic A, Imperatiz-Fonseca VL, Kleinert ADP (2006) Numerical investment in sex and caste by stingless bees (Apidae: Meliponini): a comparative analysis. Apidologie 37:207–221. doi:10.1051/apido:2006015

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Simon UE, Moritz RFA, Crewe RM (2005) Reproductive dominance among honeybee workers in experimental groups of Apis mellifera capensis. Apidologie 36:413–419

    Article  Google Scholar 

  • Smith ML, Loope KJ (2016) Caught in an evolutionary trap: worker honey bees that have drifted into foreign colonies do not invest in ovary activation. Insect Soc 63:61–65. doi:10.1007/s00040-015-0434-2

    Article  Google Scholar 

  • Tan K et al (2009) Worker reproduction in mixed-species colonies of honey bees. Behav Ecol 20:1106–1110. doi:10.1093/beheco/arp103

    Article  Google Scholar 

  • Teseo S, Kronauer DJC, Jaisson P, Chaline N (2013) Enforcement of reproductive synchrony via policing in a clonal ant. Curr Biol 23:328–332. doi:10.1016/j.cub.2013.01.011

    Article  CAS  PubMed  Google Scholar 

  • Toth E, Queller DC, Dollin A, Strassmann JE (2004) Conflict over male parentage in stingless bees. Insect Soc 51:1–11. doi:10.1007/s00040-003-0707-z

    Article  Google Scholar 

  • Tsuji K, Dobata S (2011) Social cancer and the biology of the clonal ant Pristomyrmex punctatus (Hymenoptera: Formicidae). Myrmecol News 15:91–99

    Google Scholar 

  • Van Oystaeyen A, Alves DA, Oliveira RC, do Nascimento DL, do Nascimento FS, Billen J, Wenseleers T (2013) Sneaky queens in Melipona bees selectively detect and infiltrate queenless colonies. Anim Behav 86:603–609. doi:10.1016/j.anbehav.2013.07.001

    Article  Google Scholar 

  • Verma S, Ruttner F (1983) Cytological analysis of the thleytokous parthenogenesis in the Cape honeybee (Apis mellfera capensis Escholtz). Apidologie 14:41–57. doi:10.1051/apido:19830104

    Article  Google Scholar 

  • Visscher PK (1989) A quantitative study of worker reproduction in honey bee colonies. Behav Ecol Sociobiol 25:247–254. doi:10.1007/bf00300050

    Article  Google Scholar 

  • Visscher PK, Dukas R (1995) Honey bees recognize development of nestmates’ ovaries. Anim Behav 49:542–544

    Article  Google Scholar 

  • Wang Y, Kaftanoglu O, Fondrk MK, Page RE Jr (2014) Nurse bee behaviour manipulates worker honeybee (Apis mellifera L.) reproductive development. Anim Behav 92:253–261. doi:10.1016/j.anbehav.2014.02.012

    Article  Google Scholar 

  • Wenseleers T, Ratnieks FLW (2004) Tragedy of the commons in Melipona bees. Proc R Soc B Biol Sci 271:S310–S312. doi:10.1098/rsbl.2003.0159

    Article  Google Scholar 

  • Wenseleers T, Ratnieks FLW (2006a) Comparative analysis of worker reproduction and policing in eusocial Hymenoptera supports relatedness theory. Am Nat 168:E163–E179. doi:10.1086/508619

    Article  PubMed  Google Scholar 

  • Wenseleers T, Ratnieks FLW (2006b) Enforced altruism in insect societies. Nature 444:50. doi:10.1038/444050a

    Article  CAS  PubMed  Google Scholar 

  • Wenseleers T, Hart AG, Ratnieks FLW (2004a) When resistance is useless: policing and the evolution of reproductive acquiescence in insect societies. Am Nat 164:E154–E167

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wenseleers T, Alves DA, Francoy TM, Billen J, Imperatriz-Fonseca VL (2011) Intraspecific queen parasitism in a highly eusocial bee. Biol Lett 7:173–176. doi:10.1098/rsbl.2010.0819

    Article  PubMed  Google Scholar 

  • Winston ML (1987) The Biology of the Honey Bee. Harvard University Press, Cambridge

    Google Scholar 

  • Woyciechowski M, Kuszewska K (2012) Swarming generates rebel workers in honeybees. Curr Biol 22:707–711. doi:10.1016/j.cub.2012.02.063

    Article  CAS  PubMed  Google Scholar 

  • Woyciechowski M, Lomnicki A (1987) Multiple mating of queens and the sterility of workers among eusocial Hymenoptera. J Theor Biol 128:317–327. doi:10.1016/s0022-5193(87)80074-7

    Article  Google Scholar 

  • Zanette LRS, Miller SDL, Faria CMA, Almond EJ, Huggins TJ, Jordan WC, Bourke AFG (2012) Reproductive conflict in bumblebees and the evolution of worker policing. Evolution 66:3765–3777. doi:10.1111/j.1558-5646.2012.01709.x

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Ben Oldroyd, Ken Tan, Mike Allsopp and members of the Behaviour and Genetics of Social Insects Laboratory, whose ideas contributed to this review. This research was supported by Australian Research Council Grants (MB: FT120100120 and DP0878924) and an Endeavour Research Fellowship (MJH).

Author information

Authors and Affiliations

  1. Behaviour and Genetics of Social Insects Laboratory, School of Life and Environmental Sciences, University of Sydney, Macleay A12 Science Rd, Sydney, NSW, 2006, Australia

    M. J. Holmes & M. Beekman

  2. Plant Health Australia, Level 1, 1 Phipps Close, Deakin, ACT, 2600, Australia

    M. J. Holmes

Authors
  1. M. J. Holmes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Beekman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. J. Holmes.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Holmes, M.J., Beekman, M. When does cheating pay? Worker reproductive parasitism in honeybees. Insect. Soc. 64, 5–17 (2017). https://doi.org/10.1007/s00040-016-0515-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-016-0515-x

Keywords

Search

Navigation