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Apidologie

, Volume 45, Issue 3, pp 306–326 | Cite as

Thelytoky in the honey bee

  • Frances GoudieEmail author
  • Benjamin P. Oldroyd
Review article

Abstract

Thelytoky, the asexual production of females, is rare in honey bees. However, it is ubiquitous in workers of the Cape honey bee Apis mellifera capensis. Thelytoky allows some workers to be reincarnated into the queen phenotype, and thereby selects for reproductive competition among workers. Thelytoky also acts as an exaptation for the emergence of reproductive parasites, the most extreme example of which is an entirely clonal ‘cancerous’ lineage of workers (the Clone) that lethally parasitises colonies of another subspecies Apis mellifera scutellata. The Clone is an enigma because thelytoky results in the accumulation of homozygosity at any loci that are free to recombine, yet the Clone retains considerable heterozygosity. The Clone pays a cost for its thelytoky: the selective removal of homozygous offspring at each generation. We propose that workers, queens and Clones have differing abilities to endure the costs and benefits of sex and asexuality, accounting for the heterogeneous distribution of reproductive strategies across the A. mellifera capensis population. We further suggest that multiple factors must fall into place for thelytoky to emerge as an effective reproductive strategy in a honey bee population, and that geographic isolation resulting in genetic drift and founder effects may have enabled thelytoky to emerge in A. mellifera capensis. Finally, we consider the honey bee in the broader context of haplodiploid Hymenoptera, and argue that constraints on the evolution of sex in non-haplodiploid taxa may make sexual reproduction an evolutionary ‘one-way street’.

Keywords

Apis mellifera Apis mellifera capensis asexual thelytoky reproductive parasitism 

Notes

References

  1. Allsopp, M. (1992) The Capensis calamity. South African Bee Journal 64, 52–55Google Scholar
  2. Allsopp, M., Crewe, R.M. (1993) The Cape honeybee as a Trojan horse rather than the hordes of Jenghiz Khan. Am. Bee. J. 133, 121–123Google Scholar
  3. Allsopp, M., Calis, J.M., Boot, W. (2003) Differential feeding of worker larvae affects caste characters in the Cape honeybee, Apis mellifera capensis. Behav. Ecol. Sociobiol. 54, 555–561Google Scholar
  4. Allsopp, M., Beekman, M., Gloag, R., Oldroyd, B.P. (2010) Maternity of replacement queens in the thelytokous Cape honey bee Apis mellifera capensis. Behav. Ecol. Sociobiol. 64, 567–574Google Scholar
  5. Amdam, G.V., Seehuus, S.C. (2006) Order, disorder, death: lessons from a superorganism. Adv. Cancer Res. 95, 31–60PubMedCentralPubMedGoogle Scholar
  6. Amdam, G.V., Norberg, K., Fondrk, M.K., Page, R.E. (2004) Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. Proc. Natl. Acad. Sci. USA 101, 11350–11355PubMedCentralPubMedGoogle Scholar
  7. Barron, A.B., Oldroyd, B.P., Ratnieks, F.L.W. (2001) Worker reproduction in honey-bees (Apis) and the anarchic syndrome: a review. Behav. Ecol. Sociobiol. 50, 199–208Google Scholar
  8. Baudry, E., Kryger, P., Allsopp, M., Koeniger, N., Vautrin, D., 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, 243–252PubMedCentralPubMedGoogle Scholar
  9. Beekman, M., Oldroyd, B. (2008a) Who is the Queen's mother? Royal cheats in social insects. J. Biosci. 33, 159–161PubMedGoogle Scholar
  10. Beekman, M., Oldroyd, B.P. (2008b) When workers disunite: intraspecific parasitism in eusocial bees. Annu. Rev. Entomol. 53, 19–37PubMedGoogle Scholar
  11. Beekman, M., Calis, J.N.M., Boot, W.J. (2000) Parasitic honeybees get royal treatment. Nature 404, 723PubMedGoogle Scholar
  12. Beekman, M., Good, G., Allsopp, M., Radloff, S., Pirk, C., et al. (2002) A non-policing honey bee colony (Apis mellifera capensis). Naturwissenschaften 89, 479–482PubMedGoogle Scholar
  13. Beekman, M., Allsopp, M.H., Wossler, T.C., Oldroyd, B.P. (2008) Factors affecting the dynamics of the honeybee (Apis mellifera) hybrid zone of South Africa. Heredity 100, 13–18PubMedGoogle Scholar
  14. Beekman, M., Allsopp, M.H., Jordan, L.A., Lim, J., Oldroyd, B.P. (2009) A quantitative study of worker reproduction in queenright colonies of the Cape honey bee, Apis mellifera capensis. Mol. Ecol. 18, 2722–2727PubMedGoogle Scholar
  15. Beekman, M., Allsopp, M.H., Lim, J., Goudie, F., Oldroyd, B.P. (2011) Asexually produced Cape honeybee queens (Apis mellifera capensis) reproduce sexually. J. Hered. 102, 562–566PubMedGoogle Scholar
  16. Beekman, M., Allsopp, M., Holmes, M., Lim, J., Noach-Pienaar, L.-A., et al. (2012) Racial mixing in South African honeybees: the effects of genotype mixing on reproductive traits of workers. Behav. Ecol. Sociobiol. 66, 897–904Google Scholar
  17. Bessoltane, N., Toffano-Nioche, C., Solignac, M., Mougel, F. (2012) Fine scale analysis of crossover and non-crossover and detection of recombination sequence motifs in the honeybee (Apis mellifera). PLoS Biol. 7, e36229Google Scholar
  18. Beye, M., Hasselmann, M., Fondrk, M.K., Page, R.E., Omholt, S.W. (2003) The gene cds is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114, 419–429PubMedGoogle Scholar
  19. Beye, M., Gattermeier, I., Hasselmann, M., Gemp, T., Schioett, M., et al. (2006) Exceptionally high levels of recombination across the honey bee genome. Genome Res. 16, 1339–1344PubMedCentralPubMedGoogle Scholar
  20. Blacher P., Yagound B., Lecoutey E., Devinne P., Chameron S., et al. (2013) Drifting behaviour as an alternative reproductive strategy for social insect workers. Proc. R. Soc. B. doi:  http://dx.doi.org/10.1098/rspb
  21. Bull, J.J. (1994) Perspective—virulence. Evolution 48, 1423–1437Google Scholar
  22. Calis, J.N.M., Boot, W.J., Allsopp, M.H., Beekman, M. (2002) Getting more than a fair share: nutrition of worker larvae related to social parasitism in the Cape honey bee Apis mellifera capensis. Apidologie 33, 193–202Google Scholar
  23. Châline, N., Ratnieks, F.L.W., 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, 1795–1803PubMedGoogle Scholar
  24. Chapman, N.C., Nanork, P., Gloag, R.S., Wattanachaiyingcharoen, W., Beekman, M., et al. (2009) Queenless colonies of the Asian red dwarf honey bee (Apis florea) are infiltrated by workers from other queenless colonies. Behav. Ecol. 20, 817–820Google Scholar
  25. Cobey, S. (1999) The African bee, Apis mellifera scutellata, threatened in her South African homeland by the Cape bee, Apis melliera capensis. Am. Bee. J. 139, 462–467Google Scholar
  26. Daly, H.V. (1966) Biological studies on Ceratina dallatorreana, an alien bee in California which reproduces by parthenogenesis (Hymenoptera: Apoidea). Ann. Entomol. Sco. Am. 59, 1138–1154Google Scholar
  27. Dietemann, V., Lubbe, A., Crewe, R.M. (2006a) Human factors facilitating the spread of a parasitic honey bee in South Africa. J. Econ. Entomol. 99, 7–13PubMedGoogle Scholar
  28. Dietemann, V., Pflugfelder, J., Härtel, S., Neumann, P., Crewe, R. (2006b) Social parasitism by honeybee workers (Apis mellifera capensis Esch.): evidence for pheromonal resistance to host queen's signals. Behav. Ecol. Sociobiol. 60, 785–793Google Scholar
  29. Engelstadter, J. (2008) Constraints on the evolution of asexual reproduction. BioEssays 30, 1138–1150PubMedGoogle Scholar
  30. Engelstadter, J., Sandrock, C., Vorburger, C. (2010) Contagious parthenogenesis, automixis, and a sex determination meltdown. Evolution 65, 501–511PubMedGoogle Scholar
  31. Fournier, D., Estoup, A., Orivel, R.M., Foucaud, J., Jourdan, H., et al. (2005) Clonal reproduction by males and female in the little fire ant. Nature 435, 1230–1234PubMedGoogle Scholar
  32. Gladyshev, E., Meselson, M. (2008) Extreme resistance of bdelloid rotifers to ionizing radiation. Proc. Natl. Acad. Sci. USA 105, 5139–5144PubMedCentralPubMedGoogle Scholar
  33. Goudie, F., Allsopp, M.H., Beekman, M., Lim, J., Oldroyd, B.P. (2012a) Heritability of worker ovariole number in the Cape honey bee Apis mellifera capensis. Insectes Soc. 59, 351–359Google Scholar
  34. Goudie, F., Allsopp, M.H., Beekman, M., Oxley, P.R., Lim, J., et al. (2012b) Maintenance and loss of heterozygosity in a thelytokous lineage of honey bees (Apis mellifera capensis). Evolution 66, 1897–1906PubMedGoogle Scholar
  35. Goudie, F., Allsopp, M.H., Oldroyd, B.P. (2014) Selection on overdominant genes maintains heterozygosity along multiple chromosomes in a clonal lineage of honey bee. Evolution 68, 125–136Google Scholar
  36. Greeff, J.M. (1996) Effects of thelytokous worker reproduction on kin-selection and conflict in the Cape honeybee, Apis mellifera capensis. Philos. Trans.: Biol Sci. 351, 617–625Google Scholar
  37. Greeff, J.M., Villet, M.H. (1993) Deducing the coefficient of relationship by the amount of recombination produced during automictic parthneogenesis. Heredity 70, 499–502Google Scholar
  38. Gruber M., Hoffmann B., Ritchie P., Lester P.. (2010) Crazy ant sex: genetic caste determination, clonality, and inbreeding in a apopulation of invasive Yellow crazy ants. In: Nash D.R., den Boer S.P.A., Fine Licht H.H., and Boomsma J.J. (Eds.), XVI Congress of the International Union for the Study of Social Insects, Copenhagen, Denmark.Google Scholar
  39. Hagimori, T., Abe, Y., Date, S., Miura, K. (2006) The first finding of a Rickettsia bacterium associated with parthenogenesis induction among insects. Curr. Microbiol. 52, 97–101PubMedGoogle Scholar
  40. Hamilton, W.D. (1964) The genetical evolution of social behaviour. I & II. J. Theor. Biol. 7, 1–52PubMedGoogle Scholar
  41. Härtel, S., Neumann, P., Kryger, P., von der Heide, C., Moltzer, G., et al. (2006) Infestation levels of Apis mellifera scutellata swarms by socially parasitic Cape honeybee workers (Apis mellifera capensis). Apidologie 37, 462–470Google Scholar
  42. Härtel, S., Wossler, T., Moltzer, G.-J., Crewe, R., Moritz, R.A., et al. (2011) Pheromone-mediated reproductive dominance hierarchies among pseudo-clonal honeybee workers (Apis mellifera capensis). Apidologie 42, 659–668Google Scholar
  43. Hepburn, H.R., Allsopp, M.H. (1994) Reproductive conflict between honeybees: usurpation of Apis mellifera scutellata colonies by Apis mellifera capensis. Suid-Afrikaanse Tydskrif vir Wetenskap 90, 247–249Google Scholar
  44. Hepburn, H.R., Crewe, R.M. (1990) Defining the Cape honeybee: reproductive traits of queenless workers. S. Afr. J. Sci. 86, 524–527Google Scholar
  45. Hepburn, H.R., Crewe, R.M. (1991) Portrait of the Cape honeybee, Apis mellifera capensis. Apidologie 22, 567–580Google Scholar
  46. Hepburn, H.R., Radloff, S.E. (1998) Honeybees of Africa. Springer, BerlinGoogle Scholar
  47. Heubel, K.U., Rankin, D.J., Kokko, H. (2009) How to go extinct by mating too much: population consequences of male mate choice and efficiency in a sexual-asexual species complex. Oikos 118, 513–520Google Scholar
  48. Hillesheim, E., Koeniger, N., Moritz, R.F.A. (1989) Colony performance in honeybees (Apis mellifera capensis Esch.) depends on the proportion of subordinate and dominant workers. Behav Ecol Sociobiol 24, 291–296Google Scholar
  49. Hölldobler, B., Wilson, E.O. (2008) The superorganism: the beauty, elegance, and strangeness of insect societies. W. W Norton, New YorkGoogle Scholar
  50. Holmes, M.J., Oldroyd, B.P., Allsopp, M.H., Lim, J., Wossler, T.C., et al. (2010) Maternity of emergency queens in the Cape honey bee, Apis mellifera capensis. Mol. Ecol. 19, 2792–2799PubMedGoogle Scholar
  51. Holmes, M.J., Oldroyd, B.P., Duncan, M., Allsopp, M.H., Beekman, M. (2013) Cheaters sometimes prosper: targeted worker reproduction in honeybee (Apis mellifera) colonies during swarming. Mol. Ecol. 22, 4298–4306PubMedGoogle Scholar
  52. Huigens, M.E., Stouthamer, R. (2003) Parthenogenesis associated with Wolbachia. In: Bourtzis, K., Miller, T.A. (eds.) Insect symbiosis, pp. 247–266. CRC Press, Boca RatonGoogle Scholar
  53. Jarosch, A., Stolle, E., Crewe, R.M., Moritz, R.F.A. (2011) Alternative splicing of a single transcription factor drives selfish reproductive behavior in honeybee workers (Apis mellifera). Proc. Natl. Acad. Sci. USA 108, 15282–15287PubMedCentralPubMedGoogle Scholar
  54. Johnson, B.R., Linksvayer, T.A. (2010) Deconstructing the superorganism: social physiology, reproductive groundplans, and sociogenomics. Q. Rev. Biol. 85, 57–79PubMedGoogle Scholar
  55. Jones, J., Myerscough, M., Graham, S., Oldroyd, B.P. (2004) Honey bee nest thermoregulation: diversity promotes stability. Science 305, 402–404PubMedGoogle Scholar
  56. Jordan, L.A., Allsopp, M.H., Oldroyd, B.P., Wossler, T.C., Beekman, M. (2008) Cheating honeybee workers produce royal offspring. Proc. R. Soc. Lond. B. Biol. Sci. 275, 345–351Google Scholar
  57. Keller, L. (2007) Uncovering the biodiversity of genetic and reproductive systems: time for a more open approach—American Society of Naturalists E.O. Wilson award winner address. Am. Nat. 169, 1–8PubMedGoogle Scholar
  58. Kobayashi, K., Hasegawa, E., Ohkawara, K. (2008) Clonal reproduction by males of the ant Vollenhovia emeryi (Wheeler). Entomol. Sci. 11, 167–172Google Scholar
  59. Koetz A. (2013) The Asian honey bee (Apis cerana) and its strains—with special focus on Apis cerana Java genotype. Literature review. Brisbane.Google Scholar
  60. Kryger, K. (2001) The Capensis pseudo-clone, a social parasite of African honey bees. In: Menzel, R., Rademacher, E. (eds.) International Union for the Study of Social Insects, p. 208. IUSSI, BerlinGoogle Scholar
  61. Lattorff, H.M.G., Kryger, P., Moritz, R.F.A. (2005) Queen developmental time and fitness consequences for queens of clonal social parasitic honeybees (A. m. capensis) and its host A. m. scutellata. Insectes Soc 52, 238–241Google Scholar
  62. Levin, B.R. (1996) The evolution and maintenance of virulence in microparasites. Emerg. Infect. Dis. J 2, 93–102Google Scholar
  63. Mackensen, O. (1943) The occurrence of parthenogenetic females in some strains of honey-bees. J. Econ. Entomol. 36, 465–467Google Scholar
  64. Maynard Smith, J. (1978) The Evolution of Sex. Cambridge University PressGoogle Scholar
  65. Mark Welch, J.L., Mark Welch, D.B., Meselson, M. (2004) Cytogenetic evidence for asexual evolution of bdelloid rotifers. Proc. Natl. Acad. Sci. USA 101, 1618–1621PubMedGoogle Scholar
  66. Martin, S., Wossler, T., Kryger, P. (2002) Usurpation of African Apis mellifera scutellata colonies by parasitic Apis mellifera capensis workers. Apidologie 33, 215–232Google Scholar
  67. Mattila, H.R., Seeley, T.D. (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317, 362–364PubMedGoogle Scholar
  68. Montague, C.E., Oldroyd, B.P. (1998) The evolution of worker sterility in honey bees: an investigation into a behavioral mutant causing failure of worker policing. Evolution 52, 1408–1415Google Scholar
  69. Moritz, R. (2002) Population dynamics of the Cape bee phenomenon: the impact of parasitic laying worker clones in apiaries and natural populations. Apidologie 33, 233–244Google Scholar
  70. Moritz, R.F.A., Fuchs, S. (1998) Organization of honeybeee colonies: characteristics and consequences of a superorganism concept. Apidologie 29, 7–21Google Scholar
  71. Moritz, R.F., Haberl, M. (1994) Lack of meiotic recombination in thelytokous parthenogenesis of laying workers of Apis mellifera capensis (the Cape honeybee). Heredity 73, 98–102Google Scholar
  72. Moritz, R.F.A., Southwick, E.E. (1992) Bees as superorganisms. Springer, BerlinGoogle Scholar
  73. Moritz, R.F.A., Kryger, P., Allsopp, M.H. (1996) Competition for royalty in bees. Nature 384, 31Google Scholar
  74. Moritz, R.F.A., Kryger, P., Allsopp, M.H. (1999) Lake of worker policing in the Cape honeybee (Apis mellifera capensis). Behaviour 136, 1079–1092Google Scholar
  75. Moritz, R.F.A., Pflugfelder, J., Crewe, R.M. (2003) Lethal fighting between honeybee queens and parasitic workers (Apis mellifera). Naturwissenschaften 90, 378–381PubMedGoogle Scholar
  76. Moritz, R.F.A., Lattorff, H.M.G., Crewe, R.M. (2004) Honeybee workers (Apis mellifera capensis) compete for producing queen-like pheromone signals. Proc. R. Soc. Lond. B. Biol. Sci. 271(Supplement 3), S98–S100Google Scholar
  77. Moritz, R., Pirk, C.W.W., Hepburn, H.R., Neumann, P. (2008) Short-sighted evolution of virulence in parasitic honeybee workers (Apis mellifera capensis Esch.). Naturwissenschaften 95, 507–513PubMedGoogle Scholar
  78. Moritz, R.F.A., Lattorff, H.M.G., Crous, K.L., Hepburn, H.R. (2011) Social parasitism of queens and workers in the Cape honeybee (Apis mellifera capensis). Behav. Ecol. Sociobiol. 65, 735–740Google Scholar
  79. Nanork, P., Paar, J., Chapman, N.C., Wongsiri, S., Oldroyd, B.P. (2005) Asian honey bees parasitize the future dead. Nature 437, 829PubMedGoogle Scholar
  80. Nanork, P., Chapman, N.C., Wongsiri, S., Lim, J., Gloag, R.S., et al. (2007) Social parasitism by workers in queenless and queenright Apis cerana colonies. Mol. Ecol. 16, 1107–1114PubMedGoogle Scholar
  81. Neumann, P., Hepburn, H.R. (2002) Behavioural basis for social parasitism of Cape honeybees (Apis mellifera capensis). Apidologie 33, 165–192Google Scholar
  82. Neumann, P., Moritz, R.F.A. (2002) The Cape honeybee phenomenon: the sympatric evolution of a social parasite in real time? Behav. Ecol. Sociobiol. 52, 271–281Google Scholar
  83. Neumann, P., Radloff, S.E., Moritz, R.F.A., Hepburn, H.R., Reece, S.L. (2001) Social parasitism by honeybee workers (Apis mellifera capensis Escholtz): host finding and resistance of hybrid host colonies. Behav. Ecol. 12, 419–428Google Scholar
  84. Neumann, P., Härtel, S., Kryger, P., Crewe, R.M., Moritz, R.F.A. (2011) Reproductive division of labour and thelytoky result in sympatric barriers to gene flow in honeybees (Apis mellifera L.). J. Evol. Biol. 24, 286–294PubMedGoogle Scholar
  85. Normark, B.B. (2003) The evolution of alternative genetic systems in insects. Annu. Rev. Entomol. 48, 397–423PubMedGoogle Scholar
  86. Oldroyd, B.P. (2002) The Cape honeybee: an example of a social cancer. Trends Ecol. Evol. 17, 249–251Google Scholar
  87. Oldroyd, B.P., Beekman, M. (2008) Effects of selection for honey bee worker reproduction on foraging traits. PLoS Biol. 6, e56PubMedCentralPubMedGoogle Scholar
  88. Oldroyd, B.P., Fewell, J.H. (2007) Genetic diversity promotes homeostasis in insect colonies. Trends Ecol. Evol. 22, 408–413PubMedGoogle Scholar
  89. Oldroyd, B. P., Smolenski, A. J., Cornuet, J.-M., Crozier, R. H. (1994) Anarchy in the beehive. Nature 371, 749Google Scholar
  90. Oldroyd, B.P., Allsopp, M.H., Gloag, R.S., Lim, J., Jordan, L.A., et al. (2008) Thelytokous parthenogenesis in unmated queen honeybees (Apis mellifera capensis): central fusion and high recombination rates. Genetics 180, 359–366PubMedCentralPubMedGoogle Scholar
  91. Oldroyd, B.P., Allsopp, M.H., 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, 860–868PubMedGoogle Scholar
  92. Onions, G.W. (1912) South African ‘fertile worker bees’. Agr. J. U. S. Afr. 1, 720–728Google Scholar
  93. Otto, S.P., Gerstein, A.C. (2006) Why have sex? The population genetics of sex and recombination. Biochem. Soc. Trans. 34(Part 4), 519–522PubMedGoogle Scholar
  94. Page, R.E. (2013) The spirit of the hive. The mechanisms of social evolution. Harvard University Press, Cambridge, MAGoogle Scholar
  95. Palmer, K.A., Oldroyd, B.P. (2000) Evolution of multiple mating in the genus Apis. Apidologie 31, 235–248Google Scholar
  96. Pearcy, M., Aron, S., Doums, C., Keller, L. (2004) Conditional use of sex and parthenogenesis for worker and queen production in ants. Science 306, 1780–1783PubMedGoogle Scholar
  97. Pearcy, M., Hardy, O., Aron, S. (2006) Thelytokous parthenogenesis and its consequences on inbreeding in an ant. Heredity 96, 377–382PubMedGoogle Scholar
  98. Phiancharoen, M., Pirk, C.W.W., Radloff, S., Hepburn, R. (2010) Clinal nature of the frequencies of ovarioles and spermathecae in Cape worker honeybees, Apis mellifera capensis. Apidologie 41, 129–134Google Scholar
  99. Pirk, C.W.W., Neumann, P., Hepburn, H.R. (2002) Egg laying and egg removal by workers are positively correlated in queenright Cape honeybee colonies (Apis mellifera capensis). Apidologie 33, 203–211Google Scholar
  100. Rabeling, C., Kronauer, D.J.C. (2013) Thelytokous parthenogenesis in eusocial hymenoptera. Annu. Rev. Entomol. 58, 273–292PubMedGoogle Scholar
  101. Ratnieks, F.L.W. (1988) Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am. Nat. 132, 217–236Google Scholar
  102. Ratnieks, F.L.W., Visscher, P.K. (1989) Worker policing in honeybees. Nature 342, 796–797Google Scholar
  103. Ravary, F., Jaisson, P. (2004) Absence of individual sterility in thelytokous colonies of the ant Cerapachys biroi Forel (Formicidae, Cerapachyinae). Insectes Soc. 51, 67–73Google Scholar
  104. Ruttner, F. (1977) The problem of the cape bee (Apis mellifera capensis Escholtz): parthenogenesis—size of population—evolution. Apidologie 8, 281–294Google Scholar
  105. Seeley, T.D. (1989) The honey bee colony as a superorganism. Am. Scientist 77, 546–553Google Scholar
  106. Seeley, T.D. (2010) Honeybee democracy. Princeton University Press, Princeton, NJGoogle Scholar
  107. Seeley, T.D., Tarpy, D.R. (2007) Queen promiscuity lowers disease within honeybee colonies. Proc. R. Soc. B 274, 67–72PubMedCentralPubMedGoogle Scholar
  108. Siddle, H.V., Kaufman, J. (2013) A tale of two tumours: comparison of the immune escape strategies of contagious cancers. Mol. Immunol. 55, 190–193PubMedCentralPubMedGoogle Scholar
  109. Solignac, M., Vautrin, D., Baudry, E., Mougel, F., Loiseau, A., et al. (2004) A microsatellite-based linkage map of the honeybee, Apis mellifera L. Genetics 167, 253–262PubMedCentralPubMedGoogle Scholar
  110. Solignac, M., Mougel, F., Vautrin, D., Monnerot, M., Cornuet, J.-M. (2007) A third-generation microsatellite-based linkage map of the honey bee, Apis mellifera, and its comparison with the sequence-based physical map. Genome Biol. 8, R66PubMedCentralPubMedGoogle Scholar
  111. Sumner, S., Keller, L. (2008) Social evolution: reincarnation, free-riding and inexplicable modes of reproduction. Curr. Biol. 18, R206–R207PubMedGoogle Scholar
  112. Suomalainen, E., Saura, A., Lokki, J. (1987) Cytology and evolution in parthenogenesis. CRC Press, Boca Raton, FLGoogle Scholar
  113. Tiedemann, R., Moll, K., Paulus, K.B., Schlupp, I. (2005) New microsatellite loci confirm hybrid origin, parthenogenetic inheritance, and mitotic gene conversion in the gynogenetic Amazon molly (Poecilia formosa). Mol. Ecol. Notes 5, 586–589Google Scholar
  114. Tribe, G.D. (1983) What is the Cape bee? South African Bee Journal 55, 77–87Google Scholar
  115. Verma, S., Ruttner, F. (1983) Cytological analysis of thelytokous parthenogenesis in the Cape honey bee Apis mellifera capensis. Apidologie 14, 41–57Google Scholar
  116. Visscher, P.K. (1989) A quantitative study of worker reproduction in honey bee colonies. Behav. Ecol. Sociobiol. 25, 247–254Google Scholar
  117. Weinberg, R. (1998) One renegade cell: the quest for the origins of cancer. Phoenix, LondonGoogle Scholar
  118. Wenseleers, T., Alves, D.A., Francoy, T.M., Billen, J., Imperatiz-Fonseca, V.L. (2011) Intraspecific queen parasitism in a highly eusocial bee. Biol. Lett. 7, 173–176PubMedCentralPubMedGoogle Scholar
  119. Wheeler, W.M. (1911) The ant-colony as an organism. Morphology 22, 307–325Google Scholar
  120. White, M. (1984) Chromosomal mechanisms in animal reproduction. Bull. Zoo. 51, 1–23Google Scholar
  121. Winston, M.L. (1991) The biology of the honey bee. Harvard University Press, HarvardGoogle Scholar
  122. Wirtz, P., Beetsma, J. (1972) Induction of caste differentiation in the honey bee (Apis mellifera) by juvenile hormone. Entomol. Exp. Appl. 15, 517–520Google Scholar
  123. Woyke, J. (1963) What happens to diploid drone larvae in a honeybee colony? J. Apic. Res. 2, 73–75Google Scholar
  124. Zchori-Fein, E., Gottlieb, Y., Kelly, S.E., Brown, J.K., Wilson, J.M., et al. (2001) A newly discovered bacterium associated with parthenogenesis and a change in host selection behavior in parasitoid wasps. Proc. Natl. Acad. Sci. USA 98, 12555–12560PubMedCentralPubMedGoogle Scholar

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© INRA, DIB and Springer-Verlag France 2014

Authors and Affiliations

  1. 1.Behavior and Genetics of Social Insects Laboratory A12University of SydneySydneyAustralia

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