Abstract
Unlike workers of all other honey bee (Apis mellifera) subspecies, workers of the Cape honey bee of South Africa (A. mellifera capensis) reproduce thelytokously and are thus able to produce female offspring that are pseudoclones of themselves. This ability allows workers to compete with their queen over the maternity of daughter queens and, in one extreme case, has led to a clonal lineage of workers becoming a social parasite in commercially managed populations of A. mellifera scutellata. Previous work (Jordan et al., Proc R Soc Lond B Biol Sci 275:345, 2008) showed that, in A. mellifera capensis, 59% of queen cells produced during swarming events contained the offspring of workers and that, of these, 65% were the offspring of non-natal workers. Here, we confirm that a substantial proportion (38.5%) of offspring queens is worker-laid. We additionally show that: (1) Although queens produce most diploid female offspring sexually, we found some homozygous or hemizygous queen offspring, suggesting that queens also reproduce by thelytoky. These parthenogenetic individuals are probably nonviable beyond the larval stage. (2) Worker-laid offspring queens are viable and become the resident queen at the same frequency as do sexually produced queen-laid offspring queens. (3) In this study, all but one of the worker-derived queens were laid by natal workers rather than workers from another nest. This suggests that the very high rates of social parasitism observed in our previous study were enhanced by beekeeping manipulations, which increased movement of parasites between colonies.
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Baudry E, Solignac M, Garnery L, Gries M, Cornuet J-M, Koeniger N (1998) Relatedness among honeybees (Apis mellifera) of a drone congregation. Proc R Soc Lond B Biol Sci 265:2009–2014
Baudry E, Kryger P, Allsopp M, Koeniger N, Vautrin D, Mougel F, Cornuet J-M, Solignac M (2004) Whole genome scan in thelytokous-laying workers of the Cape honey bee (Apis mellifera capensis): central fusion, reduced recombination rates and centromere mapping using half-tetrad analysis. Genetics 167:243–252
Beekman M, Oldroyd BP (2008) When workers disunite: intraspecific parasitism in eusocial bees. Annu Rev Entomol 53:19–37
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
Bernasconi G, Ratnieks FLW, Rand E (2000) Effect of “spraying” by fighting honey bee queens (Apis mellifera L.) on the temporal structure of fights. Insect Soc 47:21–26
Beye M, Hasselmann M, Fondrk MK, Page RE, Omholt SW (2003) The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114:419–429
Boot WJ, Calis JNM, Allsopp M (2008) Selection for reproductive workers in the Cape honeybee population, Apis mellifera capensis, leads to social parasitism in bee colonies from the savanna. Proc Neth Entomol Soc Meet 19:41–52
Châline N, Ratnieks FLW, Raine NE, Badcock NS, Burke T (2004) Non-lethal sampling of honey bee, Apis mellifera, DNA using wing tips. Apidologie 35:311–318
Crewe R, Allsopp M (1994) Sex and the single queen: recent experiments with capensis and scutellata queens. S Afr Bee J 66:58–62
Dade HA (1977) Anatomy and dissection of the honeybee. International Bee Research Association, London
deGrandi-Hoffman G, Watkins JC, Collins AM, Loper GM, Martin JH, Arais MC, Sheppard WS (1998) Queen development time as a factor in the Africanization of European honey bee (Hymenoptera: Apidae) populations. Ann Entomol Soc Am 91:52–58
Duchateau MJ, van Leeuwen P (1990) Early sex determination in larvae of Bombus terrestris. Insect Soc 37:232–235
Evans JD, Wheeler DE (1999) Differential gene expression between developing queens and workers in the honey bee, Apis mellifera. Proc Natl Acad Sci U S A 96:5575–5580
Fletcher DJC (1978) The African bee, Apis mellifera adansonii, in Africa. Annu Rev Entomol 23:151–171
Gilley DC (2001) The behavior of honey bees (Apis mellifera ligustica) during queen duels. Ethology 107:601–622
Gilley DC, Tarpy DR (2005) Three mechanisms of queen elimination in swarming honey bee colonies. Apidologie 36:461–474
Greeff JM (1996) Effects of thelytokous worker reproduction on kin-selection and conflict in the Cape honeybee, Apis mellifera capensis. Philos Trans R Soc Lond B 351:617–625
Hayashi Y, Lo N, Miyata H, Kitade O (2007) Sex-linked genetic influence on caste determination in a termite. Science 318:985–987
Hughes WOH, Boomsma JJ (2008) Genetic royal cheats in leaf-cutting ant societies. Proc Natl Acad Sci U S A 105:5150–5153
Jay SC (1966) Drifting of honeybees in commercial apiaries. II Effect of various factors when hives are arranged in rows. J Apic Res 5:103–112
Jones J, Myerscough M, Graham S, Oldroyd BP (2004) Honey bee nest thermoregulation: diversity promotes stability. Science 305:402–404
Jordan LA, Allsopp MH, Oldroyd BP, Wossler TC, Beekman M (2008) Cheating honeybee workers produce royal offspring. Proc R Soc Lond B Biol Sci 275:345–351
Kerr WE, Nielsen RA (1966) Evidences that genetically determined Melipona queens can become workers. Genetics 54:859–866
Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317:362–364
Moritz RFA, Kryger P, Allsopp MH (1996) Competition for royalty in bees. Nature 384:31
Moritz RFA, Beye M, Hepburn HR (1998) Estimating the contribution of laying workers to population fitness in African honeybees (Apis mellifera) with molecular markers. Insectes Soc 45:277–287
Oldroyd BP, Fewell JH (2007) Genetic diversity promotes homeostasis in insect colonies. Trends Ecol Evol 22:408–413
Oldroyd BP, Smolenski AJ, Cornuet J-M, Wongsiri S, Estoup A, Rinderer TE, Crozier RH (1996) Levels of polyandry and intracolonial genetic relationships in Apis dorsata (Hymenoptera: Apidae). Ann Entomol Soc Am 89:276–283
Oldroyd BP, Allsopp MH, Gloag RS, Lim J, Jordan LA, Beekman M (2008) Thelytokous parthenogenesis in unmated queen honey bees (Apis mellifera capensis): central fusion and high recombination rates. Genetics 180:359–366
Osborne KE, Oldroyd BP (1999) Possible causes of reproductive dominance during emergency queen rearing by honeybees. Anim Behav 58:267–272
Page RE, Erickson EH (1986) Kin recognition during emergency queen rearing by worker honey bees (Hymenoptera: Apidae). Ann Entomol Soc Am 79:460–467
Page RE, Robinson GE, Fondrk MK (1989) Genetic specialists, kin recognition and nepotism in honey-bee colonies. Nature 338:576–579
Pearcy M, Aron S, Doums C, Keller L (2004) Conditional use of sex and parthenogenesis for worker and queen production in ants. Science 306:1780–1783
Pearcy M, Hardy O, Aron S (2006) Thelytokous parthenogenesis and its consequences on inbreeding in an ant. Heredity 96:377–382
Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat 132:217–236
Raymond M, Rousset F (1995) Genpop (version 1.2): Population genetics software for exact tests and ecumenism. J Hered 86:248–249
Schneider SS, Painter-Kurt S, de Grandi-Hoffman G (2001a) The role of the vibration signal during queen competition in colonies of the honeybee, Apis mellifera. Anim Behav 61:1173–1180
Schneider SS, Painter-Kurt S, DeGrandi-Hoffman G (2001b) The role of the vibration signal during queen competition in colonies of the honeybee, Apis mellifera. Anim Behav 61:1173–1180
Solignac M, Vautrin D, Loiseau A, Mougel F, Baudry E, Estoup A, Garnery L, Haberl M, Cornuet J-M (2003) Five hundred and fifty microsatellite markers for the study of the honeybee (Apis mellifera L.) genome. Mol Ecol Notes 3:307–311
Solignac M, Vautrin D, Baudry E, Mougel F, Loiseau A, Cornuet J-M (2004) A microsatellite-based linkage map of the honeybee, Apis mellifera L. Genetics 167:253–262
Sumner S, Keller L (2008) Social evolution: reincarnation, free-riding and inexplicable modes of reproduction. Curr Biol 18:R206–R207
Tarpy DR, Hatch S, Fletcher DJC (2000) The influence of queen age and quality during queen replacement in honeybee colonies. Anim Behav 59:97–101
Tilley CA, Oldroyd BP (1997) Unequal representation of subfamilies among queen and worker brood of queenless honey bee (Apis mellifera) colonies. Anim Behav 54:1483–1490
Verma LR, Ruttner F (1983) Cytological analysis of the thelytokous parthenogenesis in the Cape honeybee (Apis mellifera capensis Escholtz). Apidologie 14:47–57
Walsh PS, Metzger DA, Higuchi R (1991) Chelex (R)100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:507
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population of population structure. Evolution 38:1358–1370
Wenseleers T, Ratnieks FLW, Billen J (2003) Caste fate conflict in social Hymenoptera: an inclusive fitness analysis. J Evol Biol 10:647–658
Wenseleers T, Hart AG, Ratnieks FLW, Quezada-Euan JJG (2004) Queen execution and caste conflict in the stingless bee Melipona beecheii. Ethology 110:725–736
Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge
Wright S (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19:395–420
Acknowledgements
This work was funded by grants from the Australian Research Council to BPO and MB. We thank Christian Fransman for his outstanding assistance in the field.
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Allsopp, M.H., Beekman, M., Gloag, R.S. et al. Maternity of replacement queens in the thelytokous Cape honey bee Apis mellifera capensis . Behav Ecol Sociobiol 64, 567–574 (2010). https://doi.org/10.1007/s00265-009-0872-9
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DOI: https://doi.org/10.1007/s00265-009-0872-9