The frequency of arrhenotoky in the normally thelytokous Apis mellifera capensis worker and the Clone reproductive parasite
Tóm tắt
In most honey bees, unfertilized eggs develop into haploid males via arrhenotokous parthenogenesis. The Cape honey bee (Apis mellifera capensis) is different. Although mated queens always produce females sexually, if workers lay unfertilized eggs the eggs develop into diploid females via thelytokous parthenogenesis. Thelytoky in A. m. capensis has given rise to an entirely clonal lineage of reproductive parasites that infests colonies of their neighbouring subspecies A. m. scutellata. The switch from arrhenotoky to thelytokous worker reproduction is thought to be determined by a recessive allele at a single locus. However, it has recently been shown that this simple phenotype/genotype association may be more complex because individuals from the parasitic clonal lineage produce c.a. 15 % of eggs arrhenotokously and 85 % of eggs thelytokously. Here, we investigate the fate of these arrhenotokous eggs and show that they can develop into adult males. We further show that workers of the sexual A. m. capensis population produce far fewer arrhenotokous eggs. We discuss possible evolutionary explanations for this difference.
Tài liệu tham khảo
Allsopp MH (1992) The Capensis calamity. S African Bee J 64:52–55
Allsopp MH, Crewe RM (1993) The Cape honeybee as a Trojan horse rather than the hordes of Jenghiz Khan. Am Bee J 133:121–123
Allsopp MH, Calis JNM, Boot WJ (2003) Differential feeding of worker larvae affects caste characters in the Cape honeybee, Apis mellifera capensis. Behav Ecol Sociobiol 54:555–561
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
Anderson RH (1980) Cape honey-bee sanctuaries. S Afr Bee J 52:5–9
Baudry E, Kryger P, Allsopp M, Koeniger N, Vautrin D, Mougel F, Cornuet JM, Solignac M (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
Beekman M, Oldroyd BP (2008) When workers disunite: intraspecific parasitism in eusocial bees. Ann Rev Entomol 53:19–37
Beekman M, Calis JNM, Boot WJ (2000) Parasitic honeybees get royal treatment. Nature 404:723
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
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
Calis JNM, Boot WJ, Allsopp MH, 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 33:193–202
Chapman NC, Beekman M, Allsopp MH, Rinderer TE, Lim J, Oxley PR, Oldroyd BP (2015) Inheritance of thelytoky in the honey bee Apis mellifera capensis. Heredity. doi:10.1038/hdy.2014.127
Crewe RM, Allsopp MH (1994) Sex and the single queen: recent experiments with capensis and scutellata queens. S Afr Bee J 66:58–62
Dietemann V, Lubbe A, Crewe RM (2006) Human factors facilitating the spread of a parasitic honey bee in South Africa. J Econ Entomol 99:7–13
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
Engelstädter J (2008) Constraints on the evolution of asexual reproduction. Bioessays 30:1138–1150
Engelstädter J, Sandrock C, Vorburger C (2010) Contageous parthenogenesis, automixis, and a sex determination meltdown. Evolution 65:501–511
Estoup A, Largiader CR, Perrot E, Chourrout D (1996) Rapid one-tube DNA extraction for reliable PCR detection of fish polymorphic markers and transgenes. Mol Mar Biol Biotech 5:295–298
Goudie F, Oldroyd BP (2014) Thelytoky in the honey bee. Apidologie 45:306–326
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
Goudie F, Allsopp MH, Oldroyd BP (2013) Selection on overdominant genes maintains heterozygosity along multiple chromosomes in a clonal lineage of honey bee. Evolution 68:125–136
Greeff JM (1996) Effects of thelytokous worker reproduction on kin-selection and conflict in the Cape honeybee, Apis mellifera capensis. Phil Trans Roy Soc London Ser B Biol Sci 351:617–625
Greeff JM, Villet MH (1993) Deducing the coefficient of relationship by the amount of recombination produced during automictic parthneogenesis. Heredity 70:499–502
Hasselmann M, Beye M (2004) Signatures of selection among sex-determining alleles of the honey bee. Proc Nat Acad Sci USA 101:4888–4893
Hepburn HR, Crewe RM (1991) Portrait of the Cape honeybee, Apis mellifera capensis. Apidologie 22:567–580
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
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
Jarosch A, Stolle E, Crewe RM, Moritz RFA (2011) Alternative splicing of a single transcription factor drives selfish reproductive behavior in honeybee workers (Apis mellifera). Proc Nat Acad Sci USA 108:15282–15287
Jordan LA, Allsopp MH, Oldroyd BP, Wossler TC, Beekman M (2008) Cheating honeybee workers produce royal offspring. Proc Roy Soc B Biol Sci 275:345–351
Kryger P (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, Berlin
Lattorff HMG, Moritz RFA, Crewe RM, Solignac M (2007) Control of reproductive dominance by the thelytoky gene in honeybees. Biol Lett 3:292–295
Levin BR (1996) The evolution and maintenance of virulence in microparasites. Emerg Infect Dis J 2:93–102
Mackensen O (1943) The occurence of parthenogenetic females in some strains of honey-bees. J Econ Entomol 36:465–467
Martin S, Wossler TC, Kryger P (2002) Usurpation of African Apis mellifera scutellata colonies by parasitic Apis mellifera capensis workers. Apidologie 33:215–232
Moritz RFA (2002) Population dynamics of the Cape bee phenomenon: the impact of parasitic laying worker clones in apiaries and natural populations. Apidologie 33:233–244
Moritz RFA, Kryger P, Allsopp MH (1999) Lack of worker policing in the Cape honeybee (Apis mellifera capensis). Behaviour 136:1079–1092
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
Moritz RFA, Lattorff HMG, Crous KL, Hepburn HR (2011) Social parasitism of queens and workers in the Cape honeybee (Apis mellifera capensis). Behav Ecol Sociobiol 65:735–740
Neumann P, Hepburn HR (2002) Behavioural basis for social parasitism of Cape honeybees (Apis mellifera capensis). Apidologie 33:165–192
Neumann P, Moritz RFA (2002) The Cape honeybee phenomenon: the sympatric evolution of a social parasite in real time? Behav Ecol Sociobiol 52:271–281
Normark BB (2003) The evolution of alternative genetic systems in insects. Ann Rev Entomol 48:397–423
Oldroyd BP (2002) The Cape honeybee: an example of a social cancer. Trends Ecol Evol 17:249–251
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
Oldroyd BP, Allsopp MH, Lim J, Beekman M (2011a) A thelytokous lineage of socially parasitic honey bees has retained heterozygosity despite at least 10 years of inbreeding. Evolution 65:860–868
Oldroyd BP, Allsopp MH, Lim J, Beekman M (2011b) A thelytokous lineage of socially parasitic honey bees has retained heterozygosity despite at least 10 years of inbreeding. Evolution 65:860–868
Onions GW (1912) South African ‘fertile worker bees’. Agricult J Union S Africa 1:720–728
Pearcy M, Hardy O, Aron S (2006) Thelytokous parthenogenesis and its consequences on inbreeding in an ant. Heredity 96:377–382
Rabeling C, Kronauer DJC, Berenbaum MR (2013) Thelytokous parthenogenesis in eusocial Hymenoptera. Ann Rev Entomol 58:273–292
Remnant EJ, Koetz A, Tan K, Hinson E, Beekman M, Oldroyd BP (2014) Reproductive interference between honey bee species in Australia and China. Mol Ecol 23:1096–1107
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
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:R66
Vavre F, deJong JH, Stouthamer R (2004) Cytogenetic mechanism and genetic consequences of thelytoky in the wasp Trichogramma cacoeciae. Heredity 93:592–596
Verma S, Ruttner F (1983) Cytological analysis of the thelytokous parthenogenesis in the Cape honeybee (Apis mellifera capensis Escholtz). Apidologie 14:41–57
Walsh PS, Metzger DA, Higuchi R (1991) Chelex 1000 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513
Winston ML (1991) The biology of the honey bee. Harvard University Press, Cambridge
Winston ML (1992) Killer bess: the Africanized honey bee in the Americas. Harvard University Press, Cambridge
Wirtz P, Beetsma J (1972) Induction of caste differentiation in the honey bee (Apis mellifera) by juvenile hormone. Entomol Exp Appl 15:517–520