The Science of Nature

, 105:22 | Cite as

The transcriptomic changes associated with the development of social parasitism in the honeybee Apis mellifera capensis

  • Denise Aumer
  • Fiona N. Mumoki
  • Christian W. W. Pirk
  • Robin F. A. Moritz
Original Paper


Social insects are characterized by the division of labor. Queens usually dominate reproduction, whereas workers fulfill non-reproductive age-dependent tasks to maintain the colony. Although workers are typically sterile, they can activate their ovaries to produce their own offspring. In the extreme, worker reproduction can turn into social parasitism as in Apis mellifera capensis. These intraspecific parasites occupy a host colony, kill the resident queen, and take over the reproductive monopoly. Because they exhibit a queenlike behavior and are also treated like queens by the fellow workers, they are so-called pseudoqueens. Here, we compare the development of parasitic pseudoqueens and social workers at different time points using fat body transcriptome data. Two complementary analysis methods—a principal component analysis and a time course analysis—led to the identification of a core set of genes involved in the transition from a social worker into a highly fecund parasitic pseudoqueen. Comparing our results on pseudoqueens with gene expression data of honeybee queens revealed many similarities. In addition, there was a set of specific transcriptomic changes in the parasitic pseudoqueens that differed from both, queens and social workers, which may be typical for the development of the social parasitism in A. m. capensis.


Worker reproduction Reproductive dominance Social parasitism Apis mellifera capensis Thelytoky Pseudoqueen 



We are grateful to the members of the Research Unit FOR2281 “Sociality and the reversal of the fecundity-longevity trade-off,” especially to Daniel Elsner and Mark Harrison, for their valuable input regarding the data analysis. We also thank Nikita Venter, Cathy Bester, and Alex Nepomuceno for their assistance in handling the experimental bees.

Funding information

Financial support was granted by the Deutsche Forschungsgemeinschaft (RFAM).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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  1. Alexa A, Rahnenfuhrer J, Lengauer T (2006) Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 2:1600–1607CrossRefGoogle Scholar
  2. Allsopp MH (1992) The Capensis Calamity. South African Bee J 64:52–54Google Scholar
  3. Allsopp MH, Crewe R (1993) The Cape honeybee as a Trojan horse rather than the hordes of Jenghiz Khan. Am Bee J 133:121–123Google Scholar
  4. Amdam GV, Fennern E, Havukainen H (2012) Vitellogenin in honey bee behavior and lifespan. In: Galizia C, Eisenhardt D, Giurfa M (eds) Honeybee neurobiology and behavior. Springer, DordrechtGoogle Scholar
  5. Amdam GV, Norberg K, Fondrik MK, Page RE (2004) Reproductive ground plan may mediate colony-level selection effects on individual foraging behaviour in honey bees. PNAS 101:11350–11355CrossRefPubMedPubMedCentralGoogle Scholar
  6. Amdam GV, Norberg KA, Hagen A, Omholt SW (2003) Social exploitation of vitellogenin. Proc Natl Acad Sci U S A 100:1799–1802CrossRefPubMedPubMedCentralGoogle Scholar
  7. Anders S, Pyl PT, Huber W (2015) HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31:166–169CrossRefPubMedGoogle Scholar
  8. Anderson RH (1963) The laying worker in the Cape honeybee, Apis mellifera capensis. J Apic Res 2:85–92CrossRefGoogle Scholar
  9. Anderson RH (1968) The effect of queen loss on colonies of Apis mellifera capensis. S Afri J Agri Sci 11:383–388Google Scholar
  10. Aufauvre J, Misme-Acouturier B, Viguès B, Texier C, Delbac F, Blot N (2014) Transcriptome analyses of the honeybee response to Nosema ceranae and insecticides. PLoS One 9:e91686CrossRefPubMedPubMedCentralGoogle Scholar
  11. Aumer D, Allsopp MH, Lattorf MHG, Moritz RFA, Jarosch-Perlow A (2017) Thelytoky in Cape honeybees (Apis mellifera capensis) is controlled by a single recessive locus. Apidologie 48:401–410CrossRefGoogle Scholar
  12. Barchuk AR, Cristino AS, Kucharski R, Costa LF, Simoes ZLP, Maleszka R (2007) Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. BMC Dev Biol 7:70CrossRefPubMedPubMedCentralGoogle Scholar
  13. 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 167:243–252CrossRefPubMedPubMedCentralGoogle Scholar
  14. Beekman M, Calis JNM, Boot WJ (2000) Parasitic honeybees get royal treatment. Nature 404:723CrossRefPubMedGoogle Scholar
  15. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics: btu170Google Scholar
  16. Bonasio R, Shiekhattar R (2014) Regulation of transcription by long noncoding RNAs. Annu Rev Genet 48:433–455CrossRefPubMedPubMedCentralGoogle Scholar
  17. Butler CG (1959) The source of substance produced by a queen honeybee which inhibits development of the ovaries of the workers of her colony. Proc Roy Ent Soc A 34:137–138Google Scholar
  18. Calis JNM, Allsopp MH, Boot WJ (2005) Establishment of Cape honey bees as social parasites in African honeybee colonies. Proc Neth Entomol Soc Meet 16:81–90Google Scholar
  19. Cardoen D, Wenseleers T, Ernst UR, Danneels EL, Laget D, de Graaf DC, Schoofs L, Verleyen P (2011) Genome-wide analysis of alternative reproductive phenotypes in honeybee workers. Mol Ecol 20:4070–4084CrossRefPubMedGoogle Scholar
  20. Carreck NL, Andree M, Brent CS, Cox-Foster D, Dade HA, Ellis JD, Hatjina F, van Englesdorp D (2013) Standard methods for Apis mellifera anatomy and dissection. J Api Res 52:1–40CrossRefGoogle Scholar
  21. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidnium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159CrossRefPubMedGoogle Scholar
  22. Cini A, Patalano S, Segonds-Pichon A, Busby GB, Cervo R, Sumner S (2015) Social parasitism and the molecular basis of phenotypic evolution. Front Genet 6:32CrossRefPubMedPubMedCentralGoogle Scholar
  23. Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y, Hughes KA, Robinson GE (2007) Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc Natl Acad Sci U S A 104:7128–7133CrossRefPubMedPubMedCentralGoogle Scholar
  24. Crewe RM (1984) Differences in behaviour and morphology between capensis and adansonii. S Afr Bee J 5:16–21Google Scholar
  25. Crewe RM, Velthuis HHW (1980) False queens: a consequence of mandibular gland signals in worker honeybees. Naturwissenschaften 67:467–469CrossRefGoogle Scholar
  26. Danihlik J, Aronstein K, Petrivalsky M (2015) Antimicrobial peptides: a key component of honey bee innate immunity. J Apic Res 54:123–136CrossRefGoogle Scholar
  27. Doublet V, Paxton RJ, McDonnel CM, Dubois E, Nidelet S, Moritz RFA, Alaux C, Le Conte Y (2016) Brain transcriptomes of honey bees (Apis mellifera) experimentally infected by two pathogens: black queen cell virus and Nosema ceranae. Genomics Data 10:79–82CrossRefPubMedPubMedCentralGoogle Scholar
  28. Dunn OJ (1964) Multiple comparison using RANK sums. Technometrics 6:241–252CrossRefGoogle Scholar
  29. Dzierzon J (1845) Chodowanie pszczół - Sztuka zrobienica złota, nawet z zielska, in: Tygodnik Polski Poświęcony Włościanom (pl), Issue 20, Pszczyna (Pless)Google Scholar
  30. Elsik CG, Worley KC, Bennett AK, Beye M, Camara F, Childers CP, de Graaf DC, Debyser G, Deng J, Devreese B, Elhaik E, Evans JD, Foster LJ, Graur D, Guigo R, HGSC production teams, Hoff K, Holder ME, Hudson ME, Hunt GJ, Jiang H, Joshi V, Khetani RS, Kosarev P, Kovar CL, Ma J, Maleszka R, Moritz RFA, Munoz-Torres MC, Murphy TD, Muzny DM, Newsham IF, Reese JT, Robertson HM, Robinson GE, Rueppell O, Solovyev V, Stanke M, Stolle E, Tsuruda JM, Vaerenbergh M, Waterhouse RM, Weaver DB, Whitfield CW, Wu Y, Zdobnov EM, Zhang L, Zhu D, Gibbs RA, on behalf of Honey Bee Genome Sequencing Consortium (2014) Finding the missing honey bee genes: lessons learned from a genome upgrade. BMC Genomics 15:86CrossRefPubMedPubMedCentralGoogle Scholar
  31. Emery C (1909) Über den Ursprung der dulotischen, parasitischen und myrmekophilen Ameisen. Biol Zentralbl 29:352–362Google Scholar
  32. Engels W (1974) Occurrence and significance of vitellogenins in female castes of social Hymenoptera. Am Zool 14:1229–1237CrossRefGoogle Scholar
  33. Engels W, Fahrenhorst H (1974) Alters- und kastenspezifische Veränderungen der Haemolymph-Protein-Spektren bei Apis mellificia. Roux’s Arch 174:285–296CrossRefGoogle Scholar
  34. Fleig R (1995) Role of the follicle cells for yolk uptake in ovarian follicles of the honey-bee Apis-mellifera L (Hymenoptera, Apidae). Int J Insect Morphol Embryol 24:427–433CrossRefGoogle Scholar
  35. Fraley C, Raftery AE, Murphy TB, Scrucca L (2012) mclust Version 4 for R: normal mixture modeling for model-based clustering, classification, and density estimation. Technical Report No. 597, Department of Statistics, University of WashingtonGoogle Scholar
  36. Forêt S, Maleszka R (2006) Function and evolution of a gene family encoding odorant binding-like proteins in a social insect, the honey bee (Apis mellifera). Genome Res 16:1404–1413Google Scholar
  37. Forêt S, Wanner KW, Maleszka R (2007) Chemosensory proteins in the honey bee: Insights from the annotated genome, comparative analyses and expressional profiling. Insect Bochem and Molec Biol 37:19–28 Google Scholar
  38. Grozinger CM, Fan Y, Hoover SER, Winston ML (2007) Genome-wide analysis reveals differences in brain gene expression patterns associated with caste and reproductive status in honey bees (Apis mellifera). Mol Ecol 16:4837–4848CrossRefPubMedGoogle Scholar
  39. Haunerland NH, Shirk PD (1995) Regional and functional differentiation in the insect fat body. Annu Rev Entomol 40:121–145CrossRefGoogle Scholar
  40. 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(2):183–193Google Scholar
  41. Härtel S, Wossler T, Moltzer G-J, Crewe R, Moritz RFA, Neumann P (2011) Pheromone-mediated reproductive dominance hierarchies among pseudo-clonal honeybee workers (Apis mellifera capensis). Apidologie 42:659–668CrossRefGoogle Scholar
  42. Hemmling C, Koeniger N, Ruttner F (1979) Quantitative Bestimmung der 9-Oxodecensäure im Lebenszyklus der Kapbiene (Apis mellifera capensis Escholtz). Apidologie 10:227–240CrossRefGoogle Scholar
  43. Hepburn HR, Crewe RM (1991) Portrait of the Cape honeybee, Apis mellifera capensis. Apidologie 22:567–580CrossRefGoogle Scholar
  44. Hepburn HR, Magnuson P, Herbert L, Whiffler LA (1991) The development of laying workers in field colonies of the Cape honey bee. J Api Res 30:107–112CrossRefGoogle Scholar
  45. Hess G (1942) Ueber den Einfluss der Weisellosigkeit und des Fruchtbarkeitsvitamins E auf die Ovarien der Bienenarbeiterin (Ein Beitrag zur Frage der Regulationen im Bienenstaat). Beih Schweiz Bienen Ztg 2:33–111Google Scholar
  46. Hillesheim E, Koeniger N, Moritz RFA (1989) Colony performance in honeybees (Apis mellifera capensis Esch.) depends on the proportion of subordinate and dominant workers. Behav Ecol Socioboil 24:291–296CrossRefGoogle Scholar
  47. Hoover SER, Keeling CI, Winston ML, Slessor KN (2003) The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 90:477–480CrossRefPubMedGoogle Scholar
  48. Huarte M (2013) LncRNAs have a say in protein translation. Cell Res 23:449–451CrossRefPubMedGoogle Scholar
  49. Humann FC, Hartfelder K (2011) Representational difference analysis (RDA) reveals differential expression of conserved as well as novel genes during castespecific development of the honey bee (Apis mellifera L.) ovary. Insect Biochem Mol Biol 41:602–612CrossRefPubMedGoogle Scholar
  50. Humann FC, Tiberio GJ, Hartfelder K (2013) Sequence and expression characteristics of long noncoding RNAs in honey bee caste development—potential novel regulators for transgressive ovary size. PLoS One 8:e78915CrossRefPubMedPubMedCentralGoogle Scholar
  51. Jayakodi M, Jung JW, Park D, Ahn Y-J, Lee S-C, Shin S-Y, Shin C, Yang T-J, Kwon H-W (2015) Genome-wide characterization long intergenic non-coding RNAs (lincRNAs) provides new insight into viral diseases in honey bees Apis cerana and Apis mellifera. BMC Genomics 16:680–692CrossRefPubMedPubMedCentralGoogle Scholar
  52. Johannsmeier MF (1983) Experiences with the Cape bee in the Transvaal. S Afr Bee J 55:130–138Google Scholar
  53. Johannsmeier MF (1992) The Cape bee: a problem in the Transvaal. Plant Protection Research Institute. Pretoria, LeafletGoogle Scholar
  54. Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong S-Y, Lopez R, Hunter S (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240CrossRefPubMedPubMedCentralGoogle Scholar
  55. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36CrossRefPubMedPubMedCentralGoogle Scholar
  56. Koeniger G, Würkner W (1992) Die Kap Honigbiene (Apis mellifera capensis) Natürliche Verbreitung und die Schwierigkeit der Haltung unter unseren klimatischen Bedingungen. Die Biene 128:583–588Google Scholar
  57. Köhler A, Nicolson SW, Pirk CWW (2013) A new design for honey bee hoarding cages for laboratory experiments. J Api Res 52:12–14CrossRefGoogle Scholar
  58. Koywiwattrakul P, Sittipraneed S (2009) Expression of vitellogenin and transferrin in activated ovaries of worker honey bees, Apis mellifera. Biochem Genet 4:19–26CrossRefGoogle Scholar
  59. Kucharski R, Maleszka R (2003) Transcriptional profiling reveals multifunctional roles for transferrin in the honeybee Apis mellifera. J Insect Sci 3:27–34Google Scholar
  60. Langmead B, Salzberg SL (2012) Fast gapped read-alignment with Bowtie 2. Nat Meth 9:357–359Google Scholar
  61. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25CrossRefPubMedPubMedCentralGoogle Scholar
  62. Lattorff HMG, Moritz RFA, Crewe RM, Solignac M (2007) Control of reproductive dominance by the thelytoky gene in honeybees. Biol Lett 3:292–295CrossRefPubMedPubMedCentralGoogle Scholar
  63. Lattorff HMG, Moritz RFA, Fuchs S (2005) A single locus determines thelytokous parthenogenesis of laying honeybee workers (Apis mellifera capensis). Heredity 94:533–537CrossRefPubMedGoogle Scholar
  64. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, and 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25:2078–2079Google Scholar
  65. Li R, Zhang L, Fang Y, Han B, Lu X, Zhou T, Feng M, Li J (2013) Proteome and phosphoproteome analysis of honeybee (Apis mellifera) venom collected from electrical stimulation and manual extraction of the venom gland. BMC Genomics 14:766–778Google Scholar
  66. Li X, Schuler MA, Berenbaum MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52:231–253Google Scholar
  67. Lin H, Winston ML, Haunerland NH, Slessor KN (1999) Influence of age and population size on ovarian development and of trophallaxis on ovarian development and vitellogenin titres of queenless worker honeybee (Hymenoptera: Apidae). Can Entomol 131:695–706CrossRefGoogle Scholar
  68. Long Y, Wang X, Youmans DT, Chech TR (2017) How do lncRNAs regulate transcription? Sci Adv 3:eaao2110CrossRefPubMedPubMedCentralGoogle Scholar
  69. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550CrossRefPubMedPubMedCentralGoogle Scholar
  70. Lyko F, Foret S, Kucharski R, Wolf S, Falckenhayn C, Maleszka R (2010) The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol 8:e1000506CrossRefPubMedPubMedCentralGoogle Scholar
  71. Martin SJ, Beekman M, Wossler TC, Ratnieks FLW (2002a) Parasitic Cape honeybee workers, Apis mellifera capensis, evade policing. Nature 415:163–165CrossRefPubMedGoogle Scholar
  72. Martin S, Wossler T, Kryper P (2002b) Usurpation of African Apis mellifera scutellata colonies by parasitic Apis mellifera capensis workers. Apidologie 33:215–232CrossRefGoogle Scholar
  73. Moritz RFA, Crewe RM, Hepburn HR (2002) Queen avoidance and mandibular gland secretion of honeybee workers (Apis mellifera L.) Insect Soc 49:86–91CrossRefGoogle Scholar
  74. Moritz RFA, Hillesheim E (1985) Inheritance of dominance in honeybees (Apis mellifera capensis). Behav Ecol Sociobiol 17:87–89CrossRefGoogle Scholar
  75. Moritz RFA, Kryger P, Allsopp MH (1996) Competition for royalty in bees. Nature 384:31CrossRefGoogle Scholar
  76. Moritz RFA, Kryger P, Allsopp MH (1999) Lack of worker policing in the Cape honeybee (Apis mellifera capensis). Behaviour 136:1079–1092CrossRefGoogle Scholar
  77. Moritz RFA, Lattorff HMG, Crewe RM (2004) Honeybee workers (Apis mellifera capensis) compete for producing queen-like pheromone signals. Proc Roy Soc Lond B 271:98–100CrossRefGoogle Scholar
  78. Moritz RF, Pflugfelder J, Crewe RM (2003) Lethal fighting between honeybee queens and parasitic workers (Apis mellifera). Naturwissenschaften 9:378–381Google Scholar
  79. Moritz RFA, Simon UE, Crewe RM (2000) Pheromonal contest between honeybee workers (Apis mellifera capensis). Naturwissenschaften 87:395–397CrossRefPubMedGoogle Scholar
  80. Neumann P, Hepburn R (2002) Behavioural basis for social parasitism of Cape honeybees (Apis mellifera capensis). Apidologie 33:165–192CrossRefGoogle Scholar
  81. Neumann P, Moritz RFA (2002) The Cape honeybee phenomenon: the sympatric evolution of a social parasite in real time? Behav Ecol Sociobiol 52:271–281CrossRefGoogle Scholar
  82. Niu D, Zheng H, Corona M, Lu Y, Chen X, Cao L, Sohr A, Hu F (2014) Transcriptome comparison between inactivated and activated ovaries of the honey bee Apis mellifera L. Insect Mol Biol 23:668–681CrossRefPubMedGoogle Scholar
  83. Nueda MJ, Tarazona S, Conesa A (2014) Next maSigPro: updating maSigPro bioconductor package for RNA-seq time series. Bioinformatics 30:2598–2602CrossRefPubMedPubMedCentralGoogle Scholar
  84. Okosun OO, Yusuf AA, Crewe RM, Pirk CW (2015) Effects of age and reproductive status on tergal gland secretions in queenless honey bee workers, Apis mellifera scutellata and A. m. capensis. J Chem Ecol 41:896–903CrossRefPubMedGoogle Scholar
  85. Onions GW (1912) South African “fertile-worker bees”. S Afr Agric J 1:720–728Google Scholar
  86. Onions GW (1914) South African “fertile worker bees”. Union S Afr Agric J 7:44–46Google Scholar
  87. Pflugfelder J, Koeniger N (2003) Fight between virgin queens (Apis mellifera) is initiated by contact to the dorsal abdominal surface. Apidologie 34:249–256CrossRefGoogle Scholar
  88. Phiancharoen M, Pirk CWW, Radloff SE, Hepburn R (2010) Clinal nature of the frequencies of ovarioles and spermathecae in Cape worker honeybees, Apis mellifera capensis. Apidologie 41:129–134CrossRefGoogle Scholar
  89. Pelosi P, Calvello M, Ban L (2005) Diversity of odorant-binding proteins and chemosensory proteins in insects. Chem Senses 30(1):i291–292Google Scholar
  90. Pinto LZ, Bitondi MMG, Simões ZLP (2000) Inhibition of vitellogenin synthesis in Apis mellifera workers by juvenile hormone analogue, pyriproxyfen. J Insect Physiol 46:153–160CrossRefPubMedGoogle Scholar
  91. Pirk CWW, Human H, Crewe RM, vanEngelsdorp D (2014) A survey of managed honey bee colony losses in the Repulic of South Africa—2009 to 2011. J Api Res 53:35–42CrossRefGoogle Scholar
  92. 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 33:203–211CrossRefGoogle Scholar
  93. Plettner E, Slessor K, Winston M, Robinson G, Page R (1993) Mandibular gland components and ovarian development as measures of caste differentiation in the honey bee (Apis mellifera L.) J Insect Physiol 39:235–240CrossRefGoogle Scholar
  94. Remolina SC, Hughes KA (2008) Evolution and mechanisms of long life and high fertility in queen honey bees. Age 30:177–185CrossRefPubMedPubMedCentralGoogle Scholar
  95. Ruttner F. (1988) Biogeography and taxonomy of honeybees, Springer-Verlag, BerlinGoogle Scholar
  96. Ruttner F, Hesse B (1981) Rassenspezifische Unterschiede in Ovarentwicklung und Eiablage von weisellosen Arbeiterinnen der Honigbiene Apis mellifera l. Apidologie 12:159–183CrossRefGoogle Scholar
  97. Sakagami SF (1958) The false queen: fourth adjustive response in dequeened colonies. Behaviour 8:280–296CrossRefGoogle Scholar
  98. Satyavathi V, Ghosh R, Subramanian S (2017) Long Non-Coding RNAs Regulating Immunity in Insects. Non-Coding RNA 3:14Google Scholar
  99. Sawata M, Yoshino D, Takeuchi H, Kamikouchi A, Ohashi K, Kubo T (2002) Identification and punctate nuclear localization of a novel noncoding RNA, Ks-1, from the honeybee brain. RNA 8:772–785CrossRefPubMedPubMedCentralGoogle Scholar
  100. Seehuus S-C, Norberg K, Krekling T, Fondrk K, Amdam GV (2007) Immunogold localization of vittellogenin in the ovaries, hypopharyngeal glands and head fat bodies of honeybee workers, Apis Mellifera. J Insect Sci 7:52CrossRefPubMedCentralGoogle Scholar
  101. Simon U, Moritz RFA, Crewe RM (2001) The ontogenetic pattern of mandibular gland components in queenless worker bees (Apis mellifera capensis Esch.) J Insect Physio 47:735–738CrossRefGoogle Scholar
  102. Slessor KN, Kaminski L-A, King GGS, Borden JH, Winston ML (1988) Semiochemical basis of the retinue response to queen honey bees. Nature 332:354–356CrossRefGoogle Scholar
  103. Smith CR, Helms Cahan S, Kemena C, Brady SG, Yang W, Bornberg-Bauer E, Eriksson T, Gadau J, Helmkampf M, Gotzek D, Okamoto Miyakawa M, Suarez AV, Mikheyev A (2015) How do genomes create novel phenotypes? Insights from the loss of the worker caste in ant social parasites. Mol Biol Evol 32:2919–2931CrossRefPubMedPubMedCentralGoogle Scholar
  104. Tadano H, Yamazaki Y, Takeuchi H, Kubo T (2009) Age- and division-of-labour-dependent differential expression of a novel non-coding RNA, Nb-1, in the brain of worker honeybees, Apis mellifera L. Insect Mol Biol 18:715–726CrossRefPubMedGoogle Scholar
  105. Tribe GD (1983) What is the Cape bee? S Afr Bee J 55:77–87Google Scholar
  106. Velthuis HHW (1976) Egg laying, aggression and dominance in bees. Proc 15th Int Congr Entomol, Washington: 436–449Google Scholar
  107. Velthuis HHW, Ruttner F, Crewe RM (1990) Differentiation in reproductive physiology and behaviour during the development of laying worker honeybees. In: Engels W (Ed.) Social insects. Springer Verlag, Berlin Heidelberg, New York: 231–243Google Scholar
  108. Wanner KW, Nicols AS, Walden KKO, Brockmann A, Luetje CW, Robertson HM (2007) A honey bee odorant receptor for the queen substance 9-oxo-2-decenoic acid. PNAS 104:14383–14388CrossRefPubMedPubMedCentralGoogle Scholar
  109. Wegener J, Huang ZY, Lorenz MW, Bienefeld K (2009) Regulation of hypopharyngeal gland activity and oogenesis in honey bee (Apis mellifera) worker. J Insec Physiol 55:716–725CrossRefGoogle Scholar
  110. Weiner SA, Toth, AL (2012) Epigenetics in social insects: a new direction for understanding the evolution of castes. Genet Res Int: Article ID 609810Google Scholar
  111. West-Eberhard MJ (1996) Wasp societies as microcosms for the study of development and evolution. In: Turillazzi S, West-Eberhard MJ (eds) Natural history and evolution of paper-wasps. Oxford University Press, Oxford, pp 90–317Google Scholar
  112. Wilson EO (1971) The insect societies. Harvard Bellknap, CambridgeGoogle Scholar
  113. Winston ML (1987) The biology of the honey bee. Cambridge, Massachusetts: Harvard University Press, LondonGoogle Scholar
  114. Winston ML, Slessor KN (1998) Honey bee primer pheromones and colony organization: gaps in our knowledge. Apidologie 29:81–95CrossRefGoogle Scholar
  115. Whitfield CW, Cziko AM, Robinson GE (2003) Gene expression profiles in the brain predict behaviour in individual honey bees. Science 302:296–299CrossRefPubMedGoogle Scholar
  116. Woyke J (1995) Invasion of capensis bee. In: Magnuson P (Ed.) Proceedings of the First International Electronic Conference on the Cape Bee Problem in South Africa, 5–30 June 1995, PPRI, Pretoria: 35Google Scholar
  117. Wu X-B, Wang Z-L, Li S-Y, Zeng Z-J (2016) Transcriptome comparison between newly emerged and sexualy matured bees of Apis mellifera. J Asia Pac Entomol 19:893–897CrossRefGoogle Scholar
  118. Wu Y, Zheng H, Corona M, Pirk C, Meng F, Zheng Y, Hu F (2017) Comparative transcriptome analysis on the synthesis pathway of honey bee (Apis mellifera) mandibular gland secretions. Sci Rep 7:4530CrossRefPubMedPubMedCentralGoogle Scholar
  119. Yoon J-H, Abdelmohsen K, Gorospe M (2013) Post-transcriptional gene regulation by long noncoding RNA. J Mol Biol 425:3723–3730CrossRefPubMedGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Molecular EcologyMartin-Luther University Halle-WittenbergHalle (Saale)Germany
  2. 2.Social Insect Research Group, Department of Zoology and EntomologyUniversity of PretoriaPretoriaSouth Africa
  3. 3.German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-LeipzigLeipzigGermany

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