Genome-wide analysis of alternative reproductive phenotypes in honeybee workers

Molecular Ecology

Volumn 20, Issue 19, 2011, Pages 4070-4084

  Cardoen, Dries ^a   Wenseleers, Tom ^a   Ernst, Ulrich R ^a   Danneels, Ellen L ^b   Laget, Dries ^b   De Graaf, Dirk C ^b   Schoofs, Liliane ^a   Verleyen, Peter ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

Altruism; Apis mellifera; microarray; reproductive division of labour

Indexed keywords

ANIMAL; ARTICLE; BEE; ENVIRONMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOME; PHENOTYPE; PHYSIOLOGY; QUANTITATIVE TRAIT LOCUS; REPRODUCTION; SEXUAL BEHAVIOR; SIGNAL TRANSDUCTION; SOCIAL DOMINANCE;

ANIMALS; BEES; ENVIRONMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOME, INSECT; HIERARCHY, SOCIAL; PHENOTYPE; QUANTITATIVE TRAIT LOCI; REPRODUCTION; SEXUAL BEHAVIOR, ANIMAL; SIGNAL TRANSDUCTION;

APIS MELLIFERA; HEXAPODA;

EID: 80053290846     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2011.05254.x     Document Type: Article

References (87)

1. Alaux C, Le Conte Y, Adams HA, et al. (2009a) Regulation of brain gene expression in honey bees by brood pheromone. Genes, Brain and Behavior, 8, 309-319.
2. Alaux C, Sinha S, Hasadsri L, et al. (2009b) Honey bee aggression supports a link between gene regulation and behavioral evolution. Proceedings of the National Academy of Sciences, USA, 106, 15400-15405.
3. Alexa A, Rahnenfuhrer J, Lengauer T, (2006) Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics, 22, 1600-1607. (Pubitemid 43985293)
4. Amdam GV, Norberg K, Fondrk MK, et al. (2004) Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. Proceedings of the National Academy of Sciences, USA, 101, 11350-11355. (Pubitemid 39038350)
5. Amdam GV, Csondes A, Fondrk MK, et al. (2006) Complex social behaviour derived from maternal reproductive traits. Nature, 439, 76-78. (Pubitemid 43053631)
6. de Azevedo SV, Hartfelder K, (2008) The insulin signaling pathway in honey bee (Apis mellifera) caste development- differential expression of insulin-like peptides and insulin receptors in queen and worker larvae. Journal of Insect Physiology, 54, 1064-1071.
7. Barchuk AR, Bitondi MMG, Simoes ZLP, (2002) Effects of juvenile hormone and ecdysone on the timing of vitellogenin appearance in hemolymph of queen and worker pupae of Apis mellifera. Journal of Insect Science (Tucson), 2, 1-9.
8. Barchuk AR, Cristino AS, Kucharski R, et al. (2007) Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. BMC Developmental Biology, 7, 70.
9. Barron AB, Oldroyd BP, Ratnieks FLW, (2001) Worker reproduction in honey-bees (Apis) and the anarchic syndrome: a review. Behavioral Ecology and Sociobiology, 50, 199-208. (Pubitemid 32748074)
10. Beckstead RB, Lam G, Thummel CS, (2005) The genomic response to 20-hydroxyecdysone at the onset of Drosophila metamorphosis. Genome Biology, 6, R99.
11. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate-a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B, 57, 289-300.
12. Bloch G, Borst DW, Huang Z, et al. (2000) Juvenile hormone titers, juvenile hormone biosynthesis, ovarian development and social environment in Bombus terrestris. Journal of Insect Physiology, 46, 47-57. (Pubitemid 29498172)
13. Boerjan B, Cardoen D, Bogaerts A, et al. (2010) Mass spectrometric profiling of (neuro)-peptides in the worker honeybee, Apis mellifera. Neuropharmacology, 58, 248-258.
14. Bourke AFG, (1988) Worker reproduction in the higher Eusocial hymenoptera. Quarterly Review of Biology, 63, 291-311. (Pubitemid 19324057)
15. Brito RM, McHale M, Oldroyd BP, (2010) Expression of genes related to reproduction and pollen foraging in honey bees (Apis mellifera) narcotized with carbon dioxide. Insect Molecular Biology, 19, 451-461.
16. Brockmann A, Annangudi SP, Richmond TA, et al. (2009) Quantitative peptidomics reveal brain peptide signatures of behavior. Proceedings of the National Academy of Sciences, USA, 106, 2383-2388.
17. Canavoso LE, Jouni ZE, Karnas KJ, et al. (2001) Fat metabolism in insects. Annual Review of Nutrition, 21, 23-46. (Pubitemid 32695263)
18. Capella ICS, Hartfelder K, (1998) Juvenile hormone effect on DNA synthesis and apoptosis in caste-specific differentiation of the larval honey bee (Apis mellifera L.) ovary. Journal of Insect Physiology, 44, 385-391. (Pubitemid 28319470)
19. Corona M, Velarde RA, Remolina S, et al. (2007) Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proceedings of the National Academy of Sciences, USA, 104, 7128-7133. (Pubitemid 47186020)
20. Dampney JR, Barron AB, Oldroyd BP, (2004) Measuring the cost of worker reproduction in honeybees: work tempo in an 'anarchic' line. Apidologie, 35, 83-88. (Pubitemid 38143360)
21. Darwin C, (1859) On the origin of species by means of natural selection, John Murray, London.
22. Elango N, Hunt BG, Goodisman MA, et al. (2009) DNA methylation is widespread and associated with differential gene expression in castes of the honeybee, Apis mellifera. Proceedings of the National Academy of Sciences, USA, 106, 11206-11211.
23. Foret 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 Research, 16, 1404-1413. (Pubitemid 44664683)
24. Franks NR, Scovell E, (1983) Dominance and reproductive success among slave-making worker ants. Nature, 304, 724-725.
25. Gotz S, Garcia-Gomez JM, Terol J, et al. (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Research, 36, 3420-3435. (Pubitemid 351859009)
26. Grozinger CM, Sharabash NM, Whitfield CW, et al. (2003) Pheromone-mediated gene expression in the honey bee brain. Proceedings of the National Academy of Sciences, USA, 100 (Suppl. 2), 14519-14525. (Pubitemid 37499275)
27. Grozinger CM, Fan Y, Hoover SE, et al. (2007) Genome-wide analysis reveals differences in brain gene expression patterns associated with caste and reproductive status in honey bees (Apis mellifera). Molecular Ecology, 16, 4837-4848. (Pubitemid 350135217)
28. Guidugli KR, Hepperle C, Hartfelder K, (2004) A member of the short-chain dehydrogenase/reductase (SDR) superfamily is a target of the ecdysone response in honey bee (Apis mellifera) caste development. Apidologie, 35, 37-47. (Pubitemid 38149415)
29. Guidugli KR, Nascimento AM, Amdam GV, et al. (2005) Vitellogenin regulates hormonal dynamics in the worker caste of a eusocial insect. FEBS Letters, 579, 4961-4965. (Pubitemid 41242836)
30. Guidugli-Lazzarini KR, do Nascimento AM, Tanaka ED, et al. (2008) Expression analysis of putative vitellogenin and lipophorin receptors in honey bee (Apis mellifera L.) queens and workers. Journal of Insect Physiology, 54, 1138-1147.
31. Hamilton WD, (1964b) Genetical evolution of social behaviour I & II. Journal of Theoretical Biology, 7, 1-52.
32. Hartfelder K, Kostlin K, Hepperle C, (1995) Ecdysteroid-dependent protein-synthesis in caste-specific development of the larval honey-bee ovary. Rouxs Archives of Developmental Biology, 205, 73-80.
33. Hartfelder K, Bitondi MMG, Santana WC, et al. (2002) Ecdysteroid titer and reproduction in queens and workers of the honey bee and of a stingless bee: loss of ecdysteroid function at increasing levels of sociality? Insect Biochemistry and Molecular Biology, 32, 211-216. (Pubitemid 34076085)
34. Hepperle C, Hartfelder K, (2001) Differentially expressed regulatory genes in honey bee caste development. Naturwissenschaften, 88, 113-116. (Pubitemid 32417610)
35. Hillesheim E, Koeniger N, Moritz RFA, (1989) Colony performance in honeybees (Apis mellifera mapensis Esch) depends on the proportion of subordinate and dominant Workers. Behavioral Ecology and Sociobiology, 24, 291-296.
36. Hoover SER, Keeling CI, Winston ML, et al. (2003) The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften, 90, 477-480. (Pubitemid 37363559)
37. Hoover SER, Higo HA, Winston ML, (2006) Worker honey bee ovary development: seasonal variation and the influence of larval and adult nutrition. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology, 176, 55-63. (Pubitemid 41772263)
38. Hummon AB, Richmond TA, Verleyen P, et al. (2006) From the genome to the proteome: uncovering peptides in the Apis brain. Science, 314, 647-649. (Pubitemid 44646388)
39. Hunt GJ, Amdam GV, Schlipalius D, et al. (2007) Behavioral genomics of honeybee foraging and nest defense. Naturwissenschaften, 94, 247-267. (Pubitemid 46452155)
40. Kocher SD, Richard FJ, Tarpy DR, et al. (2008) Genomic analysis of post-mating changes in the honey bee queen (Apis mellifera). BMC Genomics, 9, 232.
41. Kocher SD, Ayroles JF, Stone EA, et al. (2010) Individual variation in pheromone response correlates with reproductive traits and brain gene expression in worker honey bees. PLoS ONE, 5, e9116.
42. Kubo T, Sasaki M, Nakamura J, et al. (1996) Change in the expression of hypopharyngeal-gland proteins of the worker honeybees (Apis mellifera L) with age and/or role. Journal of Biochemistry, 119, 291-295. (Pubitemid 26061526)
43. Kucharski R, Maleszka J, Foret S, et al. (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science, 319, 1827-1830. (Pubitemid 351451590)
44. Lindemans M, Liu F, Janssen T, et al. (2009) Adipokinetic hormone signaling through the gonadotropin-releasing hormone receptor modulates egg-laying in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 106, 1642-1647.
45. Linksvayer TA, Rueppell O, Siegel A, et al. (2009) The genetic basis of transgressive ovary size in honeybee workers. Genetics, 183, 693-707.
46. Maisonnasse A, Lenoir JC, Beslay D, et al. (2010) E-beta-ocimene, a volatile brood pheromone involved in social regulation in the honey bee colony (Apis mellifera). PLoS ONE, 5, e13531.
47. Martin SJ, Beekman M, Wossler TC, et al. (2002) Parasitic Cape honeybee workers, Apis mellifera capensis, evade policing. Nature, 415, 163-165. (Pubitemid 34059515)
48. Miller DG, Ratnieks FLW, (2001) The timing of worker reproduction and breakdown of policing behaviour in queenless honey bee (Apis mellifera L.) societies. Insectes Sociaux, 48, 178-184. (Pubitemid 32620779)
49. Mohammedi A, Paris A, Crauser D, et al. (1998) Effect of aliphatic esters on ovary development of queenless bees (Apis mellifera L.). Naturwissenschaften, 85, 455-458. (Pubitemid 28457572)
50. Oldroyd BP, Beekman M, (2008) Effects of selection for honey bee worker reproduction on foraging traits. PLoS Biology, 6, e56.
51. Oxley PR, Thompson GJ, Oldroyd BP, (2008) Four quantitative trait loci that influence worker sterility in the honeybee (Apis mellifera). Genetics, 179, 1337-1343.
52. Palmer KA, Oldroyd BP, (2000) Evolution of multiple mating in the genus Apis. Apidologie, 31, 235-248. (Pubitemid 30339856)
53. Park JM, Kunieda T, Kubo T, (2003) The activity of Mblk-1, a mushroom body-selective transcription factor from the honeybee, is modulated by the Ras/MAPK pathway. Journal of Biological Chemistry, 278, 18689-18694. (Pubitemid 36799497)
54. Patel A, Fondrk MK, Kaftanoglu O, et al. (2007) The making of a queen: TOR pathway is a key player in diphenic caste development. PLoS ONE, 2, e509.
55. Queller DC, (2003) Theory of genomic imprinting conflict in social insects. BMC Evolutionary Biology, 3, 15.
56. Rachinsky A, Hartfelder K, (1990) Corpora allata activity, a prime regulating element for caste-specific juvenile-hormone titer in honey-bee larvae (Apis-mellifera-carnica). Journal of Insect Physiology, 36, 189-194.
57. Rachinsky A, Strambi C, Strambi A, et al. (1990) Caste and metamorphosis-hemolymph titers of juvenile-hormone and ecdysteroids in last instar honeybee larvae. General and Comparative Endocrinology, 79, 31-38. (Pubitemid 20206161)
58. Ratnieks FLW, (1988) Reproductive harmony via mutual policing by workers in eusocial hymenoptera. American Naturalist, 132, 217-236. (Pubitemid 19324056)
59. Ratnieks FLW, (1993) Egg-laying, egg-removal, and ovary development by workers in queenright honey-bee colonies. Behavioral Ecology and Sociobiology, 32, 191-198. (Pubitemid 24406734)
60. Ratnieks FLW, Visscher PK, (1989) Worker policing in the honeybee. Nature, 342, 796-797. (Pubitemid 20424340)
61. Ratnieks FL, Wenseleers T, (2008) Altruism in insect societies and beyond: voluntary or enforced? Trends in Ecology & Evolution, 23, 45-52.
62. Ratnieks FLW, Foster KR, Wenseleers T, (2011) Darwin's special difficulty: the evolution of "neuter insects" and current theory. Behavioral Ecology and Sociobiology, 65, 481-492.
63. Rembold H, (1987) Caste specific modulation of juvenile-hormone titers in Apis-mellifera. Insect Biochemistry, 17, 1003-1006.
64. Robinson GE, Huang ZY, (1998) Colony integration in honey bees: genetic, endocrine and social control of division of labor. Apidologie, 29, 159-170. (Pubitemid 28163092)
65. Robinson GE, Vargo EL, (1997) Juvenile hormone in adult eusocial hymenoptera: gonadotropin and behavioral pacemaker. Archives of Insect Biochemistry and Physiology, 35, 559-583. (Pubitemid 127705854)
66. Robinson GE, Strambi C, Strambi A, et al. (1991) Comparison of juvenile-hormone and ecdysteroid hemolymph titers in adult worker and queen honey-bees (Apis-mellifera). Journal of Insect Physiology, 37, 929-935.
67. Robinson GE, Strambi C, Strambi A, et al. (1992) reproduction in worker honey-bees is associated with low juvenile-hormone titers and rates of biosynthesis. General and Comparative Endocrinology, 87, 471-480.
68. Sakagami SF, Akahira Y, (1958) Comparison of ovarian size and number of ovarioles between the workers of Japanese and European honeybees. Kontyu, 26, 103-109.
69. Santos KS, dos Santos LD, Mendes MA, et al. (2005) Profiling the proteome complement of the secretion from hypopharyngeal gland of Africanized nurse-honeybees (Apis mellifera L.). Insect Biochemistry and Molecular Biology, 35, 85-91. (Pubitemid 40015514)
70. Schafer MO, Dietemann V, Pirk CWW, et al. (2006) Individual versus social pathway to honeybee worker reproduction (Apis mellifera): pollen or jelly as protein source for oogenesis? Journal of Comparative Physiology A-Neuroethology Sensory Neural and Behavioral Physiology, 192, 761-768.
71. Slessor KN, Winston ML, Le Conte Y, (2005) Pheromone communication in the honeybee (Apis mellifera L.). Journal of Chemical Ecology, 31, 2731-2745. (Pubitemid 41597345)
72. Smyth G, (2005) Limma: linear models for microarray data. Bioinformatics and computational biology solutions using R and Bioconductor. Springer, New York, pp. 397-420.
73. Snodgrass RE, (1984) Anatomy of the honey bee. 1-334.
74. The Honeybee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature, 443, 931-949.
75. Thompson GJ, Kucharski R, Maleszka R, et al. (2006) Towards a molecular definition of worker sterility: differential gene expression and reproductive plasticity in honey bees. Insect Molecular Biology, 15, 637-644. (Pubitemid 44652083)
76. Thompson GJ, Yockey H, Lim J, et al. (2007) Experimental manipulation of ovary activation and gene expression in honey bee (Apis mellifera) queens and workers: testing hypotheses of reproductive regulation. Journal of Experimental Zoology Part A-Ecological Genetics and Physiology, 307, 600-610. (Pubitemid 47529078)
77. Thompson GJ, Kucharski R, Maleszka R, et al. (2008) Genome-wide analysis of genes related to ovary activation in worker honey bees. Insect Molecular Biology, 17, 657-665.
78. Toth AL, Varala K, Henshaw MT, et al. (2010) Brain transcriptomic analysis in paper wasps identifies genes associated with behaviour across social insect lineages. Proceedings of the Royal Society B-Biological Sciences, 277, 2139-2148.
79. Wanner KW, Nichols AS, Walden KKO, et al. (2007) A honey bee odorant receptor for the queen substance 9-oxo-2-decenoic acid. Proceedings of the National Academy of Sciences, USA, 104, 14383-14388. (Pubitemid 350003270)
80. Weaver RJ, Audsley N, (2009) Neuropeptide regulators of juvenile hormone synthesis. Annals of the New York Academy of Sciences, 1163, 316-329.
81. Wenseleers T, Ratnieks FL, (2006) Enforced altruism in insect societies. Nature, 444, 50. (Pubitemid 44684748)
82. Wheeler DE, Buck N, Evans JD, (2006) Expression of insulin pathway genes during the period of caste determination in the honey bee, Apis mellifera. Insect Molecular Biology, 15, 597-602. (Pubitemid 44652089)
83. Whitfield CW, Cziko AM, Robinson GE, (2003) Gene expression profiles in the brain predict behavior in individual honey bees. Science, 302, 296-299. (Pubitemid 37248762)
84. Whitfield CW, Ben-Shahar Y, Brillet C, et al. (2006) Genomic dissection of behavioral maturation in the honey bee. Proceedings of the National Academy of Sciences, USA, 103, 16068-16075. (Pubitemid 44715152)
85. Winston ML, (1987) The biology of the honey bee, Harvard University, Cambridge, Massachusetts.
86. Wolschin F, Amdam GV, (2007) Comparative proteomics reveal characteristics of life-history transitions in a social insect. Proteome Science, 5, 10.
87. Yamanaka N, Yamamoto S, Zitnan D, et al. (2008) Neuropeptide receptor transcriptome reveals unidentified neuroendocrine pathways. PLoS ONE, 3, e3048.