The developmental genetics and physiology of honeybee societies

Animal Behaviour

Volumn 79, Issue 5, 2010, Pages 973-980

  Amdam, Gro V ^a,b   Page Jr , Robert E ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

insulin like signalling; juvenile hormone; nuclear hormone receptor; ovary; pollen hoarding; reproductive behaviour; social evolution; vitellogenin; worker behaviour

Indexed keywords

ADAPTIVE RADIATION; BIOLOGICAL DEVELOPMENT; CACHING; EUSOCIALITY; EVOLUTIONARY BIOLOGY; FORAGING BEHAVIOR; GENE EXPRESSION; HONEYBEE; HORMONE; HYPOTHESIS TESTING; LABOR DIVISION; LIFE HISTORY TRAIT; PHYSIOLOGY; POLLEN; PROTEIN; SENSORY SYSTEM; SEXUAL CONFLICT; SIGNALING; SOCIAL BEHAVIOR; STERILITY; WORKER CASTE;

ANIMALIA; APIS MELLIFERA; APOIDEA; DECAPODA (CRUSTACEA); FORMICIDAE; HETEROCEPHALUS GLABER; HEXAPODA; RATTUS;

EID: 77950865705     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2010.02.007     Document Type: Article

References (84)

1. Amdam G.V., and Omholt S.W. The hive bee to forager transition in honeybee colonies: the double repressor hypothesis. Journal of Theoretical Biology 223 (2003) 451-464
2. Amdam G.V., and Page R.E. Oldroyd and Beekman do not test ground plan hypothesis that explains origins of social behavior. PLoS Biology 6 (2008) e56r2248
3. Amdam G.V., Norberg K., Hagen A., and Omholt S.W. Social exploitation of vitellogenin. Proceedings of the National Academy of Sciences, U.S.A. 100 (2003) 1799-1802
4. Amdam G.V., Simões Z.L.P., Guidugli K.R., Norberg K., and Omholt S.W. Disruption of vitellogenin gene function in adult honeybees by intra-abdominal injection of double-stranded RNA. BMC Biotechnology 3 (2003) 1-8
5. Amdam G.V., Hartfelder K., Norberg K., Hagen A., and Omholt S.W. Altered physiology in worker honey bees (Hymenoptera: Apidae) infested by the mite Varroa destructor (Acari: Varroidae): a factor in colony loss during over-wintering?. Journal of Economic Entomology 97 (2004) 741-747
6. Amdam G.V., Norberg K., Fondrk M.K., and Page R.E. Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. Proceedings of the National Academy of Sciences, U.S.A. 101 (2004) 11350-11355
7. Amdam G.V., Csondes A., Fondrk M.K., and Page R.E. Complex social behavior derived from maternal reproductive traits. Nature 439 (2006) 76-78
8. Amdam G.V., Nilsen K.A., Norberg K., Fondrk M.K., and Hartfelder K. Variation in endocrine signaling underlies variation in social life history. American Naturalist 170 (2007) 37-46
9. Amdam G.V., Ihle K.E., and Page R.E. Regulation of honey bee (Apis mellifera) life histories by vitellogenin. In: Pfaff D., Arnold A., Etgen A., Fahrbach S., and Rubin R. (Eds). Hormones, Brain and Behavior (2009), Elsevier Academic Press, San Diego
10. Ament S.A., Corona M., Pollock H.S., and Robinson G.E. Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. Proceedings of the National Academy of Sciences, U.S.A. 105 (2008) 4226-4231
11. Atchley D.P., Weaver K.L., and Eckel L.A. Taste responses to dilute sucrose solutions are modulated by stage of the estrous cycle and fenfluramine treatment in female rats. Physiology & Behavior 86 (2005) 265-271
12. Barchuk A.R., Bitondi M.M.G., and Simões Z.L.P. 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 2 (2002) 1-8. Available online: insectscience.org/2.1
13. Barchuk A.R., Maleszka R., and Simões Z.L.P. Apis mellifera ultraspiracle: cDNA sequence and rapid up-regulation by juvenile hormone. Insect Molecular Biology 13 (2004) 459-467
14. Barron A.B., Oldroyd B.P., and Ratnieks F.L.W. Worker reproduction in honey-bees (Apis) and the anarchic syndrome: a review. Behavioral Ecology and Sociobiology 50 (2001) 199-208
15. Brandt B.W., Zwaan B.J., Beekman M., Westendorp R.G.J., and Slagboom P.E. Shuttling between species for pathways of lifespan regulation: a central role for the vitellogenin gene family?. Bioessays 27 (2005) 339-346
16. Calderone N.W., and Page R.E. Effects of interactions among genotypically diverse nestmates on task specialization by foraging honey bees (Apis mellifera). Behavioral Ecology and Sociobiology 30 (1992) 219-226
17. Cayre M., Strambi C., Charpin P., Augier R., Renucci M., and Strambi A. Inhibition of polyamine biosynthesis alters oviposition behavior in female crickets. Behavioral Neuroscience 110 (1996) 1117-1125
18. Chakraborty T.R., and Gore A.C. Aging-related changes in ovarian hormones, their receptors, and neuroendocrine function. Experimental Biology and Medicine 229 (2004) 977-987
19. Clarke S.N., and Ossenkopp K.P. Taste reactivity responses in rats: influence of sex and the estrous cycle. American Journal of Physiology 274 (1998) R718-R724
20. Clements A.N. The Biology of Mosquitoes: Volume 1: Development, Nutrition and Reproduction (1992), Chapman & Hall, New York
21. Corona M., Velarde R.A., Remolina S., Moran-Lauter A., Wang Y., Hughes K.A., and Robinson G.E. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proceedings of the National Academy of Sciences, U.S.A. 104 (2007) 7128-7133
22. Dingle H., and Winchell R. Juvenile hormone as a mediator of plasticity in insect life histories. Archives of Insect Biochemistry and Physiology 35 (1997) 359-373
23. Dolezal A., Brent C., Gadau J., Hölldobler B., and Amdam G.V. Endocrine physiology of division of labor in Pogonomyrmex californicus founding queens. Animal Behaviour 77 (2009) 1005-1010
24. Duportets L., Dufour M.C., Couillaud F., and Gadenne C. Biosynthetic activity of corpora allata, growth of sex accessory glands and mating in the male moth Agrotis ipsilon (Hufnagel). Journal of Experimental Biology 201 (1998) 2425-2432
25. Engels W. Occurrence and significance of vitellogenins in female castes of social hymenoptera. American Zoologist 14 (1974) 1229-1237
26. Engels W. Social Insects: an Evolutionary Approach to Castes and Reproduction (1990), Springer-Verlag, Berlin
27. Engels W., Kaatz H., Zillikens A., Simões Z.L.P., Truve A., Braun R.P., and Dittrich F. Honey bee reproduction: vitellogenin and caste-specific regulation of fertility. In: Hoshi M., and Yamashita O. (Eds). Advances in Invertebrate Reproduction (1990), Elsevier Science, Amsterdam 495-502
28. Fewell J.H., and Page R.E. Colony-level selection effects on individual and colony foraging task performance in honeybees, Apis mellifera L. Behavioral Ecology and Sociobiology 48 (2000) 173-181
29. Flatt T., Tu M.P., and Tatar M. Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history. BioEssays 27 (2005) 999-1010
30. Guidugli K.R., Nascimento A.M., Amdam G.V., Barchuk A.R., Omholt S.W., Simões Z.L.P., and Hartfelder K. Vitellogenin regulates hormonal dynamics in the worker caste of a eusocial insect. FEBS Letters 579 (2005) 4961-4965
31. Hancock R.G., and Foster W.A. Exogenous Juvenile hormone and methoprene, but not male accessory gland substances or ovariectomy, affect the blood/nectar choice of female Culex nigiripalpus mosquitoes. Medical and Veterinary Entomology 14 (2000) 373-382
32. Hölldobler B., and Wilson E.O. The Ants (1990), Belknap Press of Harvard University Press, Cambridge, Massachusetts
33. Hölldobler B., and Wilson E.O. The Superorganism: the Beauty, Elegance, and Strangeness of Insect Societies (2008), W.W. Norton, New York
34. Honey Bee Genome Sequencing Consortium. Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443 (2006) 931-949
35. Hoover S.E.R., Keeling C.I., Winston M.L., and Slessor K.N. The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 90 (2003) 477-480
36. Huang Z.-Y., and Robinson G.E. Seasonal changes in juvenile hormone titers and rates of biosynthesis in honey bees. Journal of Comparative Physiology B 165 (1995) 18-28
37. Hunt G.J., Page R.E., Fondrk M.K., and Dullum C.J. Major quantitative trait loci affecting honey-bee foraging behavior. Genetics 141 (1995) 1537-1545
38. Hunt G.J., Amdam G.V., Schlipalius D., Emore C., Sardesai N., Williams C.E., Rueppell O., Guzmán-Novoa E., Arechavaleta-Velasco M., Chandra S., Fondrk M.K., Beye M., and Page Jr. R.E. Behavioral genomics of honeybee foraging and nest defense. Naturwissenschaften 94 (2007) 247-267
39. Ihle, K. E., Page, R. E., Jr, Frederick, K., Fondrk, M. K. & Amdam, G. V. 2010. Genotype effect on regulation of behaviour by vitellogenin supports reproductive origin of honeybee foraging bias. Animal Behaviour, 79, 1001-1006.
40. Khila A., and Abouheif E. Reproductive constraint is a developmental mechanism that maintains social harmony in advanced ant societies. Proceedings of the National Academy of Sciences, U.S.A. 105 (2008) 17884-17889
41. Klowden M.J. The endogenous regulation of mosquito reproductive behavior. Experientia 46 (1990) 660-670
42. Lam G.T., Jiang C., and Thummel C.S. Coordination of larval and prepupal gene expression by the DHR3 orphan receptor during Drosophila metamorphosis. Development 124 (1997) 1757-1769
43. Linksvayer T.A., Fondrk M.K., and Page Jr. R.E. Honeybee social regulatory networks are shaped by colony-level selection. American Naturalist 173 (2009) E99-E107
44. Makert G.R., Paxton R.J., and Hartfelder K. Ovariole number: a predictor for differential reproductive success among worker subfamilies in queenless honey bee (Apis mellifera L.) colonies. Behavioral Ecology and Sociobiology 60 (2006) 815-825
45. Marco Antonio D.S., Guidugli-Lazzarini K.R., Nascimento A.M., Simões Z.L.P., and Hartfelder K. RNAi-mediated silencing of vitellogenin gene function turns honeybee (Apis mellifera) workers into extremely precocious foragers. Naturwissenschaften 95 (2008) 953-961
46. Mitchell S.D. Biological Complexity and Integrative Pluralism (2003), Cambridge University Press, Cambridge, Massachusetts
47. Nelson C.M., Ihle K., Amdam G.V., Fondrk M.K., and Page R.E. The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biology 5 (2007) 673-677
48. Oldroyd B.P., Wossler T., and Ratnieks F.L.W. Regulation of ovary activation in worker honey-bees (Apis mellifera): larval signal production and adult response thresholds differ between anarchistic and wild-type bees. Behavioral Ecology and Sociobiology 50 (2001) 366-370
49. Oldroyd B.P., and Beekman M. Effects of selection for honey bee worker reproduction on foraging traits. PLoS Biology 6 (2008) e56
50. Oster G.F., and Wilson E.O. Caste and Ecology in the Social Insects (1978), Princeton University Press, Princeton, New Jersey
51. Page R.E., and Amdam G.V. The making of a social insect: developmental architectures of social design. BioEssays 29 (2007) 334-343
52. Page R.E., and Fondrk M.K. The effects of colony-level selection on the social organization of honey bee (Apis mellifera L.) colonies: colony-level components of pollen hoarding. Behavioral Ecology and Sociobiology 36 (1995) 135-144
53. Page R.E., and Mitchell S.D. Self organization and adaptation in insect societies. In: Fine A., Forbes M., and Wessels L. (Eds). PSA (1991), Philosophy of Science Association, East Lansing, Michigan 289-298
54. Page R.E., Robinson G.E., Fondrk M.K., and Nasr M.E. Effects of worker genotypic diversity on honey bee colony development and behavior (Apis mellifera L.). Behavioral Ecology and Sociobiology 36 (1995) 387-396
55. Page R.E., Erber J., and Fondrk M.K. The effect of genotype on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.). Journal of Comparative Physiology A 182 (1998) 489-500
56. Page R.E., Fondrk M.K., Hunt G.J., Guzman-Novoa E., Humphries M.A., Nguyen K., and Greene A.S. Genetic dissection of honeybee (Apis mellifera L.) foraging behavior. Journal of Heredity 91 (2000) 474-479
57. Pankiw T., and Page R.E. Response thresholds to sucrose predict foraging division of labor in honeybees. Behavioral Ecology and Sociobiology 47 (2000) 265-267
58. Pankiw T., and Page R.E. Genotype and colony environment affect honeybee (Apis mellifera L.) development and foraging behavior. Behavioral Ecology and Sociobiology 51 (2001) 87-94
59. Pinto L.Z., Bitondi M.M.G., and Simões Z.L.P. Inhibition of vitellogenin synthesis in Apis mellifera workers by a juvenile hormone analogue, pyriproxyfen. Journal of Insect Physiology 46 (2000) 153-160
60. Robinson G.E. Regulation of division of labor in insect societies. Annual Review of Entomology 37 (1992) 637-665
61. Rueppell O., Pankiw T., Nielson D., Fondrk M.K., Beye M., and Page R.E. The genetic architecture of the behavioral ontogeny of honey bee workers. Genetics 167 (2004) 1767-1779
62. Rueppell O., Pankiw T., and Page R.E. Pleiotropy, epistasis and new QTL: the genetic architecture of honey bee foraging behavior. Journal of Heredity 95 (2004) 481-491
63. Rueppell O., Hunggims E., and Tingek S. Association between larger ovaries and pollen foraging in queenless Apis cerana workers supports the reproductive ground-plan hypothesis of social evolution. Journal of Insect Behaviour 21 (2008) 317-321
64. Rutz W., and Lüscher M. The occurrence of vitellogenin in workers and queens of Apis mellifica and the possibility of its transmission to the queen. Journal of Insect Physiology 20 (1974) 897-909
65. Scheiner R., Page R.E., and Erber J. The effects of genotype, foraging role, and sucrose responsiveness on the tactile learning performance of honey bees (Apis mellifera L.). Neurobiology of Learning and Memory 76 (2001) 138-150
66. Schmidt-Capella I.C., and Hartfelder K. 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 (1998) 385-391
67. Schubiger M., and Truman J.W. The RXR ortholog USP suppresses early metamorphic processes in Drosophila in the absence of ecdysteroids. Development 127 (2000) 1151-1159
68. Seehuus S.C., Norberg K., Gimsa U., Krekling T., and Amdam G.V. Reproductive protein protects sterile honey bee workers from oxidative stress. Proceedings of the National Academy of Sciences, U.S.A. 103 (2006) 962-967
69. Seeley T.D. Adaptive significance of the age polyethism schedule in honeybee colonies. Behavioral Ecology and Sociobiology 11 (1982) 287-293
70. Simonet G., Poels J., Claeys I., Van Loy T., Franssens V., De Loof A., and Broeck J.V. Neuroendocrinological and molecular aspects of insect reproduction. Journal of Neuroendocrinology 16 (2004) 649-659
71. Snodgrass R.E. Anatomy of the Honey Bee (1956), Comstock, New York
72. Tatar M. The neuroendocrine regulation of Drosophila aging. Experimental Gerontology 39 (2004) 1745-1750
73. Toth A.L., and Robinson G.E. Evo-devo and the evolution of social behavior. Trends in Genetics 23 (2007) 334-341
74. Tsuruda J., Amdam G.V., and Page R.E. Sensory response system of social behavior tied to female reproductive traits. PLoS One 3 (2008) e3397
75. Tu M.P., and Tatar M. Juvenile diet restriction and the aging and reproduction of adult Drosophila melanogaster. Aging Cell 2 (2003) 327-333
76. Vancassel M., Foraste M., Strambi A., and Strambi C. Normal and experimentally induced changes in hormonal hemolymph titers during parental behavior of the earwig Labidura riparia. General and Comparative Endocrinology 56 (1984) 444-456
77. Velarde R.A., Robinson G.E., and Fahrbach S.E. Coordinated responses to developmental hormones in the Kenyon cells of the adult worker honey bee brain (Apis mellifera L.). Journal of Insect Physiology 55 (2009) 59-69
78. Wang Y., Amdam G.V., Rueppell O., Wallrichs M.A., Fondrk M.K., Kaftanoglu O., and Page Jr. R.E. PDK1 and HR46 gene homologs tie social behavior to ovary signals. PLoS One 4 (2009) e4899
79. West-Eberhard M.J. Flexible strategy and social evolution. In: Itô Y., Brown J.L., and Kikkawa J. (Eds). Animal Societies: Theories and Fact (1987), Japan Science Society Press, Tokyo 35-51
80. West-Eberhard M.J. Wasp societies as microcosms for the study of development and evolution. In: Turillazzi S., and West-Eberhard M.J. (Eds). Natural History and Evolution of Paper Wasp (1996), Oxford University Press, New York 290-317
81. Wheeler W.M. The ant-colony as an organism. Morphology 22 (1911) 307-325
82. Wilson E.O. The Insect Societies (1971), Belknap Press of Harvard University Press, Cambridge, Massachusetts
83. Wilson D.S., and Sober E. Reviving the superorganism. Journal of Theoretical Biology 136 (1989) 337-356
84. Zufelato M.S., Bitondi M.M.G., Simões Z.L.P., and Hartfelder K. The juvenile hormone analog pyriproxyfen affects ecdysteroid-dependent cuticle melanization and shifts the pupal ecdysteroid peak in the honey bee (Apis mellifera). Arthropod Structure & Development 29 (2000) 111-119