Social context, stress, and plasticity of aging

Aging Cell

Volumn 10, Issue 1, 2011, Pages 18-27

  Amdam, Gro V ^a,b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

Aging reversal; Honey bee; Insulin like peptides; Recovery related plasticity; Social contact; Stress reactivity

Indexed keywords

VITELLOGENIN;

AGING; ANIMAL BEHAVIOR; DROSOPHILA; ENVIRONMENTAL FACTOR; FORAGER; GENE EXPRESSION; HONEYBEE; INSECT SOCIETY; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; ONTOGENY; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; REVIEW; SOCIAL BEHAVIOR; SOCIAL ENVIRONMENT; SOCIAL INTERACTION; SOCIAL STRESS; SURVIVAL;

AGING; ANIMALS; BEES; BEHAVIOR, ANIMAL; DROSOPHILA; ENERGY METABOLISM; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; SOCIAL ENVIRONMENT; STRESS, PHYSIOLOGICAL;

APIS MELLIFERA; HEXAPODA;

EID: 78651341456     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2010.00647.x     Document Type: Review

References (109)

1. Al-Lawati AL, Bienefeld K (2009) Maternal age effects on embryo mortality and juvenile development of offspring in the honey bee (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 102, 881-888.
2. Amdam GV, Omholt SW (2002) The regulatory anatomy of honeybee lifespan. J. Theor. Biol. 216, 209-228.
3. Amdam GV, Omholt SW (2003) The hive bee to forager transition in honeybee colonies: the double repressor hypothesis. J. Theor. Biol. 223, 451-464.
4. Amdam GV, Seehuus SC (2006) Order, disorder, death: lessons from a superorganism. Adv. Cancer Res. 95, 31-60.
5. Amdam GV, Norberg K, Hagen A, Omholt SW (2003) Social exploitation of vitellogenin. Proc. Natl Acad. Sci. USA 100, 1799-1802.
6. Amdam GV, Simões ZLP, Hagen A, Norberg K, Schrøder K, Mikkelsen O, Kirkwood TBL, Omholt SW (2004) Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees. Exp. Gerontol. 39, 767-773.
7. Amdam GV, Aase ALTO, Seehuus SC, Norberg K, Hartfelder K, Fondrk MK (2005) Social reversal of immunosenescence in honey bee workers. Exp. Gerontol. 40, 939-947.
8. Amdam GV, Nilsen KA, Norberg K, Fondrk MK, Hartfelder K (2007) Variation in endocrine signaling underlies variation in social life history. Am. Nat. 170, 37-46.
9. Ament SA, Corona M, Pollock HS, Robinson GE (2008) Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. Proc. Natl Acad. Sci. USA 105, 4226-4231.
10. Baker N, Wolschin F, Amdam GV (2010) Age-Related Learning Deficits can be Reversed in Honeybees Apis Mellifera. MS thesis, Arizona State University.
11. Bedick JC, Tunaz H, Aliza ARN, Putnam SM, Ellis MD, Stanley DW (2001) Eicosanoids act in nodulation reactions to bacterial infections in newly emerged adult honey bees, Apis mellifera, but not in older foragers. Comp. Biochem. Physiol. 130, 107-117.
12. Beggs KT, Glendining KA, Marechal NM, Vergoz V, Nakamura I, Slessor KN, Mercer AR (2007) Queen pheromone modulates brain dopamine function in worker honey bees. Proc. Natl Acad. Sci. USA 104, 2460-2464.
13. Behrends A, Scheiner R (2010) Learning at old age: a study on winter bees. Front. Behav. Neurosci. 4, 15.
14. Behrends A, Scheiner R, Baker N, Amdam GV (2007) Cognitive aging is linked to social role in honey bees (Apis mellifera). Exp. Gerontol. 42, 1146-1153.
15. Bisschop MI, Kriegsman DM, van Tilburg TG, Penninx BW, van Eijk JT, Deeg DJ (2003) The influence of differing social ties on decline in physical functioning among older people with and without chronic diseases: the Longitudinal Aging Study Amsterdam. Aging Clin. Exp. Res. 15, 164-173.
16. Broughton S, Partridge L (2009) Insulin/IGF-like signalling, the central nervous system and aging. Biochem. J. 418, 1-12.
17. Charles ST, Carstensen LL (2010) Social and emotional aging. Annu. Rev. Psychol. 61, 383-409.
18. 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. USA 104, 7128-7133.
19. Crailsheim K (1990) The protein balance of the honey bee worker. Apidologie 21, 417-429.
20. Diangelo JR, Bland ML, Bambina S, Cherry S, Birnbaum MJ (2009) The immune response attenuates growth and nutrient storage in Drosophila by reducing insulin signaling. Proc. Natl Acad. Sci. USA 106, 20853-20858.
21. Dukas R (2008) Mortality rates of honey bees in the wild. Insectes Soc. 55, 252-255.
22. Elekonich MM, Roberts SP (2005) Honey bees as a model for understanding mechanisms of life history transitions. Comp. Biochem. Physiol. A 141, 362-371.
23. Finch CE (1990) Longevity, Senescence and the Genome. Chicago: Univ Chicago Press.
24. Fischer P, Grozinger CM (2008) Pheromonal regulation of starvation resistance in honey bee workers (Apis mellifera). Naturwissenschaften 95, 723-729.
25. Flatt T, Tu MP, Tatar M (2005) Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history. Bioessays 27, 999-1010.
26. Flatt T, Heyland A, Rus F, Porpiglia E, Sherlock C, Yamamoto R, Garbuzov A, Palli SR, Tatar M, Silverman N (2008) Hormonal regulation of the humoral innate immune response in Drosophila melanogaster. J. Exp. Biol. 211, 2712-2724.
27. Fluri P, Wille H, Gerig L, Lüscher M (1977) Juvenile hormone, vitellogenin and haemocyte composition in winter worker honeybees (Apis mellifera). Experientia 33, 1240-1241.
28. Gary NE (1992) Activities and behavior of honey bees. In The Hive and the Honey Bee (Graham JM ed.). Hamilton: Dadant & Sons, pp. 269-371.
29. Gruntenko NE, Wilson TG, Monastirioti M, Rauschenbach IY (2000) Stress-reactivity and juvenile hormone degradation in Drosophila melanogaster strains having stress-related mutations. Insect Biochem. Mol. Biol. 30, 775-783.
30. Gruntenko NE, Chentsova NA, Andreenkova EV, Bownes M, Segal D, Adonyeva NV, Rauschenbach IY (2003) Stress response in a juvenile hormone-deficient Drosophila melanogaster mutant apterous56f. Insect Mol. Biol. 12, 353-363.
31. Guidugli KR, Nascimento AM, Amdam GV, Barchuk AR, Omholt SW, Simões ZLP, Hartfelder K (2005) Vitellogenin regulates hormonal dynamics in the worker caste of a eusocial insect. FEBS Lett. 579, 4961-4965.
32. Haddad LS, Kelbert L, Hulbert AJ (2007) Extended longevity of queen honey bees compared to workers is associated with peroxidation-resistant membranes. Exp. Gerontol. 42, 601-609.
33. Harris JW, Woodring J (1992) Effects of stress, age, season, and source colony on levels of octopamine, dopamine and serotonin in the honey bee (Apis mellifera L.) brain. J. Insect Physiol. 38, 29-35.
34. Hart CL, Taylor MD, Davey Smith G, Whalley LJ, Starr JM, Hole DJ, Wilson V, Deary IJ (2003) Childhood IQ, social class, deprivation, and their relationships with mortality and morbidity risk in later life. Psychosom. Med. 65, 877-883.
35. Haydak MH (1963) Age of nurse bees and brood rearing. Minnesota Agric. Exp. Sta. Sci. J. Ser. 5122, 101-103.
36. Hölldobler B, Wilson EO (2008) The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies. New York: W. W. Norton.
37. Holtzman RE, Rebok GW, Saczynski JS, Kouzis AC, Wilcox Doyle K, Eaton WW (2004) Social network characteristics and cognition in middle-aged and older adults. J. Gerontol. B 59, P278-P284.
38. Huang Z-Y, Robinson GE (1992) Honeybee colony integration: Worker-worker interactions mediate hormonally regulated plasticity in division of labor. Proc. Natl Acad. Sci. USA 89, 11726-11729.
39. Huang Z-Y, Robinson GE (1995) Seasonal changes in juvenile hormone titers and rates of biosynthesis in honey bees. J. Comp. Physiol. B. 165, 18-28.
40. Huang Z-Y, Robinson GE (1996) Regulation of honey bee division of labor by colony age demography. Behav. Ecol. Sociobiol. 39, 147-158.
41. Ihle KE, Page RE, Frederick K, Fondrk MK, Amdam GV (2010) Genotype effect on regulation of behaviour by vitellogenin supports reproductive origin of honeybee foraging bias. Anim. Behav. 79, 1001-1006.
42. Jaycox ER, Skowronek W, Guynn G (1974) Behavioral changes in worker honey bees (Apis mellifera) induced by injections of a juvenile hormone mimic. Ann. Entomol. Soc. Am. 67, 529-534.
43. Kaatz H, Eichmüller S, Kreissl S (1994) Stimulatory effect of octopamine on juvenile hormone biosynthesis in honey bees (Apis mellifera): physiological and immunocytochemical evidence. J. Insect Physiol. 40, 865-872.
44. Kenyon C (2005) The plasticity of aging: insights from long-lived mutants. Cell 120, 449-460.
45. Kudielka BM, Schmidt-Reinwald AK, Hellhammer DH, Schurmeyer T, Kirschbaum C (2000) Psychosocial stress and HPA functioning: no evidence for a reduced resilience in healthy elderly men. Stress 3, 229-240.
46. Lazareva AA, Roman G, Mattox W, Hardin PE, Dauwalder B (2007) A role for the adult fat body in Drosophila male courtship behavior. PLoS Genet. 3, e16.
47. Le Conte Y, Sreng L, Trouiller J (1994) The recognition of larvae by worker honeybees. Naturwissenschaften 81, 462-465.
48. Leoncini I, Le Conte Y et al. (2004) Regulation of behavioral maturation by a primer pheromone produced by adult worker honey bees. Proc. Natl Acad. Sci. USA 101, 17559-17564.
49. Lin HR, Dusset C, Huang ZY (2004) Short-term changes in juvenile hormone titers in honey bee workers due to stress. Apidologie 35, 319-327.
50. Liu H, Sadygov RG, Yates JR III (2004) A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 76, 4193-4201.
51. Mardilovich K, Pankratz SL, Shaw LM (2009) Expression and function of the insulin receptor substrate proteins in cancer. Cell Commun. Signal. 7, 14.
52. Maurizio A (1950) The influence of pollen feeding and brood rearing on the length of life and physiological condition of the honeybee preliminary report. Bee World 31, 9-12.
53. Menzel R, Leboulle G, Eisenhardt D (2006) Small brains, bright minds. Cell 124, 237-239.
54. Miojevic BD (1940) A new interpretation of the social life of the honeybee. Bee World 21, 39-41.
55. Münch D, Amdam GV (2010) The curious case of aging plasticity in honey bees. FEBS Lett. 584, 2496-2503.
56. Münch D, Baker N, Kreibich C, Amdam GV (2010) In the laboratory and during free-flight: aged honey bees reveal learning and extinction deficits that mirror mammalian functional decline. PLoS ONE 5, e13504.
57. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, Li H, Kenyon C (2003) Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424, 277-284.
58. Nelson CM, Ihle K, Amdam GV, Fondrk MK, Page RE (2007) The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biol. 5, 673-677.
59. Nilsen KA, Ihle KE, Frederick K, Smedal B, Fondrk MK, Hartfelder K, Amdam GV (2011) In honeybee fat body, insulin-like peptide genes respond differently to manipulation of social behavioral physiology. J. Exp. Biol. in press.
60. Omholt SW (1987) Thermoregulation in the winter cluster of the honeybee, Apis mellifera. J. Theor. Biol. 128, 219-231.
61. Page RE, Peng CY-S (2001) Aging and development in social insects with emphasis on the honey bee, Apis mellifera L. Exp. Gerontol. 36, 695-711.
62. Pankiw T (2004) Worker honey bee pheromone regulation of foraging ontogeny. Naturwissenschaften 91, 178-181.
63. Pankiw T, Page RE (2003) Effect of pheromones, hormones, and handling on sucrose response thresholds of honey bees (Apis mellifera L.). J. Comp. Physiol. A. 189, 675-684.
64. Patel A, Fondrk MK, Kaftanoglu O, Emore C, Hunt G, Amdam GV (2007) The making of a queen: TOR pathway governs diphenic caste development. PLoS ONE 6, e509.
65. Pierce SB, Costa M et al. (2001) Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes Dev. 15, 672-686.
66. Pinto LZ, Bitondi MMG, Simões ZLP (2000) Inhibition of vitellogenin synthesis in Apis mellifera workers by a juvenile hormone analogue, pyriproxyfen. J. Insect Physiol. 46, 153-160.
67. Ramsden E (2007) A differential paradox: the controversy surrounding the Scottish mental surveys of intelligence and family size. J. Hist. Behav. Sci. 43, 109-134.
68. Remolina SC, Hughes KA (2008) Evolution and mechanisms of long life and high fertility in queen honey bees. Age 30, 177-185.
69. Remolina SC, Hafez DM, Robinson GE, Hughes KA (2007) Senescence in the worker honey bee Apis Mellifera. J. Insect Physiol. 53, 1027-1033.
70. Robine JM, Jagger C (2005) The relationship between increasing life expectancy and healthy life expectancy. Ageing Horiz. 3, 14-21.
71. Robinson GE (1987) Regulation of honey bee age polyethism by juvenile hormone. Behav. Ecol. Sociobiol. 20, 329-338.
72. Robinson GE, Page RE, Strambi C, Strambi A (1992) Colony integration in honey bees: mechanisms of behavioral reversion. Ethology 90, 336-348.
73. Rohr MK, Lang FR (2009) Aging well together - a mini-review. Gerontology 55, 333-343.
74. Rook KS (2000) The evolution of social relationships in later adulthood. In Psychology and the Aging Revolution (Qualls SH, ed.). Washington, DC: American Psychological Association, pp. 173-191.
75. Ruan H, Wu CF (2008) Social interaction-mediated lifespan extension of Drosophila Cu/Zn superoxide dismutase mutants. Proc. Natl Acad. Sci. USA 105, 7506-7510.
76. Rueppell O, Fondrk MK, Page RE (2005) Biodemographic analysis of male honey bee mortality. Aging Cell 4, 13-19.
77. Rueppell O, Christine S, Mulcrone C, Groves L (2007a) Aging without functional senescence in honey bee workers. Curr. Biol. 17, R274-R275.
78. Rueppell O, Bachelier C, Fondrk MK, Page RE Jr (2007b) Regulation of life history determines lifespan of worker honey bees (Apis mellifera L.). Exp. Gerontol. 42, 1020-1032.
79. Scheiner R, Amdam GV (2009) Impaired tactile learning is related to social role in honeybees. J. Exp. Biol. 212, 994-1002.
80. Schultz DJ, Robinson GE (2001) Octopamine influences division of labor in honey bee colonies. J. Comp. Physiol. A. 187, 53-61.
81. Schultz DJ, Huang Z-Y, Robinson GE (1998) Effects of colony food shortage on behavioral development in honey bees. Behav. Ecol. Sociobiol. 42, 295-303.
82. Schulz DJ, Robinson GE (1999) Biogenic amines and division of labor in honey bee colonies: behaviorally related changes in the antennal lobes and age-related changes in the mushroom bodies. J. Comp. Physiol. A. 184, 481-488.
83. Seehuus SC, Krekling T, Amdam GV (2006a) Cellular senescence in the honey bee brain may be largely independent of chronological age. Exp. Gerontol. 41, 1117-1125.
84. Seehuus SC, Norberg K, Gimsa U, Krekling T, Amdam GV (2006b) Reproductive protein protects sterile honey bee workers from oxidative stress. Proc. Natl Acad. Sci. USA 103, 962-967.
85. Seeley TD (1982) Adaptive significance of the age polyethism schedule in honeybee colonies. Behav. Ecol. Sociobiol. 11, 287-293.
86. Seeley TD (1995) The Wisdom of the Hive. Cambridge: Harvard Univ Press.
87. Sekiguchi K, Sakagami SF (1966) Structure of foraging population and related problems in the honeybee, with considerations on division of labour in bee colonies. Hakkaido National Agric. Exp. Stat. Report No. 69, 1-58.
88. Smedal B, Brynem M, Kreibich CD, Amdam GV (2009) Brood pheromone suppresses physiology of extreme longevity in honeybees (Apis mellifera). J. Exp. Biol. 212, 3795-3801.
89. Sullivan JP, Jassim O, Fahrbach SE, Robinson GE (2000) Juvenile hormone paces behavioral development in the adult worker honey bee. Horm. Behav. 37, 1-14.
90. Sullivan JP, Fahrbach SE, Harrison JF, Capaldi EA, Fewell JH, Robinson GE (2003) Juvenile hormone and division of labor in honey bee colonies: effects of allatectomy on flight behavior and metabolism. J. Exp. Biol. 206, 2287-2296.
91. Svetec N, Ferveur JF (2005) Social experience and pheromonal perception can change male-male interactions in Drosophila melanogaster. J. Exp. Biol. 208, 891-898.
92. Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, Garofalo RS (2001) A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292, 107-110.
93. Tatar M, Bartke A, Antebi A (2003) The endocrine regulation of aging by insulin-like signals. Science 299, 1346-1350.
94. Tauchman SJ, Lorch JM, Orth AP, Goodman WG (2007) Effects of stress on the hemolymph juvenile hormone binding protein titers of Manduca sexta. Insect Biochem. Mol. Biol. 37, 847-854.
95. Terada Y, Garofalo CA, Sakagami SF (1975) Age-survival curves for workers of two eusocial bees (Apis mellifera and Plebeia droryana) in a subtropical climate, with notes on worker polyethism in P. droryana. J. Apic. Res. 14, 161-170.
96. Thanakwang K (2009) Social relationships influencing positive perceived health among Thai older persons: a secondary data analysis using the National Elderly Survey. Nurs. Health Sci. 11, 144-149.
97. Toivonen JM, Partridge L (2009) Endocrine regulation of aging and reproduction in Drosophila. Mol. Cell. Endocrinol. 299, 39-50.
98. Toth AL, Robinson GE (2005) Worker nutrition and division of labour in honeybees. Anim. Behav. 69, 427-435.
99. Tucker JS, Schwartz JE, Clark KM, Friedman HS (1999) Age-related changes in the associations of social network ties with mortality risk. Psychol. Aging 14, 564-571.
100. Vance JT, Williams JB, Elekonich MM, Roberts SP (2009) The effects of age and behavioral development on honey bee (Apis mellifera) flight performance. J. Exp. Biol. 212, 2604-2611.
101. Vecchi MA, Bragaglia MM, Wille H (1972) Etude sur l'hemolymphe de l'abeille adulte (Apis mellifica, L.), troisieme partie: observations ultrastructurales sur deux elements cellulaires. Bull Société Entomol. Suisse 45, 291-298.
102. Vermeulen CJ, Loeschcke V (2007) Longevity and the stress response in Drosophila. Exp. Gerontol. 42, 153-159.
103. Wagener-Hulme C, Kuehn JC, Schultz DJ, Robinson GE (1999) Biogenic amines and division of labor in honey bee colonies. J. Comp. Physiol. A. 184, 471-479.
104. Wang Y, Mutti NS, Ihle KE, Siegel A, Dolezal AG, Kaftanoglu O, Amdam GV (2010) Down-regulation of honey bee IRS gene biases behavior toward food rich in protein. PLoS Genet. 6, e1000896.
105. Weinstock GM, Robinson GE et al. (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931-949.
106. Wille H, Rutz W (1975) Beziehungen zwischen Juvenilhormontiter und Hämozyten erwachsener Sommerbienen (Apis mellifera L.). Schweiz. Landwirtsch. Forsch. 14, 339-353.
107. Winston ML (1987) The Biology of the Honey Bee. Cambridge: Harvard Univ Press.
108. Wolschin F, Munch D, Amdam GV (2009) Structural and proteomic analyses reveal regional brain differences during honeybee aging. J. Exp. Biol. 212, 4027-4032.
109. Zwaan B, Bijlsma R, Hoekstra RF (1995) Direct selection on life span in Drosophila melanogaster. Evolution 49, 649-659.