AGE

, Volume 36, Issue 1, pp 89–101 | Cite as

Reproduction, social behavior, and aging trajectories in honeybee workers

Article

Abstract

While a negative correlation between reproduction and life span is commonly observed, specialized reproductive individuals outlive their non-reproductive nestmates in all eusocial species, including the honeybee, Apis mellifera (L). The consequences of reproduction for individual life expectancy can be studied directly by comparing reproductive and non-reproductive workers. We quantified the life span consequences of reproduction in honeybee workers by removal of the queen to trigger worker reproduction. Furthermore, we observed the social behavior of large cohorts of workers under experimental and control conditions to test for associations with individual life expectancy. Worker life expectancy was moderately increased by queen removal. Queenless colonies contained a few long-lived workers, and oviposition behavior was associated with a strong reduction in mortality risk, indicating that a reproductive role confers a significant survival advantage. This finding is further substantiated by an association between brood care behavior and worker longevity that depends on the social environment. In contrast, other in-hive activities, such as fanning, trophallaxis, and allogrooming did not consistently affect worker life expectancy. The influence of foraging varied among replicates. An earlier age of transitioning from in-hive tasks to outside foraging was always associated with shorter life spans, in accordance with previous studies. In sum, our studies quantify how individual mortality is affected by particular social roles and colony environments and demonstrate interactions between the two. The exceptional, positive association between reproduction and longevity in honeybees extends to within-caste plasticity, which may be exploited for mechanistic studies.

Keywords

Biodemography Reproduction Behavioral profiles Social evolution Division of Labor Mortality dynamics 

References

  1. Aamodt RM (2009) Age-and caste-dependent decrease in expression of genes maintaining DNA and RNA quality and mitochondrial integrity in the honeybee wing muscle. Exp Gerontol 44(9):586–593. doi:10.1016/j.exger.2009.06.004 PubMedCrossRefGoogle Scholar
  2. Amdam GV, Page RE (2005) Intergenerational transfers may have decoupled physiological and chronological age in a eusocial insect. Aging Res Rev 4(3):398–408CrossRefGoogle Scholar
  3. Amdam GV, Rueppell O, Fondrk MK, Page RE, Nelson CM (2009) The nurse's load: early-life exposure to brood-rearing affects behavior and life span in honeybees (Apis mellifera). Exp Gerontol 44(6–7):467–471PubMedCentralPubMedCrossRefGoogle Scholar
  4. Backx AG, Guzman-Novoa E, Thompson GJ (2012) Factors affecting ovary activation in honeybee workers: a meta-analysis. Insect Soc 59(3):381–388. doi:10.1007/s00040-012-0230-1 CrossRefGoogle Scholar
  5. Carey JR, Papadopoulos N, Kouloussis N, Katsoyannos B, Muller HG, Wang JL, Tseng YK (2006) Age-specific and lifetime behavior patterns in Drosophila melanogaster and the Mediterranean fruit fly, Ceratitis capitata. Exp Gerontol 41(1):93–97. doi:10.1016/j.exger.2005.09.014 PubMedCentralPubMedCrossRefGoogle Scholar
  6. Corona M, Hughes KA, Weaver DB, Robinson GE (2005) Gene expression patterns associated with queen honeybee longevity. Mech Ageing Dev 126(11):1230–1238PubMedCrossRefGoogle Scholar
  7. Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y, Hughes KA, Robinson GE (2007) Vitellogenin, juvenile hormone, insulin signaling, and queen honeybee longevity. Proc Natl Acad Sci U S A 104(17):7128–7133PubMedCentralPubMedCrossRefGoogle Scholar
  8. De Loof A (2011) Longevity and aging in insects: is reproduction costly; cheap; beneficial or irrelevant? A critical evaluation of the “trade-off” concept. J Ins Physiol 57(1):1–11CrossRefGoogle Scholar
  9. de Magalhaes JP, Curado J, Church GM (2009) Meta-analysis of age-related gene expression profiles identifies common signatures of aging. Bioinformatics 25(7):875–881. doi:10.1093/bioinformatics/btp073 PubMedCrossRefGoogle Scholar
  10. Delaplane KS, Harbo JR (1987) Effect of queenlessness on worker survival, honey gain and defense behavior in honeybees. J Apic Res 26(1):37–42Google Scholar
  11. Dukas R (2008) Mortality rates of honeybees in the wild. Insect Soc 55(3):252–255. doi:10.1007/s00040-008-0995-4 CrossRefGoogle Scholar
  12. Eban-Rothschild AD, Bloch G (2008) Differences in the sleep architecture of forager and young honeybees (Apis mellifera). J Exp Biol 211(Pt 15):2408–2416. doi:10.1242/jeb.016915 PubMedCrossRefGoogle Scholar
  13. Finch CE, Tanzi RE (1997) Genetics of aging. Science 278(5337):407–411. doi:10.1126/science.278.5337.407 PubMedCrossRefGoogle Scholar
  14. Ford D (2012) Honeybees and cell lines as models of DNA methylation and aging in response to diet. Exp Gerontol. doi:10.1016/j.exger.2012.07.010 PubMedGoogle Scholar
  15. Free JB (1958) The drifting of honeybees. J Agric Sci 51:294–306CrossRefGoogle Scholar
  16. Graham AM, Munday MD, Kaftanoglu O, Page RE Jr, Amdam GV, Rueppell O (2011) Support for the reproductive ground plan hypothesis of social evolution and major QTL for ovary traits of Africanized worker honeybees (Apis mellifera L.). BMC Evol Biol 11:95PubMedCentralPubMedCrossRefGoogle Scholar
  17. Grozinger CM, Fan YL, Hoover SER, Winston ML (2007) Genome-wide analysis reveals differences in brain gene expression patterns associated with caste and reproductive status in honeybees (Apis mellifera). Mol Ecol 16(22):4837–4848PubMedCrossRefGoogle Scholar
  18. Haddad LS, Kelbert L, Hulbert AJ (2007) Extended longevity of queen honeybees compared to workers is associated with peroxidation-resistant membranes. Exp Gerontol 42(7):601–609PubMedCrossRefGoogle Scholar
  19. Hartmann A, Heinze J (2003) Lay eggs, live longer: division of labor and life span in a clonal ant species. Evolution 57(10):2424–2429PubMedGoogle Scholar
  20. Herb BR, Wolschin F, Hansen KD, Aryee MJ, Langmead B, Irizarry R, Amdam GV, Feinberg AP (2012) Reversible switching between epigenetic states in honeybee behavioral subcastes. Nat Neurosci 15(10):1371–1373PubMedCentralPubMedCrossRefGoogle Scholar
  21. Hoover SER, Keeling CI, Winston ML, Slessor KN (2003) The effect of queen pheromones on worker honeybee ovary development. Naturwissenschaften 90(10):477–480PubMedCrossRefGoogle Scholar
  22. Keller L, Genoud M (1997) Extraordinary life spans in ants: a test of evolutionary theories of ageing. Nature 389:958–960CrossRefGoogle Scholar
  23. Kenyon C (2005) The plasticity of aging: insights from long-lived mutants. Cell 120(4):449–460. doi:10.1016/j.cell.2006.02.002 PubMedCrossRefGoogle Scholar
  24. Kucharski R, Maleszka J, Foret S, Maleszka R (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science 319(5871):1827–1830PubMedCrossRefGoogle Scholar
  25. Kuszewska K, Woyciechowski M (2013) Reversion in honeybee, Apis mellifera, workers with different life expectancies. Anim Behav 85(1):247–253CrossRefGoogle Scholar
  26. Laidlaw HH, Page RE (1997) Queen rearing and bee breeding. Wicwas Press, CheshireGoogle Scholar
  27. Lattorff HMG, Moritz RFA, Crewe RM, Solignac M (2007) Control of reproductive dominance by the thelytoky gene in honeybees. Biol Lett 3(3):292–295PubMedCentralPubMedCrossRefGoogle Scholar
  28. Le Conte Y, Hefetz A (2008) Primer pheromones in social hymenoptera. Annu Rev Entomol 53:523–542PubMedCrossRefGoogle Scholar
  29. Mackay TF (2002) The nature of quantitative genetic variation for Drosophila longevity. Mech Ageing Dev 123(2–3):95–104PubMedCrossRefGoogle Scholar
  30. Makert GR, Paxton RJ, Hartfelder K (2006) Ovariole number—a predictor of differential reproductive success among worker subfamilies in queenless honeybee (Apis mellifera L.) colonies. Behav Ecol Sociobiol 60(6):815–825CrossRefGoogle Scholar
  31. Neukirch A (1982) Dependence of the life span of the honeybee (Apis mellifica) upon flight performance and energy consumption. J Comp Physiol 146:35–40Google Scholar
  32. Omholt SW, Amdam GV (2004) Epigenic regulation of aging in honeybee workers. Sci Aging Knowl Environ 26:pe28Google Scholar
  33. Page RE, Erickson EH (1988) Reproduction by worker honeybees (Apis mellifera L). Behav Ecol Sociobiol 23(2):117–126CrossRefGoogle Scholar
  34. Page RE, Metcalf RA (1984) A population investment sex ratio for the honeybee (Apis mellifera L.). Am Nat 124:680–702CrossRefGoogle Scholar
  35. Page RE, Peng Y-SC (2001) Aging and development in social insects with emphasis on the honeybee, Apis mellifera L. Exp Gerontol 36(4–6):695–711PubMedCrossRefGoogle Scholar
  36. Page RE, Robinson GE (1994) Reproductive competition in queenless honeybee colonies (Apis mellifera L). Behav Ecol Sociobiol 35(2):99–107CrossRefGoogle Scholar
  37. Remolina SC, Hughes KA (2008) Evolution and mechanisms of long life and high fertility in queen honeybees. AGE 30(2–3):177–185PubMedCrossRefGoogle Scholar
  38. Robinson GE, Page RE, Fondrk MK (1990) Intracolonial behavioral variation in worker oviposition, oophagy, and larval care in queenless honeybee colonies. Behav Ecol Sociobiol 26:315–323CrossRefGoogle Scholar
  39. Rueppell O, Amdam GV, Page RE Jr, Carey JR (2004) From genes to society: Social insects as models for research on aging. Sci Aging Knowl Environ 5:pe5Google Scholar
  40. Rueppell O, Bachelier C, Fondrk MK, Page RE Jr (2007) Regulation of life history determines life span of worker honeybees (Apis mellifera L.). Exp Gerontol 42:1020–1032PubMedCentralPubMedCrossRefGoogle Scholar
  41. Rueppell O, Linford R, Gardner P, Coleman J, Fine K (2008) Aging and demographic plasticity in response to experimental age structures in honeybees (Apis mellifera L). Behav Ecol Sociobiol 62:1621–1631PubMedCentralPubMedCrossRefGoogle Scholar
  42. Rueppell O, Kaftanouglu O, Page RE (2009) Honeybee (Apis mellifera) workers live longer in small than in large colonies. Exp Gerontol 44(6–7):447–452PubMedCentralPubMedCrossRefGoogle Scholar
  43. Rueppell O, Phaincharoen M, Kuster R, Tingek S (2011) Cross-species correlation between queen mating numbers and worker ovary sizes suggests kin conflict may influence ovary size evolution in honeybees. Naturwissenschaften 98(9):795–799. doi:10.1007/s00114-011-0822-z PubMedCentralPubMedCrossRefGoogle Scholar
  44. Smedal B, Brynem M, Kreibich CD, Amdam GV (2009) Brood pheromone suppresses physiology of extreme longevity in honeybees (Apis mellifera). J Exp Biol 212(23):3795–3801. doi:10.1242/jeb.035063 PubMedCrossRefGoogle Scholar
  45. Stout TL, Slone JD, Schneider SS (2011) Age and behavior of honeybee workers, Apis mellifera, that interact with drones. Ethology 117(5):459–468. doi:10.1111/j.1439-0310.2011.01895.x CrossRefGoogle Scholar
  46. Tezze AA, Farina WM (1999) Trophallaxis in the honeybee, Apis mellifera: the interaction between viscosity and sucrose concentration of the transferred solution. Anim Behav 57:1319–1326. doi:10.1006/anbe.1999.1110 PubMedCrossRefGoogle Scholar
  47. The “R” Development Core Team (2005) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
  48. Wilson-Rich N, Spivak M, Fefferman NH, Starks PT (2009) Genetic, individual, and group facilitation of disease resistance in insect societies. Annu Rev Entomol 54:405–423PubMedCrossRefGoogle Scholar
  49. Winston ML (1987) The biology of the honeybee. Harvard University Press, CambridgeGoogle Scholar
  50. Woyciechowski M, Kozlowski J (1998) Division of labor by division of risk according to worker life expectancy in the honeybee (Apis mellifera L.). Apidologie 29:191–205CrossRefGoogle Scholar
  51. Woyciechowski M, Moron D (2009) Life expectancy and onset of foraging in the honeybee (Apis mellifera). Insect Soc 56(2):193–201CrossRefGoogle Scholar

Copyright information

© American Aging Association 2013

Authors and Affiliations

  1. 1.Department of BiologyUniversity of North Carolina at GreensboroGreensboroUSA
  2. 2.Life Science DepartmentWinston-Salem State UniversityWinston-SalemUSA
  3. 3.Bioinformatics Graduate ProgramNorth Carolina State UniversityRaleighUSA

Personalised recommendations