Abstract
Division of labour is a fundamental property of any social system. The specialization of different individuals in different tasks increases the overall work performance and efficiency. Specialization is thought to be the very foundation of the success of human societies but also in complex colonies of social insects. In human societies an advanced form of division of labour, especially since the industrialisation, is shift work, where individuals perform the same task but in subsequent cohorts in time. Although social insects can measure and are aware of time, shift work has not been documented in colonies of social insects so far. We observed foragers of two honeybee (Apis mellifera) colonies (approximately 140 workers each) and genotyped them with microsatellite DNA markers. We determined paternity and assigned them to the various subfamilies in the colony to test whether there is genetic variance for shift work in foraging honeybees. We could show that the patriline identity of the foragers had a significant effect on foraging either in the morning or evening. Individual foragers differed in their preference for the “early” or “late” shift, and shift work indeed existed in the colony.
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References
Boomsma JJ, Ratnieks FLW (1996) Paternity in eusocial hymenoptera. Phil Trans R Soc Lond B 351:947–975
Calderone NW, Page RE (1988) Genotypic variability in age polyethism and task specialisation in the honey bee, Apis mellifera (Hymenoptera: Apidae). Behav Ecol Sociobiol 22:17–25
Estoup A, Solignac M, Cornuet JM (1994) Precise assessment of the number of patrilines and of genetic relatedness in honeybee colonies. Proc R Soc Lond B 258:1–7
Frumhoff PC, Baker J (1988) A genetic component to division of labour within honey bee colonies. Nature 333:358–361
Hölldobler B, Wilson EO (1991) The ants. Springer, Berlin
Hughes WOH, Sumner S, van Borm S, Boomsma JJ (2003) Worker caste polymorphism has a genetic basis in Acromyrmex leaf-cutting ants. Proc Natl Acad Sci USA 100:9394–9397. doi:10.1073/pnas.1633701100
Hughes WOH, Oldroyd BP, Beekman M, Ratnieks FLW (2008) Ancestral monogamy shows kin selection is key to the evolution of eusociality. Sci 320:1213–1216
Hur YM, Bouchard TJ Jr, Lykken DT (1998) Genetic and environmental influence on morningness–eveningness. Personal Individ Diff 14:806–814. doi:10.1016/S0191-8869(98)00089-0
Jaffe R, Kronauer DJC, Kraus FB, Boomsma JJ, Moritz RFA (2007) Worker caste determination in the army ant Eciton burchellii. Biol Lett 3:513–516. doi:10.1098/rsbl.2007.0257
Jones J, Myerscough M, Graham S, Oldroyd BP (2004) Honey bee nest thermoregulation: diversity promotes stability. Sci 305:402–404
Kerkhof GA (1985) Inter-individual differences in the human circadian system: a review. Biol Psychol 20:83–112
Kraus FB, Neumann P, Moritz RFA (2005) Genetic variance of mating frequency in the honeybee (Apis mellifera L.). Insect Soc 52:1–5
Kronauer DJC, Johnson RA, Boomsma JJB (2007) The evolution of multiple mating in army ants. Evol 61:413–422. doi:10.1111/j.1558-5646.2007.00040.x
Lattorff HMG, Moritz RFA, Crewe RM, Solingnac M (2007) Control of reproductive dominance by the thelytoky gene in honeybees. Biol Lett 3:292–295
Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Sci 317:362–364
Merrow M, Spoelstra K, Roenneberg T (2005) The circadian cycle: daily rhythms from behaviour to genes. EMBO Report 6:930–935
Moffett MW (1987) Division of labour and diet in the extremely polymorphic ant Pheidologeton diversus. Nat Geograph Res 3:282–304
Moore D (2001) Honey bee circadian clocks: behavioral control from individual workers to whole-colony rhythms. J Insect Physiol 47:843–857
Moore D, Rankin MA (1983) Diurnal changes in the accuracy of the honeybee foraging rhythm. Biol Bull 164:472–482
Moore D, Giray T, Robinson GE (1996) Genotypic differences in the ontogeny of circadian rhythmicity in honey bees. Soc for Neurosci Abstr 22:151
Moore D, Angel JE, Cheeseman IM, Fahrbach SE, Robinson GE (1998) Timekeeping in the honey bee colony: intergration of circadian rhythms and division of labour. Behav Ecol Sociobiol 43:147–160
Moritz RFA, Sakofski F (1991) The role of the queen in circadian rhythms of honeybees (Apis mellifera L.). Behav Ecol Sociobiol 29:361–365
Moritz RFA, Lattorff HMG, Neumann P, Kraus FB, Radloff SE, Hepburn HR (2005) Rare royal families in honeybees, Apis mellifera. Naturwissenschaften 92:488–491. doi:10.1007/s00114-005-0025-6
Pamilo P (1993) Polyandry and allele frequency differences between the sexes in the ant Formica aquilonia. Heredity 70:472–480
Pati AK, Chandrawanshi A, Reinberg A (2001) Shift work: consequences and management. Curr Sci 8:32–52
Ridley M (1996) The origins of virtue–human instincts and the evolution of cooperation. Penguin Books, London
Robinson GE, Page RE (1988) Genetic determination of guarding and undertaking in honey-bee colonies. Nature 333:356–358
Robinson GE, Page RE (1989) Genetic determination of nectar foraging, pollen foraging, and nest-site scouting in honey bee colonies. Behav Ecol Sociobiol 24:317–323
Shaibi T, Lattorff HMG, Moritz RFA (2008) A microsatellite DNA toolkit for studying population structure in Apis mellifera. Mol Ecol Res 8:1034–1036
Sharma VK, Lone SR, Goel A, Chandrashekaran MK (2004a) Circadian consequences of social organization in the ant species Camponotus compressus. Naturwissenschaften 91:386–390
Sharma VK, Lone SR, Mathew D, Goel A, Chandrashekaran MK (2004b) Possible evidence for shift work schedules in the media workers of the ant Species Camponotus compressus. Chronobiol Internat 21:297–308
Smith CR, Toth AL, Suarez AV, Robinson GE (2008) Genetic and genomic analyses of the division of labour in insect societies. Nature Rev Genet 9:735–748. doi:10.1038/nrg2429
Sokal RR, Rohlf FJ (1994) Biometry: the principles and practice of statistics in biological research. WH Freeman, New York
Spangler HG (1972) Daily activity rhythms of individual worker and drone honey bees. An Entomol Soc Am 66:449–451
Uribe-Rubio JL, Guzman-Novoa E, Vasquez-Pelaez CG, Hunt GJ (2008) Genotype, task specialisation, and nest environment influence the stinging response thresholds of individual Africanized and European honeybees to electrical stimulation. Behav Genet 38:93–100. doi:10.1007/s10519-007-9177-9
Vink JM, Groot AS, Kerkhof GA, Boomsma DI (2001) Genetic analysis of morningness and eveningness. Chronobiol Internat 18:809–822
Walsh PS, Metzger DA, Higuchi R (1991) Chelex100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513
Wheeler DE (1991) The developmental basis of worker caste polymorphism in ants. Am Nat 138:1218–1238
Wilson EO (1971) The insect societies. Belknap Press of Harvard University Press, Cambridge
Wittmann M, Dinich J, Merrow M, Roenneberg T (2006) Social jetlag: misalignment of biological and social time. Chronobiol Internat 23:497–509. doi:10.1080/07420520500545979
Acknowledgments
We would like to thank Petra Leibe for assistance in the laboratory and Ray WK Moritz for helping with the collection of data and assistance in the field.
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Edited by Yong-Kyu Kim.
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Bernhard Kraus, F., Gerecke, E. & Moritz, R.F.A. Shift Work has a Genetic Basis in Honeybee Pollen Foragers (Apis mellifera L.). Behav Genet 41, 323–328 (2011). https://doi.org/10.1007/s10519-010-9382-9
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DOI: https://doi.org/10.1007/s10519-010-9382-9