The architecture of the pollen hoarding syndrome in honey bees: Implications for understanding social evolution, behavioral syndromes, and selective breeding

Apidologie

Volumn 45, Issue 3, 2014, Pages 364-374

  Rueppell, Olav ^a  

^a UNIVERSITY OF NORTH CAROLINA AT GREENSBORO   (United States)

Author keywords

Apis mellifera; artificial selection; behavioral syndrome; correlated evolution; honey bee health; ovary; pleiotropy; social behavior

Indexed keywords

CACHING; EVOLUTIONARY BIOLOGY; GENETIC MARKER; GENETIC VARIATION; HONEYBEE; LABOR DIVISION; LIFE HISTORY TRAIT; PLEIOTROPY; POLLEN; SELECTIVE BREEDING; SOCIAL BEHAVIOR;

EID: 84899565306     PISSN: 00448435     EISSN: 12979678     Source Type: Journal    
DOI: 10.1007/s13592-013-0244-3     Document Type: Review

References (90)

1. Agrawal, A.F.; Stinchcombe, J.R. (2009) How much do genetic covariances alter the rate of adaptation? Proc. R. Soc. B-Biol. Sci. 276(1659), 1183-1191
2. Amdam, G.V.; Csondes, A.; Fondrk, M.K.; Page, R.E. (2006a) Complex social behaviour derived from maternal reproductive traits. Nature 439, 76-78
3. Amdam, G.V.; Nilsen, K.A.; Norberg, K.; Fondrk, M.K.; Hartfelder, K. (2007) Variation in endocrine signaling underlies variation in social life history. Am. Nat. 170(1), 37-46
4. Amdam, G.V.; Norberg, K.; Fondrk, M.K.; Page, R.E. (2004) Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. Proc. Natl. Acad. Sci. U. S. A. 101(31), 11350-11355
5. Amdam, G.V.; Norberg, K.; Hagen, A.; Omholt, S.W. (2003) Social exploitation of vitellogenin. Proc. Natl. Acad. Sci. U. S. A. 100(4), 1799-1802
6. Amdam, G.V.; Norberg, K.; Page, R.E.; Erber, J.; Scheiner, R. (2006b) Downregulation of vitellogenin gene activity increases the gustatory responsiveness of honey bee workers (Apis mellifera). Behav. Brain Res. 169(2), 201-205
7. Amdam, G.V.; Page, R.E. (2010) The developmental genetics and physiology of honeybee societies. Anim. Behav. 79(5), 973-980
8. Amdam, G.V.; Page, R.E.; Fondrk, M.K.; Brent, C.S. (2010) Hormone response to bidirectional selection on social behavior. Evol. Dev. 12(5), 428-436
9. Arechavaleta-Velasco, M.E.; Alcala-Escamilla, K.; Robles-Rios, C.; Tsuruda, J.M.; Hunt, G.J. (2012) Fine-scale linkage mapping reveals a small set of candidate genes influencing honey bee grooming behavior in response to Varroa mites. PLoS One 7(11), e47269
10. Arias, M.C.; Sheppard, W.S. (2005) Phylogenetic relationships of honey bees (Hymenoptera:Apinae:Apini) inferred from nuclear and mitochondrial DNA sequence data. Mol. Phylogenet. Evol. 37(1), 25-35
11. Bailey, L.; Ball, B.V. (1991) Honey Bee Pathology. Academic, London
12. Behrens, D.; Huang, Q.; Gessner, C.; Rosenkranz, P.; Frey, E.; Locke, B.; Moritz, R.F.; Kraus, F.B. (2011) Three QTL in the honey bee Apis mellifera L. suppress reproduction of the parasitic mite Varroa destructor. Ecol. Evol. 1(4), 451-458
13. Bourgeois, A.L.; Rinderer, T.E. (2009) Genetic characterization of Russian Honey Bee stock selected for improved resistance to Varroa destructor. J. Econ. Entomol. 102(3), 1233-1238
14. Camazine, S. (1986) Differential reproduction of the mite, Varroa jacobsoni (Mesostigmata, Varroidae), on Africanized and European honey bees (Hymenoptera, Apidae). Ann. Entomol. Soc. Am. 79(5), 801-803
15. Conner, J.K. (2003) Artificial selection: a powerful tool for ecologists. Ecology 84(7), 1650-1660
16. Delph, L.F.; Arntz, A.M.; Scotti-Saintagne, C.; Scotti, I. (2010) The genomic architecture of sexual dimorphism in the dioecious plant Silene latifolia. Evolution 64(10), 2873-2886
17. Dixon, L.R.; McQuage, M.R.; Lonon, E.J.; Buehler, D.; Seck, O.; Rueppell, O. (2012) Pleiotropy of segregating genetic variants that affect honey bee worker life expectancy. Exp. Gerontol. 47(8), 631-637
18. Dreller, C.; Page, R.E.; Fondrk, M.K. (1999) Regulation of pollen foraging in honeybee colonies: effects of young brood, stored pollen, and empty space. Behav. Ecol. Sociobiol. 45, 227-233
19. Dreller, C.; Tarpy, D.R. (2000) Perception of the pollen need by foragers in a honeybee colony. Anim. Behav. 59(1), 91-96
20. Engel, M.S. (1998) Fossil honey bees and evolution in the genus Apis (Hymenoptera: Apidae). Apidologie 29(3), 265-281
21. Fewell, J.H.; Page, R.E. (1993) Genotypic variation in foraging responses to environmental stimuli by honey bees, Apis mellifera. Experientia 49(12), 1106-1112
22. Fewell, J.H.; Winston, M.L. (1992) Colony state and regulation of pollen foraging in the honey-bee, Apis mellifera L. Behav. Ecol. Sociobiol. 30, 387-393
23. Fewell, J.H.; Winston, M.L. (1996) Regulation of nectar collection in relation to honey storage levels by honey bees, Apis mellifera. Behav. Ecol. 7(3), 286-291
24. Gadagkar, R. (1997) The evolution of caste polymorphism in social insects: genetic release followed by diversifying evolution. J. Genet. 76(3), 167-179
25. Goode, K.; Huber, Z.; Mesce, K.A.; Spivak, M. (2006) Hygienic behavior of the honey bee (Apis mellifera) is independent of sucrose responsiveness and foraging ontogeny. Horm. Behav. 49(3), 391-397
26. Graham, A.M.; Munday, M.D.; Kaftanoglu, O.; Page, R.E.; Amdam, G.V.; Rueppell, O. (2011) Support for the reproductive ground plan hypothesis of social evolution and major QTL for ovary traits of Africanized worker honey bees (Apis mellifera L.). BMC Evol. Biol. 11, 95
27. Harris, J.W. (2007) Bees with Varroa sensitive hygiene preferentially remove mite infested pupae aged < = five days post capping. J. Apic. Res. 46(3), 134-139
28. Hellmich, R.L.; Kulincevic, J.M.; Rothenbuhler, W.C. (1985) Selection for high and low pollen-hoarding honey bees. J. Hered. 76(3), 155-158
29. Holloway, B.; Sylvester, H.A.; Bourgeois, L.; Rinderer, T.E. (2012) Association of single nucleotide polymorphisms to resistance to chalkbrood in Apis mellifera. J. Apic. Res. 51(2), 154-163
30. Huang, Q.; Kryger, P.; Le Conte, Y.; Moritz, R.F. (2012) Survival and immune response of drones of a Nosemosis tolerant honey bee strain towards N. ceranae infections. J. Invertebr. Pathol. 109(3), 297-302
31. Humann, F.C.; Hartfelder, K. (2011) Representational Difference Analysis (RDA) reveals differential expression of conserved as well as novel genes during caste-specific development of the honey bee (Apis mellifera L.) ovary. Insect Biochem. Mol. 41(8), 602-612
32. Humphries, M.A.; Fondrk, M.K.; Page, R.E. (2005) Locomotion and the pollen hoarding behavioral syndrome of the honeybee (Apis mellifera L.). J. Comp. Physiol. A. 191(7), 669-674
33. Humphries, M.A.; Muller, U.; Fondrk, M.K.; Page, R.E. (2003) PKA and PKC content in the honey bee central brain differs in genotypic strains with distinct foraging behavior. J. Comp. Physiol. A. 189(7), 555-562
34. Hunt, G.J.; Amdam, G.V.; Schlipalius, D.; Emore, C.; Sardesai, N.; et al. (2007) Behavioral genomics of honeybee foraging and nest defense. Naturwissenschaften 94(4), 247-267
35. Hunt, G.J.; Page Jr.; R.E.; Fondrk, M.K.; Dullum, C.J. (1995) Major quantitative trait loci affecting honey bee foraging behavior. Genetics 141, 1537-1545
36. Ihle, K.E.; Page, R.E.; Frederick, K.; Fondrk, M.K.; Amdam, G.V. (2010) Genotype effect on regulation of behaviour by vitellogenin supports reproductive origin of honeybee foraging bias. Anim. Behav. 79(5), 1001-1006
37. Jandt, J.M.; Bengston, S. Pinter-Wollman, N. Pruitt, J.N.; Raine, N.E.; Dornhaus, A. Sih A. (2013) Behavioural syndromes and social insects: personality at multiple levels. Biol. Rev. Online. In press.
38. Kulincevic, J.M.; Rothenbuhler, W.C. (1975) Selection for resistance and susceptibility to hairless-black syndrome in the honeybee. J. Invertebr. Pathol. 25(3), 289-295
39. Laidlaw, H.H.; Page, R.E. (1997) Queen rearing and bee breeding. Wicwas Press, Cheshire
40. Lande, R. (1982) A quantitative genetic theory of life history evolution. Ecology 63(3), 607-615
41. Lande, R. (1984) The genetic correlation between characters maintained by selection, linkage and inbreeding. Genet. Res. 44(3), 309-320
42. Lapidge, K.L.; Oldroyd, B.P.; Spivak, M. (2002) Seven suggestive quantitative trait loci influence hygienic behavior of honey bees. Naturwissenschaften 89(12), 565-568
43. Le Conte, Y.; Alaux, C.; Martin, J.F.; Harbo, J.R.; Harris, J.W.; Dantec, C.; Severac, D.; Cros-Arteil, S.; Navajas, M. (2011) Social immunity in honeybees (Apis mellifera): transcriptome analysis of varroa-hygienic behaviour. Insect Mol. Biol. 20(3), 399-408
44. Linksvayer, T.A.; Fondrk, M.K.; Page, R.E. (2009a) Honeybee social regulatory networks are shaped by colony-level selection. Am. Nat. 173(3), E99-E107
45. Linksvayer, T.A.; Rueppell, O.; Siegel, A.; Kaftanoglu, O.; Page, R.E.; Amdam, G.V. (2009b) The genetic basis of transgressive ovary size in honey bee workers. Genetics 183, 693-707
46. Mutti, N.S.; Dolezal, A.G.; Wolschin, F.; Mutti, J.S.; Gill, K.S.; Amdam, G.V. (2011) IRS and TOR nutrient-signaling pathways act via juvenile hormone to influence honey bee caste fate. J. Exp. Biol. 214(23), 3977-3984
47. Nelson, C.M.; Ihle, K.E.; Fondrk, M.K.; Page, R.E.; Amdam, G.V. (2007) The gene vitellogenin has multiple coordinating effects on social organization. Plos Biol. 5(3), e62
48. Nilsen, K.A.; Ihle, K.E.; Frederick, K.; Fondrk, M.K.; Smedal, B.; Hartfelder, K.; Amdam, G.V. (2011) Insulin-like peptide genes in honey bee fat body respond differently to manipulation of social behavioral physiology. J. Exp. Biol. 214(9), 1488-1497
49. O'Hagan, S.J.; Knowles, D.B.; Kell (2012) Exploiting genomic knowledge in optimising molecular breeding programmes: algorithms from evolutionary computing. PLoS One 7(11). In press.
50. Oxley, P.R.; Spivak, M.; Oldroyd, B.P. (2010) Six quantitative trait loci influence task thresholds for hygienic behaviour in honeybees (Apis mellifera). Mol. Ecol. 19(7), 1452-1461
51. Page, R.E.; Amdam, G.V. (2007) The making of a social insect: developmental architectures of social design. Bioessays 29, 334-343
52. Page, R.E.; Erber, J. (2002) Levels of behavioral organization and the evolution of division of labor. Naturwissenschaften 89, 91-106
53. Page, R.E.; Fondrk, M.K. (1995) The effects of colony level selection on the social organization of honey bee (Apis mellifera L) colonies - colony level components of pollen hoarding. Behav. Ecol. Sociobiol. 36(2), 135-144
54. Page, R.E.; Fondrk, M.K.; Hunt, G.J.; Guzman-Novoa, E.; Humphries, M.A.; Nguyen, K.; Greene, A.S. (2000) Genetic dissection of honeybee (Apis mellifera L.) foraging behavior. J Hered. 91(6), 474-479
55. Page, R.E.; Fondrk, M.K.; Rueppell, O. (2012a) Complex pleiotropy characterizes the pollen hoarding syndrome in honey bees (Apis mellifera L.). Behav. Ecol. Sociobiol. 66(11), 1459-1466
56. Page, R.E.; Rueppell, O.; Amdam, G.V. (2012b) Genetics of reproduction and regulation of honeybee (Apis mellifera L.) social behavior. Annu. Rev. Genet. 46, 97-119
57. Palmer, K.A.; Oldroyd, B.P. (2003) Evidence for intra-colonial genetic variance in resistance to American foulbrood of honey bees (Apis mellifera): further support for the parasite/pathogen hypothesis for the evolution of polyandry. Naturwissenschaften 90(6), 265-268
58. Pankiw, T. (2003) Directional change in a suite of foraging behaviors in tropical and temperate evolved honey bees (Apis mellifera L.). Behav. Ecol. Sociobiol. 54(5), 458-464
59. Pankiw, T.; Page, R.E. (2001) Genotype and colony environment affect honeybee (Apis mellifera L.) development and foraging behavior. Behav. Ecol. Sociobiol. 51, 87-94
60. Pianka, E.R. (1970) On r- and K-selection. Am. Nat. 104(940), 592-597
61. Price, T.; Langen, T. (1992) Evolution of correlated characters. Trends Ecol. Evol. 7(9), 307-310
62. Rinderer, T.E.; Harris, J.W.; Hunt, G.J.; de Gusman, L.I. (2010) Breeding for resistance to Varroa destructor in North America. Apidologie 41(3), 409-424
63. Roff, D.A. (2011) Genomic insights into life history evolution. In: Flatt, T.; Heyland, A. (eds.) Mechanisms of Life History Evolution, pp. 11-25. Oxford University Press, Oxford
64. Rueppell, O. (2009) Characterization of quantitative trait loci for the age of first foraging in honey bee workers. Behav. Genet. 39, 541-553
65. Rueppell, O.; Bachelier, C.; Fondrk, M.K.; Page, R.E. (2007) Regulation of life history determines lifespan of worker honey bees (Apis mellifera L.). Exp. Gerontol. 42, 1020-1032
66. Rueppell, O.; Chandra, S.B.C.; Pankiw, T.; Fondrk, M.K.; Beye, M.; Hunt, G.J.; Page, R.E. (2006a) The genetic architecture of sucrose responsiveness in the honey bee (Apis mellifera L.). Genetics 172, 243-251
67. Rueppell, O.; Fondrk, M.K.; Page, R.E. (2006b) Male maturation response to selection of the pollen-hoarding syndrome in honey bees (Apis mellifera L.). Anim. Behav. 71, 227-234
68. Rueppell, O.; Hunggims, E.; Tingek, S. (2008) Association between larger ovaries and pollen foraging in queenless Apis cerana workers supports the reproductive ground-plan hypothesis of social evolution. J. Insect Behav. 21, 317-321
69. Rueppell, O.; Metheny, J.D.; Linksvayer, T.A.; Fondrk, M.K.; Page, R.E.; Amdam, G.V. (2011) Genetic architecture of ovary size and asymmetry in European honeybee workers. Heredity 106, 894-903
70. Rueppell, O.; Pankiw, T.; Nielsen, D.I.; Fondrk, M.K.; Beye, M.; Page, R.E. (2004) The genetic architecture of the behavioral ontogeny of foraging in honey bee workers. Genetics 167, 1767-1779
71. Rüppell, O.; Pankiw, T.; Nielson, D.I.; Fondrk, M.K.; Beye, M.; Page, R.E. (2004) Pleiotropy, epistasis and new QTL: the genetic architecture of honey bee foraging behavior. J. Hered. 95, 481-491
72. Scheiner, R.; Page, R.E.; Erber, J. (2001) The effects of genotype, foraging role, and sucrose responsiveness on the tactile learning performance of honey bees (Apis mellifera L.). Neurobiol. Learn. Mem. 76(2), 138-150
73. Schmid-Hempel, P. (1998) Parasites in social insects. Princeton University Press, Princeton
74. Sih, A.; Bell, A.; Johnson, J.C. (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol. Evol. 19, 372-378
75. Spivak, M.; Gilliam, M. (1998) Hygienic behaviour of honey bees and its application for control of brood diseases and Varroa Part I. Hygienic behaviour and resistance to American foulbrood. Bee World 79(3), 124-134. 169-186
76. Spivak, M.; Reuter, G.S.; Lee, K.; Ranum, B. (2009) The future of the MN hygienic stock of bees is in good hands! Am. Bee J. 149(10), 965-967
77. Stearns, S.C. (1989) Trade-offs in life-history evolution. Funct. Ecol. 3(3), 259-268
78. Toth, A.L.; Robinson, G.E. (2007) Evo-devo and the evolution of social behavior. Trends Genet. 23(7), 334-341
79. Tsuruda, J.M.; Harris, J.W.; Bourgeois, L.; Danka, R.G.; Hunt, G.J. (2012) High-resolution linkage analyses to identify genes that influence Varroa sensitive hygiene behavior in honey bees. PLoS One 7(11)
80. Tsuruda, J.M.; Page, R.E. (2009) The effects of foraging role and genotype on light and sucrose responsiveness in honey bees (Apis mellifera L.). Behav Brain Res. 205(1), 132-137
81. vanEngelsdorp, D.; Evans, J.D.; Saegerman, C.; Mullin, C.; Haubruge, E.; et al. (2009) Colony collapse disorder: a descriptive study. PLoS ONE 4(8), e6481
82. vanEngelsdorp, D.; Meixner, M.D. (2010) A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J. Invertebr. Pathol. 103, S80-S95
83. vanEngelsdorp, D.; Tarpy, D.R.; Lengerich, E.J.; Pettis, J.S. (2013) Idiopathic brood disease syndrome and queen events as precursors of colony mortality in migratory beekeeping operations in the eastern United States. Prev. Vet. Med. 108(2-3), 225-233
84. Waddington, K.D.; Nelson, M.; Page, R.E. (1998) Effects of pollen quality and genotype on the dance of foraging honey bees. Anim. Behav. 56, 35-39
85. Wang, Y.; Amdam, G.V.; Rueppell, O.; Wallrichs, M.A.; Fondrk, M.K.; Kaftanoglu, O.; Page, R.E. (2009) PDK1 and HR46 gene homologs tie social behavior to ovary signals. PLoS ONE 4(4), e4899
86. Wang, Y.; Kocher, S.D.; Linksvayer, T.A.; Grozinger, C.M.; Page, R.E.; Amdam, G.V. (2012) Regulation of behaviorally associated gene networks in worker honey bee ovaries. J. Exp. Biol. 215(1), 124-134
87. Wang, Y.; Mutti, N.S.; Ihle, K.E.; Siegel, A.; Dolezal, A.G.; Kaftanoglu, O.; Amdam, G.V. (2010) Down-regulation of honey bee IRS gene biases behavior toward food rich in protein. PLoS Genet. 6(4), e1000896
88. Whitfield, C.W.; Ben-Shahar, Y.; Brillet, C.; Leoncini, I.; Crauser, D.; Le Conte, Y.; Rodriguez-Zas, S.; Robinson, G.E. (2006) Genomic dissection of behavioral maturation in the honey bee. Proc. Natl. Acad. Sci. U. S. A. 103(44), 16068-16075
89. Williams, G.C. (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution 11, 398-411
90. Zsolt Garamszegi, L.; Marko, G.; Herczeg, G. (2012) A meta-analysis of correlated behaviours with implications for behavioural syndromes: mean effect size, publication bias, phylogenetic effects and the role of mediator variables. Evol. Ecol. 26(5), 1213-1235