Honeybee social regulatory networks are shaped by colony-level selection

American Naturalist

Volumn 173, Issue 3, 2009, Pages

  Linksvayer, Timothy A ^a,b   Fondrk, Michael K ^a   Page Jr , Robert E ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Developmental program; Genotype by genotype epistasis; Indirect genetic effects; Interacting phenotypes; Levels of selection; Social evolution

Indexed keywords

DICOTYLEDON; EVOLUTIONARY BIOLOGY; FORAGING BEHAVIOR; GENE EXPRESSION; HOMEOSTASIS; HONEYBEE; LARVA; NATURAL SELECTION; PHYSIOLOGY; POLLEN; SOCIAL INSECT; SOCIAL NETWORK; WORKER CASTE;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BEE; BODY SIZE; FEMALE; GENETIC SELECTION; GENETICS; GENOTYPE; HISTOLOGY; MALE; OVARY; PHYSIOLOGY; POPULATION DYNAMICS; SOCIAL BEHAVIOR; ANATOMY AND HISTOLOGY;

ANIMALS; BEES; BEHAVIOR, ANIMAL; BODY SIZE; FEMALE; GENOTYPE; MALE; OVARY; POPULATION DYNAMICS; SELECTION, GENETIC; SOCIAL BEHAVIOR;

APIS MELLIFERA; HEXAPODA;

EID: 61849153985     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/596527     Document Type: Article

References (81)

1. Agrawal, A. F., E. D. Brodie III, and J. Brown. 2001. Parent-offspring coadaptation and the dual genetic control of maternal care. Science 292:1710-1712.
2. Allsopp, M. H., J. N. M. Calis, and W. J. Boot. 2003. Differential feeding of worker larvae affects caste characters in the Cape honeybee, Apis mellifera capensis. Behavioral Ecology and Sociobiology 54:555-561.
3. Amdam, G. V., and R. E. Page Jr. 2008. Oldroyd and Beekman do not test ground plan hypothesis that explains origins of social behavior. PLoS Biology 6:e56r2248.
4. Amdam, G. V., K. Norberg, M. K. Fondrk, and R. E. Page Jr. 2004. Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. Proceedings of the National Academy of Sciences of the USA 101:11350-11355.
5. Amdam, G. V., A. Csondes, M. K. Fondrk, and R. E. Page Jr. 2006. Complex social behaviour derived from maternal reproductive traits. Nature 439:76-78.
6. Amdam, G. V., K. A. Nilsen, K. Norberg, M. K. Fondrk, and K. Hartfelder. 2007. Variation in endocrine signaling underlies variation in social life history. American Naturalist 170:37-46.
7. Beekman, M., and B. P. Oldroyd. 2003. Effects of cross-feeding anarchistic and wild type honey bees: anarchistic workers are not queen-like. Naturwissenschaften 90:189-192.
8. Beekman, M., J. N. M. Calis, and W. J. Boot. 2000. Parasitic honeybees get royal treatment. Nature 404:723.
9. Bienefeld, K., and F. Pirchner. 1990. Heritabilities for several colony traits in the honeybee (Apis mellifera carnica). Apidologie 21:175-183.
10. -. 1991. Genetic correlations among several colony characters in the honey bee (Hymenoptera, Apidae) taking queen and worker effects into account. Annals of the Entomological Society of America 84:324-331.
11. Bijma, P., W. A. Muir, and J. A. M. Van Arendonk. 2007. Multilevel selection 1: quantitative genetics of inheritance and response to selection. Genetics 175:277-288.
12. Calderone, N. W., and R. E. Page. 1992. Effects of interactions among genotypically diverse nestmates on task specialization by foraging honey bees (Apis mellifera). Behavioral Ecology and Sociobiology 30:219-226.
13. Calis, J. N. M., W. J. Boot, M. H. Allsopp, and M. Beekman. 2002. Getting more than a fair share: nutrition of worker larvae related to social parasitism in the Cape honey bee Apis mellifera capensis. Apidologie 33:193-202.
14. Cheverud, J. M., and A. J. Moore. 1994. Quantitative genetics and the role of the environment provided by relatives in behavioral evolution. Pages 67-100 in C. R. B. Boake, ed. Quantitative genetic studies of behavioral evolution. University of Chicago Press, Chicago.
15. Cui, Y. H., G. Casella, and R. L. Wu. 2004. Mapping quantitative trait loci interactions from the maternal and offspring genomes. Genetics 167:1017-1026.
16. Evans, J. D., and D. E. Wheeler. 1999. Differential gene expression between developing queens and workers in the honey bee, Apis mellifera. Proceedings of the National Academy of Sciences of the USA 96:5575-5580.
17. -. 2001. Gene expression and the evolution of insect polyphenisms. Bioessays 23:62-68.
18. Fewell, J. H. 2003. Social insect networks. Science 301:1867-1870.
19. Fewell, J. H., and R. E. Page. 2000. Colony-level selection effects on individual and colony foraging task performance in honeybees, Apis mellifera L. Behavioral Ecology and Sociobiology 48:173-181.
20. Fewell, J. H., and M. L. Winston. 1992. Colony state and regulation of pollen foraging in the honey bee, Apis mellifera L. Behavioral Ecology and Sociobiology 30:387-393.
21. Gjuvsland, A. B., B. J. Hayes, S. W. Omholt, and O. Carlborg. 2007. Statistical epistasis is a generic feature of gene regulatory networks. Genetics 175:411-420.
22. Goodnight, C. J., and L. Stevens. 1997. Experimental studies of group selection: what do they tell us about group selection in nature? American Naturalist 150(suppl.):S59-S79.
23. Griffing, B. 1981. A theory of natural selection incorporating interaction among individuals. II. Use of related groups. Journal of Theoretical Biology 89:659-677.
24. Guzmán-Novoa, E., and R. E. Page. 1994. Genetic dominance and worker interactions affect honeybee colony defense. Behavioral Ecology 5:91-97.
25. Hellmich, R. L., J. M. Kulincevic, and W. C. Rothenbuhler. 1985. Selection for high and low pollen-hoarding honey bees. Journal of Heredity 76:155-158.
26. Hölldobler, B., and E. O. Wilson. 1990. The ants. Harvard University Press, Cambridge, MA.
27. Honey Bee Genome Sequencing Consortioum. 2006. Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931-949.
28. Hunt, G. J., E. Guzman-Novoa, J. L. Uribe-Rubio, and D. Prieto-Merlos. 2003. Genotype-environment interactions in honeybee guarding behaviour. Animal Behaviour 66:459-467.
29. Hunt, G. J., G. V. Amdam, D. Schlipalius, C. Emore, N. Sardesai, C. E. Williams, O. Rueppell, et al. 2007. Behavioral genomics of honeybee foraging and nest defense. Naturwissenschaften 94:247-267.
30. Hunt, J., and L. W. Simmons. 2002. The genetics of maternal care: direct and indirect genetic effects on phenotype in the dung beetle Onthophagus taurus. Proceedings of the National Academy of Sciences of the USA 99:6828-6832.
31. Kang, M. S., M. G. Balzarini, and J. L. L. Guerra. 2004. Genotype-by-environment interaction. Pages 69-94 in A. M. Saxton, ed. Genetic analysis of complex traits using SAS. SAS Institute, Cary, NC.
32. Keller, L., and K. G. Ross. 1995. Gene by environment interaction: effects of a single gene and social environment on reproductive phenotypes of fire ant queens. Functional Ecology 9:667-676.
33. Kirkpatrick, M., and R. Lande. 1989. The evolution of maternal characters. Evolution 43:485-503.
34. Kölliker, M., E. D. Brodie III, and A. J. Moore. 2005. The coadaptation of parental supply and offspring demand. American Naturalist 166:506-516.
35. Le Conte, Y., L. Sreng, and S. H. Poitout. 1995. Brood pheromone can modulate the feeding behavior of Apis mellifera workers (Hymenoptera, Apidae). Journal of Economic Entomology 88:798-804.
36. Le Conte, Y., J. M. Becard, G. Costagliola, G. de Vaublanc, M. El Maataoui, D. Crauser, E. Plettner, and K. N. Slessor. 2006. Larval salivary glands are a source of primer and releaser pheromone in honey bee (Apis mellifera L.). Naturwissenschaften 93:237-241.
37. Linksvayer, T. A. 2006. Direct, maternal, and sibsocial genetic effects on individual and colony traits in an ant. Evolution 60:2552-2561.
38. -. 2007. Ant species differences determined by epistasis between brood and worker genomes. PLoS One 2:e994.
39. Linksvayer, T. A., and M. J. Wade. 2005. The evolutionary origin and elaboration of sociality in the aculeate Hymenoptera: maternal effects, sib-social effects, and heterochrony. Quarterly Review of Biology 80:317-336.
40. Lock, J. E., P. T. Smiseth, and A. J. Moore. 2004. Selection, inheritance, and the evolution of parent-offspring interactions. American Naturalist 164:13-24.
41. Lumsden, C. J. 1982. The social regulation of physical caste: the super-organism revived. Journal of Theoretical Biology 95:749-781.
42. Lynch, M., and B. Walsh. 1998. Genetics and analysis of quantitative traits. Sinauer, Sunderland, MA.
43. Makert, G. R., R. J. Paxton, and K. Hartfelder. 2006. Ovariole number: a predictor of differential reproductive success among worker subfamilies in queenless honeybee (Apis mellifera L.) colonies. Behavioral Ecology and Sociobiology 60:815-825.
44. Maynard Smith, J., and E. Szathmáry. 1995. The major transitions in evolution. Oxford University Press, New York.
45. McAdam, A. G., S. Boutin, D. Reale, and D. Berteaux. 2002. Maternal effects and the potential for evolution in a natural population of animals. Evolution 56:846-851.
46. Moore, A. J., and T. Pizzari. 2005. Quantitative genetic models of sexual conflict based on interacting phenotypes. American Naturalist 165(suppl.):S88-S97.
47. Moore, A. J., E. D. Brodie III, and J. B. Wolf. 1997. Interacting phenotypes and the evolutionary process. I. Direct and indirect genetic effects of social interactions. Evolution 51:1352-1362.
48. Moore, A. J., K. F. Haynes, R. F. Preziosi, and P. J. Moore. 2002. The evolution of interacting phenotypes: Genetics and evolution of social dominance. American Naturalist 160(suppl.):S186-S197.
49. Moritz, R. F. A., and E. E. Southwick. 1987. Phenotype interactions in group behavior of honey bee workers (Apis mellifera L.). Behavioral Ecology and Sociobiology 21:53-57.
50. Moritz, R. F. A., E. E. Southwick, and J. R. Harbo. 1987. Maternal and pre-eclosional factors affecting alarm behavior in adult honey bees (Apis mellifera L). Insectes Sociaux 34:298-307.
51. Mutic, J. J., and J. B. Wolf. 2007. Indirect genetic effects from ecological interactions in Arabidopsis thaliana. Molecular Ecology 16:2371-2381.
52. Oldroyd, B. P., and M. Beekman. 2008. Effects of selection for honey bee worker reproduction on foraging traits. PLoS Biology 6:e56.
53. Oldroyd, B. P., and G. J. Thompson. 2007. Behavioural genetics of the honey bee Apis mellifera. Advances in Insect Physiology 33:1-49.
54. Oldroyd, B. P., T. E. Rinderer, and S. M. Buco. 1991. Heritability of morphological characters used to distinguish European and Africanized honeybees. Theoretical and Applied Genetics 82:499-504.
55. Orr, H. A. 2001. The genetics of species differences. Trends in Ecology & Evolution 16:343-350.
56. Oster, G. F., and E. O. Wilson. 1976. Caste and ecology in the social insects. Princeton University Press, Princeton, NJ.
57. Owen, R. E. 1989. The genetics of colony level selection. Pages 31-60 in M. D. Breed and R. E. Page, eds. Genetics and social evolution. Westview, Boulder, CO.
58. Page, R. E., and M. K. Fondrk. 1995. 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 36:135-144.
59. Page, R. E., R. Scheiner, J. Erber, and G. V. Amdam. 2006. The development and evolution of division of labor and foraging specialization in a social insect (Apis mellifera L.). Current Topics in Developmental Biology 74:253-286.
60. Pankiw, T., and R. E. Page. 2001. Genotype and colony environment affect honeybee (Apis mellifera L.) development and foraging behavior. Behavioral Ecology and Sociobiology 51:87-94.
61. Pankiw, T., R. E. Page, and M. K. Fondrk. 1998. Brood pheromone stimulates pollen foraging in honey bees (Apis mellifera). Behavioral Ecology and Sociobiology 44:193-198.
62. Pankiw, T., D. R. Tarpy, and R. E. Page. 2002. Genotype and rearing environment affect honeybee perception and foraging behaviour. Animal Behaviour 64:663-672.
63. Rauter, C. M., and A. J. Moore. 2002. Evolutionary importance of parental care performance, food resources, and direct and indirect genetic effects in a burying beetle. Journal of Evolutionary Biology 15:407-417.
64. Rinderer, T. E., H. A. Sylvester, A. M. Collins, and D. Pesante. 1986. Identification of Africanized and European honey bees: effects of nurse genotype and comb size. Bulletin of the Entomological Society of America 32:150-152.
65. Robinson, G. E., C. M. Grozinger, and C. W. Whitfield. 2005. Sociogenomics: social life in molecular terms. Nature Reviews Genetics 6:257-270.
66. Ross, K. G., and L. Keller. 2002. Experimental conversion of colony social organization by manipulation of worker genotype composition in fire ants (Solenopsis invicta). Behavioral Ecology and Sociobiology 51:287-295.
67. Rüppell, O., J. Heinze, and B. Hölldobler. 2001. Complex determination of queen body size in the queen size dimorphic ant Leptothorax rugatulus (Formicidae: Hymenoptera). Heredity 87:33-40.
68. Seeley, T. D. 1995. The wisdom of the hive: the social physiology of honey bee colonies. Harvard University Press, Cambridge, MA.
69. -. 1997. Honey bee colonies are group-level adaptive units. American Naturalist 150(suppl.):S22-S41.
70. Slessor, K. N., M. L. Winston, and Y. Le Conte. 2005. Pheromone communication in the honeybee (Apis mellifera L.). Journal of Chemical Ecology 31:2731-2745.
71. Tarpy, D. R., D. C. Gilley, and T. D. Seeley. 2004. Levels of selection in a social insect: a review of conflict and cooperation during honey bee (Apis mellifera) queen replacement. Behavioral Ecology and Sociobiology 55:513-523.
72. Tsuruda, J., G. V. Amdam, and R. E. Page Jr. 2008. Sensory response system of social behavior tied to female reproductive traits. PLoS One 3:e3997.
73. Wade, M. J. 1998. The evolutionary genetics of maternal effects. Pages 5-21 in T. A. Mousseau and C. W. Fox, eds. Maternal effects as adaptations. Oxford University Press, New York.
74. Whitlock, M. C., P. C. Phillips, F. B. G. Moore, and S. J. Tonsor. 1995. Multiple fitness peaks and epistasis. Annual Review of Ecology and Systematics 26:601-629.
75. Wilson, E. O. 1971. The insect societies. Harvard University Press, Cambridge, MA.
76. -. 1985. The principles of caste evolution. Fortschritte der Zoologie 31:307-324.
77. Wolf, J. B. 2000a. Gene interactions from maternal effects. Evolution 54:1882-1898.
78. -. 2000b. Indirect genetic effects and gene interactions. Pages 158-176 in J. B. Wolf, E. D. Brodie III, and M. J. Wade, eds. Epistasis and the evolutionary process. Oxford University Press, New York.
79. -. 2003. Genetic architecture and evolutionary constraint when the environment contains genes. Proceedings of the National Academy of Sciences of the USA 100:4655-4660.
80. Wolf, J. B., and E. D. Brodie III. 1998. The coadaptation of parental and offspring characters. Evolution 52:299-308.
81. Wolf, J. B., T. T. Vaughn, L. S. Pletscher, and J. M. Cheverud. 2002. Contribution of maternal effect QTL to genetic architecture of early growth in mice. Heredity 89:300-310.