Individual variation in pheromone response correlates with reproductive traits and brain gene expression in worker honey bees

PLoS ONE

Volumn 5, Issue 2, 2010, Pages

  Kocher, Sarah D ^a,b   Ayroles, Julien F ^a   Stone, Eric A ^a   Grozinger, Christina M ^a,b  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHEROMONE; TRANSCRIPTION FACTOR SNF; INSECT PROTEIN;

ARTICLE; BRAIN; FEMALE; GENE EXPRESSION; GENETIC VARIABILITY; HONEYBEE; MALE; NONHUMAN; ORGANISM COLONY; QUEEN (INSECT); REPRODUCTION; SOCIAL BEHAVIOR; TASK PERFORMANCE; WORKER (INSECT); ANIMAL; BEE; CLUSTER ANALYSIS; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORK; GENETICS; METABOLISM; OVARY; PHYSIOLOGY; SEXUAL BEHAVIOR;

APIS MELLIFERA;

ANIMALS; BEES; BRAIN; CLUSTER ANALYSIS; FEMALE; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; INSECT PROTEINS; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OVARY; PHEROMONES; REPRODUCTION; SEXUAL BEHAVIOR, ANIMAL; SOCIAL BEHAVIOR;

EID: 77949349089     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009116     Document Type: Article

References (72)

1. Robinson GE, Fernald RD, Clayton DF (2008) Genes and Social Behavior. Science 322: 896-900.
2. Nussey DH, Wilson AJ, Brommer JE (2007) The evolutionary ecology of individual phenotypic plasticity in wild populations. Journal of Evolutionary Biology 20: 831-844.
3. Oleksiak MF, Churchill GA, Crawford DL (2002) Variation in gene expression within and among natural populations. Nature Genetics 32: 261-266.
4. Whitehead A, Crawford DL (2006) Variation within and among species in gene expression: raw material for evolution. Molecular Ecology 15: 1197-1211.
5. Phelps SM, Young LJ (2003) Extraordinary diversity in vasopressin (V1a) receptor distributions among wild prairie voles (Microtus ochrogaster): patterns of variation and covariation. J Comp Neurol 466: 564-576.
6. Cummings ME, Larkins-Ford J, Reilly CR, Wong RY, Ramsey M, et al. (2008) Sexual and social stimuli elicit rapid and contrasting genomic responses. Proc Biol Sci 275: 393-402.
7. Renn SCP, Aubin-Horth N, Hofmann HA (2008) Fish and chips: functional genomics of social plasticity in an African cichlid fish. Journal of Experimental Biology 211: 3041-3056.
8. Beshers SN, Fewell JH (2001) Models of division of labor in social insects. Annual Review of Entomology 46: 413-440.
9. Barchuk AR, Cristino AS, Kucharski R, Costa LF, Simoes ZL, et al. (2007) Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. BMC Dev Biol 7: 70.
10. Kucharski R, Maleszka J, Foret S, Maleszka R (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science 319: 1827-1830.
11. Evans JD, Wheeler DE (2001) Expression profiles during honeybee caste determination. Genome Biol 2: RESEARCH0001.
12. Whitfield CW, Ben-Shahar Y, Brillet C, Leoncini I, Crauser D, et al. (2006) Genomic dissection of behavioral maturation in the honey bee. Proc Natl Acad Sci U S A 103: 16068-16075.
13. Whitfield CW, Cziko AM, Robinson GE (2003) Gene expression profiles in the brain predict behavior in individual honey bees. Science 302: 296-299.
14. Grozinger CM, Fan Y, Hoover SE, Winston ML (2007) Genome-wide analysis reveals differences in brain gene expression patterns associated with caste and reproductive status in honey bees (Apis mellifera). Mol Ecol 16: 4837-4848.
15. Grozinger CM, Sharabash NM, Whitfield CW, Robinson GE (2003) Pheromone-mediated gene expression in the honey bee brain. Proc Natl Acad Sci U S A 100 Suppl 2: 14519-14525.
16. Bloch G, Wheeler DE, Robinson GE (2002) Endocrine influences on the organization of insect societies. In: Pfaff D, ed. Hormones, Brain, and Behavior. San Diego: Academic Press. pp 195-236.
17. Huang Z-Y, Robinson GE, Borst D (1994) Physiological correlates of division of labor among similarly aged honey bees. Journal of Comparative Physiology a-Neuroethology Sensory Neural and Behavioral Physiology 174: 731-739.
18. Robinson GE, Ben-Shahar Y (2002) Social behavior and comparative genomics: new genes or new gene regulation? Genes Brain Behav 1: 197-203.
19. Schulz DJ, Robinson GE (2001) Octopamine influences division of labor in honey bee colonies. J Comp Physiol [A] 187: 53-61.
20. Page RE, Amdam GV (2007) The making of a social insect: developmental architectures of social design. Bioessays 29: 334-343.
21. Allsopp M, Calis J, Boot W (2003) Differential feeding of worker larvae affects caste characters in the Cape honeybee, Apis mellifera capensis. Behav Ecol Sociobiol 54: 555-561.
22. Calis J, Boot WJ, Allsopp MH, Beekman M (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.
23. Hoover SE, Higo HA, Winston ML (2006) Worker honey bee ovary development: seasonal variation and the influence of larval and adult nutrition. J Comp Physiol [B] 176: 55-63.
24. Hunt GJ, Amdam GV, Schlipalius D, Emore C, Sardesai N, et al. (2007) Behavioral genomics of honeybee foraging and nest defense. Naturwissenschaften 94: 247-267.
25. Hunt GJ, Guzman-Novoa E, Fondrk MK, Page RE (1998) Quantitative trait loci for honey bee stinging behavior and body size. Genetics 148: 1203-1213.
26. Oldroyd BP, Fewell JH (2007) Genetic diversity promotes homeostasis in insect colonies. Trends in Ecology & Evolution 22: 408-413.
27. Oldroyd BP, Fewell JH (2008) Large fitness benefits from polyandry in the honey bee, Apis mellifera. Trends Ecol Evol 23: 59-60.
28. Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317: 362-364.
29. Seeley TD, Tarpy DR (2007) Queen promiscuity lowers disease within honeybee colonies. Proc Biol Sci 274: 67-72.
30. Tarpy DR (2003) Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proceedings of the Royal Society of London Series B-Biological Sciences 270: 99-103.
31. Tarpy DR, Seeley TD (2006) Lower disease infections in honeybee (Apis mellifera) colonies headed by polyandrous vs monandrous queens. Naturwissenschaften 93: 195-199.
32. Le Conte Y, Arnold G, Trouiller T, Masson C, Chappe B (1990) Identification of a brood pheromone in honeybees. Naturwissenschaften 77: 334-336.
33. Leoncini I, Le Conte Y, Costagliola G, Plettner E, Toth AL, et al. (2004) Regulation of behavioral maturation by a primer pheromone produced by adult worker honey bees. Proceedings of the National Academy of Science, USA 101: 17559-17564.
34. Blum MG, Fales HM, Tucker KW, Collins AM (1978) Chemistry of the sting apparatus of the worker honey bee. J Apic Res 17: 218-221.
35. Pickett JA, Williams IH, Martin AP, Smith MC (1980) Nasonov pheromone of the honey bee, Apis mellifera L. (Hymenoptera: Apidae). Journal of Chemical Ecology 6: 1561-1573.
36. Le Conte Y, Hefetz A (2008) Primer pheromones in social hymenoptera. Annu Rev Entomol 53: 523-542.
37. Slessor KN, Winston ML, Le Conte Y (2005) Pheromone communication in the honeybee (Apis mellifera L.). Journal of Chemical Ecology 31: 2731-2745.
38. Slessor KN, Kaminski LA, King GGS, Borden JH, Winston ML (1988) Semiochemical Basis of the Retinue Response to Queen Honey Bees. Nature 332: 354-356.
39. Cardé RT, Baker TC (1984) Sexual Communication with Pheromones. In: Bell WJ, Cardé RT, eds. Chemical Ecology of Insects London: Chapman & Hall. pp 355-383.
40. Pankiw T, Winston ML, Slessor KN (1994) Variation in worker response to honey bee (Apis mellifera L.) queen mandibular pheromone (Hymenoptera: Apidae). Journal of Insect Behavior 7: 1-15.
41. Pankiw T, Winston ML, Fondrk MK, Slessor KN (2000) Selection on worker honeybee responses to queen pheromone (Apis mellifera L.). Naturwissenschaften 87: 487-490.
42. 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. Behavioral Ecology and Sociobiology 60: 815-825.
43. Hoover SE, Keeling CI, Winston ML, Slessor KN (2003) The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 90: 477-480.
44. Amdam GV, Csondes A, Fondrk MK, Page RE (2006) Complex social behaviour derived from maternal reproductive traits. Nature 439: 76-78.
45. Wolfinger RD, Gibson G, Wolfinger ED, Bennett L, Hamadeh H, et al. (2001) Assessing gene significance from cDNA microarray expression data via mixed models. Journal of Computational Biology 8: 625-637.
46. Ayroles JF, Gibson G (2006) Analysis of variance of microarray data. DNA Microarrays, Part B: Databases and Statistics 411: 214-+.
47. Kocher SD, Richard FJ, Tarpy DR, Grozinger CM (2008) Genomic analysis of post-mating changes in the honey bee queen (Apis mellifera). BMC Genomics 9: 232.
48. Benjamini Y, Hochberg Y (1995) Controlling the False Discovery Rate: a Practical and Powerful Approach to Multiple Testing. J R Statist Soc B 57: 289-300.
49. Suzuki R, Shimodaira H (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22: 1540-1542.
50. Ayroles J, Carbone M, Stone E, Jordan K, Lyman R, et al. (2009) Systems genetics of complex traits in Drosophila melanogaster. Nature Genetics 41: 299-307.
51. Stone EA, Ayroles JF (2009) Modulated Modularity Clustering as an Exploratory Tool for Functional Genomic Inference. PLoS Genet 5: e1000479.
52. Dennis G, Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3.
53. Wang J, Ross KG, Keller L (2008) Genome-wide expression patterns and the genetic architecture of a fundamental social trait. PLoS Genet 4: e1000127.
54. Jones JC, Myerscough MR, Graham S, Oldroyd BP (2004) Honey Bee Nest Thermoregulation: Diversity Promotes Stability. Science 305: 402-404.
55. Winston ML (1991) The Biology of the Honey Bee. Cambridge: Harvard University Press.
56. Pankiw T, Huang ZY, Winston ML, Robinson GE (1998) Queen mandibular gland pheromone influences worker honey bee (Apis mellifera L.) foraging ontogeny and juvenile hormone titers. Journal of Insect Physiology 44: 685-692.
57. Melathopoulos AP, Winston ML, Pettis JS, Pankiw T (1996) Effect of queen mandibular pheromone on initiation and maintenance of queen cells in the honey bee (Apis mellifera L). Canadian Entomologist 128: 263-272.
58. Page RE, Robinson GE (1994) Reproductive competition in queenless honey bee colonies (Apis mellifera L.). Behavioral Ecology and Sociobiology 35: 99-107.
59. Page RE, Erickson EH (1988) Reproduction by worker honey bees (Apis mellifera L.). Behavioral Ecology and Sociobiology 23: 117-126.
60. Robinson GE, Page RE, Fondrk MK (1990) Intracolonial behavioral variation in worker oviposition, oophagy, and larval care in queenless honey-bee colonies. Behavioral Ecology and Sociobiology 26: 315.
61. Martin C, Oldroyd B, Beekman M (2004) Differential reproductive success among subfamilies in queenless honey bee colonies (Apis mellifera L.). Behavioral Ecology and Sociobiology 56: 42-49.
62. Moritz RFA, Crewe RM, Hepburn HR (2002) Queen avoidance and mandibular gland secretion of honeybee workers (Apis mellifera L.). Insectes Sociaux 49: 86-91.
63. Pankiw T (1997) Queen rearing by high and low queen mandibular pheromone responding worker honey bees (Apis mellifera L.). Canadian Entomologist 129: 679-690.
64. Cnaani J, Robinson GE, Bloch G, Borst D, Hefetz A (2000) The effect of queen-worker conflict on caste determination in the bumblebee Bombus terrestris. Behavioral Ecology and Sociobiology 47: 346-352.
65. Wirtz P, Beetsma J (1972) Induction of caste differentiation in the honeybee (Apis mellifera) by juvenile hormone. Ent exp & app. pp 517-520.
66. Linksvayer TA, Fondrk MK, Page RE (2009) Honeybee social regulatory networks are shaped by colony-level selection. American Naturalist 173: E99-E107.
67. Wanner KW, Nichols AS, Walden KK, Brockmann A, Luetje CW, et al. (2007) A honey bee odorant receptor for the queen substance 9-oxo-2-decenoic acid. Proc Natl Acad Sci U S A 104: 14383-14388.
68. Pham-Delegue MH, Trouiller J, Caillaud CM, Roger B, Masson C (1993) Effect of queen pheromone on worker bees of different ages: behavioural and eletrophysiological responses. Apidologie 24: 267-281.
69. Grozinger CM, Robinson GE (2007) Endocrine modulation of a pheromone-responsive gene in the honey bee brain. Journal of Comparative Physiology a-Neuroethology Sensory Neural and Behavioral Physiology 193: 461-470.
70. Schulz DJ, Sullivan JP, Robinson GE (2002) Juvenile hormone and octopamine in the regulation of division of labor in honey bee colonies. Hormones and Behavior 42: 222-231.
71. Kocher SD, Richard FJ, Tarpy DR, Grozinger CM (2009) Queen reproductive state modulates queen pheromone production and queen-worker interactions in honey bees. Behavioral Ecology 20: 1007-1014.
72. Richard FJ, Tarpy DR, Grozinger CM (2007) Effects of insemination quantity on honey bee queen physiology. PLoS ONE 2: e980.