PDK1 and HR46 gene homologs tie social behavior to ovary signals

PLoS ONE

Volumn 4, Issue 4, 2009, Pages

  Wang, Ying ^a   Amdam, Gro V ^a,b   Rueppell, Olav ^c   Wallrichs, Megan A ^c   Fondrk, M Kim ^a   Kaftanoglu, Osman ^a   Page Jr , Robert E ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

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

Author keywords

[No Author keywords available]

Indexed keywords

HORMONE RECEPTOR; HORMONE RECEPTOR LIKE 46; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FORAGING BEHAVIOR; GENE EXPRESSION; GENE MAPPING; GENETIC ASSOCIATION; GENETIC LINKAGE; HONEYBEE; NONHUMAN; ORGAN SIZE; OVARY; PHENOTYPE; QUANTITATIVE TRAIT LOCUS; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; ANIMAL; BEE; FEMALE; GENE; GENETICS; METABOLISM; PHYSIOLOGY; REPRODUCTION;

APIS MELLIFERA; APOIDEA; HEXAPODA;

ANIMALS; BEES; FEMALE; GENES, INSECT; OVARY; QUANTITATIVE TRAIT LOCI; REPRODUCTION; SOCIAL BEHAVIOR;

EID: 64549115923     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004899     Document Type: Article

References (61)

1. Maynard Smith J, Szathmáry E (1995) The Major Transitions in Evolution. New York: Oxford University Press.
2. Winston ML (1987) The Biology of the Honey Bee. Cambridge, Massachusetts: Harvard Univ. Press. pp 235-250.
3. Lindauer M (1953) Division of labour in the honey bee colony. Bee World 34: 63-73.
4. Amdam GV, Norberg K, Fondrk MK, Page RE (2004) Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. Proc Natl Acad Sci USA 101: 11350-11355.
5. West-Eberhard MJ (1987) Flexible Strategy and Social Evolution. Itô Y, Brown JL, Kikkawa J, eds. Animal Societies: Theories and Fact. Tokyo: Japan Sci. Soc. Press. pp 35-51.
6. West-Eberhard MJ (1996) Wasp societies as microcosms for the study of development and evolution. In Natural History and Evolution of Paper Wasp. Turillazzi S, West-Eberhard MJ, eds. New York: Oxford University Press. pp 290-317.
7. Amdam GV, Csondes A, Fondrk MK, Page RE (2006) Complex social behavior derived from maternal reproductive traits. Nature 439: 76-78.
8. Tsuruda JM, Amdam GV, Page RE Jr (2008) Sensory response system of social behavior tied to female reproductive traits. PLoS ONE 3: e3397.
9. Page RE, Fondrk 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: 135-144.
10. Barchuk AR, Bitondi MM, Simões ZL (2002) Effects of juvenile hormone and ecdysone on the timing of vitellogenin appearance in hemolymph of queen and worker pupae of Apis mellifera. J Insect Sci 2: 1.
11. Nelson CM, Ihle KE, Fondrk MK, Page RE, Amdam GV (2007) The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biol 5: e62.
12. Page RE, Scheiner R, Erber J, Amdam GV (2007) The development and evolution of division of labor and foraging specialization in a social insect (Apis mellifera L.). Curr Topics Devel Biol 74: 253-286.
13. Page RE, Amdam GV (2007) The making of a social insect: developmental architectures of social design. Bioessays 29: 334-343.
14. Hunt GJ, Page RE, Fondrk MK, Dullum CJ (1995) Major quantitative trait loci affecting honey bee foraging behavior. Genetics 141: 1537-1545.
15. Page RE, Fondrk MK, Hunt GJ, Guzman-Novoa E, Humphries MA, et al. (2000) Genetic dissection of honey bee (Apis mellifera L.) foraging behavior. J Hered 91: 474-479.
16. Rueppell O, Pankiw T, Nielsen DI, Fondrk MK, Beye M, et al. (2004) The genetic architecture of the behavioral ontogeny of foraging in honey bee workers. Genetics 167: 1767-1779.
17. Rueppell O, Pankiw T, Page RE (2004) Pleiotropy, epistasis and new QTL: The genetic architecture of honey bee foraging behavior. J Hered 95: 481-491.
18. Lam G, Hall BL, Bender M, Thummel CS (1999) DHR3 is required for the prepupal- pupal transition and differentiation of adult structures during Drosophila metamorphosis. Dev Biol 212: 204-216.
19. Takemoto K, Kuranaga E, Tonoki A, Nagai T, Miyawaki A, et al. (2007) Local initiation of caspase activation in Drosophila salivary gland programmed cell death in vivo. Proc Natl Acad Sci USA 104: 13367-13372.
20. Calderone NW, Page RE (1992) Effects of interactions among genotypically diverse nestmates on task specialization by foraging honey bees (Apis mellifera). Behav Ecol Sociobiol 30: 219-226.
21. Hunt GJ, Amdam GV, Schlipalius D, Emore C, Sardesai N, et al. (2007) Behavioral genomics of honey bee foraging and nest defense. Naturwissenschaften 94: 247-267.
22. Daborn PJ, Yen JL, Bogwit MR, Le Goff G, Feil E, et al. (2002) A single p450 allele associated with insecticide resistance in Drosophila. Science 297: 2253-2256.
23. Thellin O, Zorzi W, Lakaye B, De Borman B, Coumans B, et al. (1999) Housekeeping genes as internal standards: use and limits. J Biotechnol 75: 291-295.
24. Labuhn M, Brack C (1997) Age-related changes in the mRNA expression of actin isoforms in Drosophila melanogaster. Gerontology 43: 261-267.
25. Page RE, Linksvayer TA, Amdam GV (2009) Social life from solitary regulatory networks: a paradigm for insect sociality. In: Gadau J, Fewell J, eds. Organization of insect societies from genome to sociocomplexity. Cambridge: Harvard University Press. pp 357-376.
26. Oldroyd BP, Beekman M (2008) Effects of selection for honey bee worker reproduction on foraging traits. PLoS Biol 6: e56.
27. Pankiw T, Page RE Jr (2001) Genotype and colony environment affect honeybee (Apis mellifera L.) development and foraging behavior. Behav Ecol Sociobiol 51: 87-94.
28. Amdam GV, Omholt SW (2003) The hive bee to forager transition in honeybee colonies: the double repressor hypothesis. J Theor Biol 223: 451-64.
29. Pankiw T, Page RE (2003) Effect of pheromones, hormones, and handling on sucrose response thresholds of honey bees (Apis mellifera L.). J Comp Physiol A189: 675-684.
30. Humphries MA, Muller U, Fondrk MK, Page RE (2003) PKA and PKC content in the honey bee central brain differs in genotypic strains with distinct foraging behavior. J Comp Physiol 189: 555-562.
31. Rueppell O, Chandra SBC, Pankiw T, Fondrk MK, Beye M, et al. (2006) The genetic architecture of sucrose responsiveness in the honey bee (Apis mellifera L.). Genetics 172: 243-251.
32. 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.
33. Richard DS, Rybczynski R, Wilson TG, Wang Y, Wayne ML, et al. (2005) Insulin signaling is necessary for vitellogenesis in Drosophila melanogaster independent of the roles of juvenile hormone and ecdysteroids: female sterility of the chico1 insulin signaling mutation is autonomous to the ovary. J Insect Physiol 51: 455-464.
34. Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, et al. (2001) A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292: 107-110.
35. Drummond-Barbosa D, Spradling AC (2004) Alpha-endosulfine, a potential regulator of insulin secretion, is required for adult tissue growth control in Drosophila. Dev Biol 266: 310-321.
36. Wu Q, Brown MR (2006) Signaling and function of insulin-like peptides in insects. Annu Rev Entomol 51: 1-24.
37. Rintelen F, Stocker H, Thomas G, Hafen E (2001) PDK1 regulates growth through Akt1 and S6K in Drosophila. Proc Natl Acad Sci USA 98: 5020-15025.
38. Orgogozo V, Broman KW, Stern DL (2006) High-resolution quantitative trait locus mapping reveals sign epistasis controlling ovariole number between two Drosophila species. Genetics 173: 197-205.
39. Tomioka M, Adachi T, Suzuki H, Kunitomo H, Schafer WR, et al. (2006) The insulin/PI3-kinase pathway regulates salt chemotaxis learning in Caenorhabditis elegans. Neuron 51: 613-625.
40. Amdam GV, Ihle KE, Page RE (2008) Regulation of worker honey bee ( Apis mellifera) life histories by vitellogenin. Hormones, Brain and Behavior. Fahrbach S, ed. San Diego CA: Elsevier.
41. Schmidt-Capella IC, Hartfelder K (1998) Juvenile hormone effect on DNA synthesis and apoptosis in caste-specific differentiation of the larval honey bee (Apis mellifera L.) ovary. J Insect Physiol 44: 385-391.
42. Namiki T, Niwa R, Sakudoh T, Shirai K, Takeuchi H, et al. (2005) Cytochrome P450 CYP307A1/Spook: a regulator for ecdysone synthesis in insects. Biochem Biophys Res Commun 337: 367-374.
43. Hartfelder K, Engels W (1998) Social insect polymorphism: hormonal regulation of plasticity in development and reproduction in the honey bee. Curr Top Dev Biol 40: 45-77.
44. Kethidi DR, Xi Z, Palli SR (2005) Developmental and hormonal regulation of juvenile hormone esterase gene in Drosophila melanogaster. J Insect Physiol 51: 393-400.
45. Kapitskaya MZ, Li C, Miura K, Segraves W, Raikhel AS (2000) Expression of the early-late gene encoding the nuclear receptor HR3 suggests its involvement in regulating the vitellogenic response to ecdysone in the adult mosquito. Mol Cell Endocrinol 60: 25-37.
46. Robinson GE, Strambi C, Strambi A, Feldlaufer MF (1991) Comparison of juvenile hormone and ecdysteroid haemolymph titres in adult worker and queen honey bees (Apis mellifera). J Insect Physiol 37: 929-935.
47. Sullivan AA, Thummel CS (2003) Temporal profiles of nuclear receptor gene expression reveal coordinate transcriptional responses during Drosophila development. Mol Endocrinol 17: 2125-2137.
48. Lam GT, Jiang C, Thummel CS (1997) Coordination of larval and prepupal gene expression by the DHR3 orphan receptor during Drosophila metamorphosis. Development 124: 1757-1769.
49. Jiang C, Lamblin AF, Steller H, Thummel CS (2000) A steroid-triggered transcriptional hierarchy controls salivary gland cell death during Drosophila metamorphosis. Mol Cell 5: 445-455.
50. Lee CY, Simon CR, Woodard CT, Baehrecke EH (2002) Genetic mechanism for the stage- and tissue-specific regulation of steroid triggered programmed cell death in Drosophila. Dev Biol 252: 138-148.
51. Schmidt Capella IC, Hartfelder K (2002) Juvenile-hormone-dependent interaction of actin and spectrin is crucial for polymorphic differentiation of the larval honey bee ovary. Cell Tissue Res 307: 265-272.
52. Faulkes CG, Abbott DH (1991) Social control of reproduction in breeding and non-breeding male naked mole-rats (Heterocephalus glaber). J Reprod Fertil 93: 427-435.
53. Brothertona PNM, Clutton-Brocka TH, O'Riainb MJ, Gaynorb D, Sharpeb L, et al. (2001) Offspring food allocation by parents and helpers in a cooperative mammal. Behav Ecol 5: 590-599.
54. DeborahSmitha, ThomasMeierb, EliGeffenc, DavidMechd, John W, et al. (1997) Is incest common in gray wolf packs? Behav Ecol 8: 384-391.
55. Nicole B, Zina HB, Rui FO, Adelino VC, Michael T (2008) Hormonal control of brood care and social status in a cichlid fish with brood care helpers. Physiol Behav 94: 349-358.
56. Goodson JL (2005) The Vertebrate Social Behavior Network: Evolutionary Themes and Variations. Horm Behav 48: 11-22.
57. Solignac M, Mougel F, Vautrin D, Monnerot M, Cornuet JM (2007) A third-generation microsatellite-based linkage map of the honey bee, Apis mellifera, and its comparison with the sequence-based physical map. Genome Biol 8: R66.
58. Whitfield CW, Ben-Shahar Y, Brillet C, Leoncini I, Crauser D, et al. (2006) Thrice out of Africa: Ancient and recent expansions of the honey bee, Apis mellifera. Science 314: 642-645.
59. Ragoussis J, Elvidge GP, Kaur K, Colella S (2006) Matrix-assisted laser desorption/ionisation, time-of-flight mass spectrometry in genomics research. PLoS Genetics 2: 920-929.
60. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18: 233-234.
61. Schug MD, Regulski EE, Pearce A, Smith SG (2004) Isolation and characterization of dinucleotide repeat microsatellites in Drosophila ananassae. Genet Res 83: 19-29.