The transcription factor Krüppel homolog 1 is linked to hormone mediated social organization in bees

BMC Evolutionary Biology

Volumn 10, Issue 1, 2010, Pages

  Shpigler, Hagai ^a   Patch, Harland M ^a,b,c   Cohen, Mira ^a   Fan, Yongliang ^a,b,d   Grozinger, Christina M ^a,b,c   Bloch, Guy ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d SYNGENTA BIOTECHNOLOGY INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BEE; BEHAVIORAL ECOLOGY; BRAIN; COLONY STRUCTURE; ENDOCRINE SYSTEM; GENE EXPRESSION; GENETIC STRUCTURE; HORMONE; JUVENILE; MOLECULAR ECOLOGY; PHEROMONE; PHYLOGENETICS; PROTEIN; REPRODUCTIVE POTENTIAL;

APIS MELLIFERA; APOIDEA; BOMBUS (GENUS); HEXAPODA; HYMENOPTERA;

INSECT PROTEIN; JUVENILE HORMONE; KRUPPEL LIKE FACTOR;

ANIMAL; ARTICLE; BEE; BRAIN; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; SOCIAL BEHAVIOR;

ANIMALS; BEES; BRAIN; INSECT PROTEINS; JUVENILE HORMONES; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MOLECULAR SEQUENCE DATA; SOCIAL BEHAVIOR;

EID: 77951588434     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-10-120     Document Type: Article

References (72)

1. Sociogenomics: social life in molecular terms. GE Robinson CM Grozinger CW Whitfield, Nat Rev Genet 2005 6 4 257 270 10.1038/nrg1575 15761469
2. The Insect Societies. EO Wilson, Cambridge, MA: The Belkap Press of Harvard University Press 1971
3. The Social Behavior of Bees. CD Michener, Cambridge: Harvard University Press 1974
4. The evolution of communication and the communication of evolution: The case of the honey bee queen pheromone. R Gadagkar, Orientation and Communication in Arthropods Basel/Switzerland: Birkhauser Verlag, Lehrer M, 1997 375 395
5. The role of queen pheromones in social insects: queen control or queen signal? L Keller P Nonacs, Anim Beh 1993 45 787 794 10.1006/anbe.1993.1092
6. Genes and social behavior. GE Robinson RD Fernald DF Clayton, Science 2008 322 5903 896 900 10.1126/science.1159277 18988841
7. Serotonin and aggression: insights gained from a lobster model system and speculations on the role of amine neurons in a complex behavior. EA Kravitz, J Comp Physiol [A] 2000 186 3 221 238 10.1007/s003590050423 10757238
8. 6. Social dominance and serotonin receptor genes in crayfish. DH Edwards N Spitzer, Curr Top Dev Biol 2006 74 177 199 10.1016/S0070-2153(06)74006-6 16860668
9. Somatostatin and somatostatin receptor gene expression in dominant and subordinate males of an African cichlid fish. BC Trainor HA Hofmann, Behav Brain Res 2007 179 2 314 320 10.1016/j.bbr.2007.02.014 17374406
10. Social regulation of gonadotropin-releasing hormone. SA White T Nguyen RD Fernald, J Exp Biol 2002 205 Pt 17 2567 2581 12151363
11. Genetic regulation of colony social organization in fire ants: an integrative overview. D Gotzek KG Ross, Q Rev Biol 2007 82 3 201 226 10.1086/519965 17937246
12. Primer pheromones in social hymenoptera. Y Le Conte A Hefetz, Annu Rev Entomol 2008 53 523 542 10.1146/annurev.ento.52.110405.091434 17877458
13. Queen mandibular gland pheromone influences worker honey bee (Apis mellifera L.) foraging ontogeny and juvenile hormone titers. T Pankiw Z Huang ML Winston GE Robinson, J Insect Physiol 1998 44 7-8 685 692 10.1016/S0022- 1910(98)00040-7 12769952
14. Queen influence on worker reproduction in bumblebees (Bombus terrestris) colonies. C Alaux P Jaisson A Hefetz, Insect Sociaux 2004 51 287 293
15. Effect of the queen on worker reproduction and new queen production in the bumble bee Bombus terrestris. C Lopez-Vaamonde RM Brown ER Lucas JJM Pereboom WC Jordan AFG Bourke, 2007 38 171 180
16. Regulation of worker reproduction in bumblebees (Bombus terrestris): workers eavesdrop on a queen signal. C Alaux P Jaisson A Hefetz, Behav Ecol Sociobiol 2006 60 439 446 10.1007/s00265-006-0184-2
17. Reevaluation of the role of mandibular glands in regulation of reproduction in bumblebee colonies. G Bloch A Hefetz, J Chem Ecol 1999 25 4 881 896 10.1023/A:1020805103379 (Pubitemid 29215692)
18. Fertility signals in the bumblebee Bombus terrestris (Hymenoptera: Apidae). A Sramkova C Schulz R Twele W Francke M Ayasse, Naturwissenschaften 2008 95 6 515 522 10.1007/s00114-008-0353-4 18320160
19. Endocrine influences on the organization of insect societies. G Bloch DE Wheeler GE Robinson, Hormones, Brain and Behavior. Non-mammalian hormone-behavior systems, Pfaff D, 2002 II 195 235
20. Primer effect of queen pheromone on juvenile hormone biosynthesis in adult worker honey bees. HH Kaatz H Hildebrandt W Engels, J Comp Physiol [B] 1992 162 588 592
21. Physiological correlates of division of labor among similarly aged honey bees. Z-Y Huang GE Robinson DW Brost, J Comp Physiol [A] 1994 174 731 739 8014920
22. Juvenile hormone paces behavioral development in the adult worker honey bee. JP Sullivan SE Fahrbach GE Robinson, Horm Behav 2000 37 1 1 14 10.1006/hbeh.1999.1552 10712853
23. Juvenile hormone titers, juvenile hormone biosynthesis, ovarian development and social environment in Bombus terrestris. G Bloch DW Borst Z Huang GE Robinson J Cnaani A Hefetz, J Insect Physiol 2000 46 1 47 57 10.1016/S0022-1910(99)00101-8 12770258
24. Effects of social conditions on juvenile hormone-mediated reproductive development in Bombus terrestris workers. G Bloch DW Borst Z-Y Huang GE Robinson A Hefetz, Physiological Entomology 1996 21 257 267 10.1111/j.1365-3032.1996. tb00863.x
25. Juvenile hormone control of oogenesis in bumblebee workers, Bombus terrestris. PF Roseler, J Insect Physiol 1977 23 985 992 10.1016/0022-1910(77) 90126-3
26. Factors influencing dominance behaviour in queenless bumblebee workers (Bombus terrestris). A Van Doorn, Physiological Entomology 1989 14 2 211 221 10.1111/j.1365-3032.1989.tb00954.x
27. Juvenile hormone does not affect division of labor in Bumble bee colonies (Hymenoptera: Apidae). SA Cameron GE Robinson, Ann Entomol Soc Am 1990 83 626 631
28. Investigations into the regulation of dominance behavior and the division of labor in bumblebee colonies (Bombus terrestris). A Van Doorn, Netherland Journal of Zoology 1987 37 3-4 255 276
29. Endocrine influences on the organization of insect societies. G Bloch H Shpigler DE Wheeler GE Robinson, Hormones, Brain and Behavior San Diego: Academic Press, Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, 2 2009 2 1027 1068
30. Uncoupling primer and releaser responses to pheromone in honey bees. CM Grozinger P Fischer JE Hampton, Naturwissenschaften 2007 94 5 375 379 10.1007/s00114-006-0197-8 17187255
31. Endocrine modulation of a pheromone-responsive gene in the honey bee brain. CM Grozinger GE Robinson, J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2007 193 4 461 470 10.1007/s00359-006-0202-x 17192826
32. Pheromone-mediated gene expression in the honey bee brain. CM Grozinger NM Sharabash CW Whitfield GE Robinson, Proc Natl Acad Sci USA 2003 100 Suppl 2 14519 14525 10.1073/pnas.2335884100 14573707
33. The gene regulatory logic of transcription factor evolution. GP Wagner VJ Lynch, Trends in Ecology and Evolution 2008 23 7 377 385 10.1016/j.tree.2008. 03.006 18501470
34. Ovarian development and egg laying in workers of Bombus terrestris. MJ Duchateau HHW Velthuis, Entomol Exp Appl 1989 51 199 213 10.1007/BF00347883
35. Three classes of C2H2 zinc finger proteins. S Iuchi, Cell Mol Life Sci 2001 58 4 625 635 10.1007/PL00000885 11361095
36. Phylogenomic analysis reveals bees and wasps (Hymenoptera) at the base of the radiation of Holometabolous insects. J Savard D Tautz S Richards GM Weinstock RA Gibbs JH Werren H Tettelin MJ Lercher, Genome Res 2006 16 1334 1338 10.1101/gr.5204306 17065606
37. Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. BM Wiegmann MD Trautwein JW Kim BK Cassel MA Bertone SL Winterton DK Yeates, BMC Biol 2009 7 34 10.1186/1741-7007-7-34 19552814
38. Regulation of reproduction by dominant workers in bumblebee colonies (Bombus terrestris) queenright colonies. G Bloch A Hefetz, Beh Ecol Sociobiol 1999 45 125 135 10.1007/s002650050546 (Pubitemid 29153787)
39. The biology of humble-bees, with special reference to the production of the worker caste. RA Cumber, Trans R Ent Soc Lond 1949 100 1 45
40. Genome-wide analysis reveals differences in brain gene expression patterns associated with caste and reproductive status in honey bees (Apis mellifera). CM Grozinger Y Fan SE Hoover ML Winston, Mol Ecol 2007 16 22 4837 4848 10.1111/j.1365-294X.2007.03545.x 17927707
41. Genomic analysis of post-mating changes in the honey bee queen (Apis mellifera). SD Kocher FJ Richard DR Tarpy CM Grozinger, BMC Genomics 2008 9 232 10.1186/1471-2164-9-232 18489784
42. Dissecting the role of Kr-h1 brain gene expression in foraging behavior in honey bees (Apis mellifera). B Fussnecker C Grozinger, Insect Mol Biol 2008 17 515 522 10.1111/j.1365-2583.2008.00819.x 18715264
43. Limits on volume changes in the mushroom bodies of the honey bee brain. SE Fahrbach SM Farris JP Sullivan GE Robinson, J Neurobiol 2003 57 141 151 10.1002/neu.10256 14556280
44. Effects of experience and juvenile hormone on the organization of the mushroom bodies of honey bees. GS Withers SE Fahrbach GE Robinson, J Neurobiol 1995 26 130 144 10.1002/neu.480260111 7714522
45. Roles of Drosophila Kruppel-homolog 1 in neuronal morphogenesis. L Shi S Lin Y Grinberg Y Beck CM Grozinger GE Robinson T Lee, Dev Neurobiol 2007 67 1614 1626 10.1002/dneu.20537 17562531
46. Kruppel homolog 1 (Kr-h1) mediates juvenile hormone action during metamorphosis of Drosophila melanogaster. C Minakuchi X Zhou LM Riddiford, Mech Dev 2008 125 91 105 10.1016/j.mod.2007.10.002 18036785
47. Kruppel homolog 1, an early juvenile hormone-response gene downstream of Methoprene-tolerant, mediates its anti-metamorphic action in the red flour beetle Tribolium castaneum. C Minakuchi T Namiki T Shinoda, Dev Biol 2008 325 341 350 10.1016/j.ydbio.2008.10.016 19013451
48. bHLH-PAS family transcription factor methoprene-tolerant plays a key role in JH action in preventing the premature development of adult structures during larval-pupal metamorphosis. R Parthasarathy A Tan SR Palli, Mech Dev 2008 125 601 616 10.1016/j.mod.2008.03.004 18450431
49. A gain-of-function screen for genes controlling motor axon guidance and synaptogenesis in Drosophila. R Kraut K Menon K Zinn, Curr Biol 2001 11 6 417 430 10.1016/S0960-9822(01)00124-5 11301252
50. From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design. SB Carroll JK Grenier SD Weatherbee, Malden, MA: Blackwell Publishing 2005
51. Evo-devo and the evolution of social behavior. AL Toth GE Robinson, Trends Genet 2007 23 334 341 10.1016/j.tig.2007.05.001 17509723
52. Juvenile hormone in adult eusocial Hymenoptera: gonadotropin and behavioral pacemaker. GE Robinson EL Vargo, Arch Insect Biochem Physiol 1997 35 4 559 583 10.1002/(SICI)1520-6327(1997)35:4<559::AID-ARCH13>3.0.CO;2-9 9210289
53. Wasp societies as microcosms for the study of development and evolution. MJ West-Eberhard, Natural history and evolution of paper wasps Oxford: Oxford University Press, Turillazzi S, West-Eberhard MJ, 1996 290 317
54. Social insect polymorphism: hormonal regulation of plasticity in development and reproduction in the honeybee. K Hartfelder W Engels, Curr Top Dev Biol 1998 40 45 77 10.1016/S0070-2153(08)60364-6 9673848
55. Developmentally determined attenuation in circadian rhythms links chronobiology to social organization in bees. S Yerushalmi S Bodenhaimer G Bloch, J Exp Biol 2006 209 1044 1051 10.1242/jeb.02125 16513930
56. Behavioral rhythmicity, age, division of labor and period expression in the honey bee brain. G Bloch DP Toma GE Robinson, J Biol Rhythms 2001 16 444 456 10.1177/074873001129002123 11669418
57. Effect of group size on ovarian development in bumblebee workers (Hymenoptera: apidae: Bombus). J Cnaani A Wong JD Thomson, Entomologia Generalis 2007 29 305 314
58. Brain biogenic amines and reproductive dominance in bumble bees (Bombus terrestris). G Bloch T Simon GE Robinson A Hefetz, J Comp Physiol [A] 2000 186 261 268 10.1007/s003590050426 10757241
59. Reproductive division of labor, dominance, and ecdysteroid levels in hemolymph and ovary of the bumble bee Bombus terrestris. S Geva K Hartfelder G Bloch, J Insect Physiol 2005 51 811 823 10.1016/j.jinsphys.2005.03.009 15885700
60. Regulation of queen-worker conflict in bumble-bee (Bombus terrestris) colonies. G Bloch, Proc R Soc Lond B Biol Sci 1999 266 2465 2469 10.1098/rspb.1999.0947
61. Development and reproductive strategies in Bombus colonies. MJ Duchateau HHW Velthuis, Behavior 1988 107 186 196 10.1163/156853988X00340
62. The ontogeny of a dominance hierarchy in colonies of the bumblebee Bombus terrestris (Hymenoptera, Apidae). A Van Doorn J Heringa, Insect Sociaux 1986 33 3 25 10.1007/BF02224031
63. Comparing injection, feeding and topical application methods for treatment of honeybees with octopamine. AB Barron J Maleszka RK Vander Meer GE Robinson R Maleszka, J Insect Physiol 2007 53 187 194 10.1016/j.jinsphys.2006. 11.009 17270208
64. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. TA Hall, Nucleo Acids Symp Ser 1999 41 95 98
65. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. S Guindon O Gascuel, Syst Biol 2003 52 696 704 10.1080/10635150390235520 14530136
66. Estimating maximum likelihood phylogenies with PhyML. S Guindon F Delsuc JF Dufayard O Gascuel, Methods Mol Biol 2009 537 113 137 19378142
67. The rapid generation of mutation data matrices from protein sequences. DT Jones WR Taylor JM Thornton, Comput Appl Biosci 1992 8 275 282 1633570
68. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. K Tamura J Dudley M Nei S Kumar, Mol Biol Evol 2007 24 1596 1599 10.1093/molbev/msm092 17488738
69. The phylogeny of the extant hexapod orders. WC Wheeler M Whiting QD Wheeler JM Carpenter, Cladistics 2001 17 113 169 10.1111/j.1096-0031.2001. tb00115.x
70. Arthropod phylogeny with special reference to insects. HB Boudreaux, New York: Wiley 1979
71. Insect Phylogeny. W Hennig, New York: Wiley 1981
72. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. S Whelan N Goldman, Mol Biol Evol 2001 18 5 691 699 11319253