Characterization of quantitative trait loci for the age of first foraging in honey bee workers

Behavior Genetics

Volumn 39, Issue 5, 2009, Pages 541-553

  Rueppell, Olav ^a  

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

Author keywords

AFLP; Behavioral ontogeny; Complex traits; Division of labor; Foraging onset; Genetic architecture; Life history; Social insects

Indexed keywords

AMONTILLADO PROTEIN; ANKYRIN; ANKYRIN 2; MITOGEN ACTIVATED PROTEIN KINASE 7; PROTEIN KINASE C; PROTEIN PRECURSOR; UNCLASSIFIED DRUG;

AGE DISTRIBUTION; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ANIMAL EXPERIMENT; ARTICLE; CHROMOSOME; CONTROLLED STUDY; FORAGING; FORAGING BEHAVIOR; GENE EXPRESSION; GENE MAPPING; GENE SEQUENCE; GENETIC LINKAGE; GENOME; GENOMICS; GENOTYPE; HONEYBEE; MICROSATELLITE INSTABILITY; MORPHOLOGICAL TRAIT; NONHUMAN; ORGANISM COLONY; POLLEN; QUANTITATIVE TRAIT LOCUS; SINGLE NUCLEOTIDE POLYMORPHISM;

ALLELES; ANIMALS; BEES; BEHAVIOR, ANIMAL; CROSSES, GENETIC; FEEDING BEHAVIOR; FEMALE; GENOMICS; GENOTYPE; MALE; MICROSATELLITE REPEATS; MODELS, GENETIC; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; SOCIAL BEHAVIOR;

APIS MELLIFERA; HEXAPODA;

EID: 69049092628     PISSN: 00018244     EISSN: 15733297     Source Type: Journal    
DOI: 10.1007/s10519-009-9278-8     Document Type: Article

References (69)

1. HA Adams BR Southey GE Robinson SL Rodriguez-Zas 2008 Meta-analysis of genome-wide expression patterns associated with behavioral maturation in honey bees BMC Genomics 9 503 10.1186/1471-2164-9-503
2. GV Amdam A Csondes MK Fondrk RE Page Jr 2006 Complex social behaviour derived from maternal reproductive traits Nature 439 76 78 10.1038/nature04340
3. AD Ammons GJ Hunt 2008 Identification of quantitative trait loci and candidate genes influencing ethanol sensitivity in honey bees Behav Genet 38 531 553 10.1007/s10519-008-9218-z
4. ME Arechavaleta-Velasco GJ Hunt 2004 Binary trait loci that influence honey bee (Hymenoptera:Apidae) guarding behavior Ann Entomol Soc Am 97 177 183 10.1603/0013-8746(2004)097[0177:BTLTIH]2.0.CO;2
5. AR Barchuk AS Cristino R Kucharski LF Costa ZLP Simoes R Maleszka 2007 Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera BMC Dev Biol 7 70
6. AB Barron DJ Schulz GE Robinson 2002 Octopamine modulates responsiveness to foraging-related stimuli in honey bees (Apis mellifera) J Comp Physiol [A] 188 603 610 10.1007/s00359-002-0335-5
7. Y Ben-Shahar A Robichon MB Sokolowski GE Robinson 2002 Influence of gene action across different time scales on behavior Science 296 741 744 10.1126/science.1069911
8. Y Ben-Shahar NL Dudek GE Robinson 2004 Phenotypic deconstruction reveals involvement of manganese transporter malvolio in honey bee division of labor J Exp Biol 207 3281 3288 10.1242/jeb.01151
9. M Beye I Gattermeier M Hasselmann T Gempe M Schioett JF Baines D Schlipalius F Mougel C Emore O Rueppell A Sirvio E Guzman-Novoa G Hunt M Solignac RE Page 2006 Exceptionally high levels of recombination across the honey bee genome Genome Res 16 1339 1344 10.1101/gr.5680406
10. SBC Chandra GJ Hunt S Cobey BH Smith 2001 Quantitative trait loci associated with reversal learning and latent inhibition in honeybees (Apis mellifera) Behav Genet 31 275 285 10.1023/A:1012227308783
11. VR Chintapalli J Wang JAT Dow 2007 Using FlyAtlas to identify better Drosophila models of human disease Nat Genet 39 715 720 10.1038/ng2049
12. A Darvasi M Soller 1994 Selective DNA pooling for determination of linkage between a molecular marker and a quantitative trait locus Genetics 138 1365 1373
13. SE Fahrbach D Moore EA Capaldi SM Farris GE Robinson 1998 Experience-expectant plasticity in the mushroom bodies of the honeybee Learn Mem 5 115 123
14. T Farooqui 2007 Octopamine-mediated neuromodulation of insect senses Neurochem Res 32 1511 1529 10.1007/s11064-007-9344-7
15. G Gort WJM Koopman A Stein 2006 Fragment length distributions and collision probabilities for AFLP markers Biometrics 62 1107 1115 10.1111/j.1541-0420.2006.00613.x
16. JC Hall SN Alahiotis DA Strumpf K White 1980 Behavioral and biochemical defects in temperature sensitive acetylcholinesterase mutants of Drosophila melanogaster Genetics 96 939 965
17. T Homyk DE Sheppard 1977 Behavioral mutants of Drosophila melanogaster. 1. Isolation and mapping of mutations which decrease flight ability Genetics 87 9 5 104
18. Honeybee Genome Consortium 2006 Insights into social insects from the genome of the honeybee Apis mellifera Nature 443 931 949 10.1038/nature05260
19. K Honjo K Furukubo-Tokunaga 2005 Induction of cAMP response element-binding protein-dependent medium-term memory by appetitive gustatory reinforcement in Drosophila larvae J Neurosci 25 7905 7913 10.1523/JNEUROSCI. 2135-05.2005
20. B Hoogendoorn N Norton G Kirov N Williams ML Hamshere G Spurlock J Austin MK Stephens PR Buckland MJ Owen MC O'Donovan 2000 Cheap, accurate and rapid allele frequency estimation of single nucleotide polymorphisms by primer extension and DHPLC in DNA pools Hum Genet 107 488 493 10.1007/s004390000397
21. MA Humphries U Muller MK Fondrk RE Page Jr 2003 PKA and PKC content in the honey bee central brain differs in genotypic strains with distinct foraging behavior J Comp Physiol [A] 189 555 562 10.1007/s00359-003-0433-z
22. MA Humphries MK Fondrk RE Page Jr 2005 Locomotion and the pollen hoarding behavioral syndrome of the honeybee (Apis mellifera L.) J Comp Physiol [A] 191 669 674 10.1007/s00359-005-0624-x
23. GJ Hunt RE Page Jr MK Fondrk CJ Dullum 1995 Major quantitative trait loci affecting honey bee foraging behavior Genetics 141 1537 1545
24. GJ Hunt E Guzman-Novoa MK Fondrk RE Page Jr 1998 Quantitative trait loci for honey bee stinging behavior and body size Genetics 148 1203 1213
25. GJ Hunt GV Amdam D Schlipalius C Emore N Sardesai CE Williams O Rueppell E Guzman-Novoa M Arechavaleta-Velasco S Chandra MK Fondrk M Beye RE Page Jr 2007 Behavioral genomics of honeybee foraging and nest defense Naturwissenschaften 94 247 267 10.1007/s00114-006-0183-1
26. I Koch H Schwarz D Beuchle B Goellner M Langegger H Aberle 2008 Drosophila ankyrin 2 is required for synaptic stability Neuron 58 210 222 10.1016/j.neuron.2008.03.019
27. A Korol Z Frenkel L Cohen E Lipkin M Soller 2007 Fractioned DNA pooling: a new cost-effective strategy for fine mapping of quantitative trait loci Genetics 176 2611 2623 10.1534/genetics.106.070011
28. ES Lander D Botstein 1989 Mapping mendelian factors underlying quantitative traits using RFLP linkage maps Genetics 121 185 199
29. KL Lapidge BP Oldroyd M Spivak 2002 Seven suggestive quantitative trait loci influence hygienic behavior of honey bees Naturwissenschaften 89 565 568
30. HMG Lattorff RFA Moritz RM Crewe M Solignac 2007 Control of reproductive dominance by the thelytoky gene in honeybees Biol Lett 3 292 295 10.1098/rsbl.2007.0083
31. Y Le Conte A Hefetz 2008 Primer pheromones in social hymenoptera Annu Rev Entomol 53 523 542 10.1146/annurev.ento.52.110405.091434
32. Lincoln SE, Daly MJ, Lander ES (1993) Constructing genetic linkage maps with MAPMAKER/EXP version 3.0: a tutorial and reference manual. In: A whitehead institute for biomedical research technical report, Cambridge, MA
33. TFC Mackay 2001 The genetic architecture of quantitative traits Annu Rev Genet 35 303 339 10.1146/annurev.genet.35.102401.090633
34. CM Nelson KE Ihle MK Fondrk RE Page Jr GV Amdam 2007 The gene vitellogenin has multiple coordinating effects on social organization PLoS Biol 5 e62 10.1371/journal.pbio.0050062
35. PR Oxley GJ Thompson BP Oldroyd 2008 Four quantitative trait loci that influence worker sterility in the honeybee (Apis mellifera) Genetics 179 1337 1343 10.1534/genetics.108.087270
36. RE Page Jr GV Amdam 2007 The making of a social insect: developmental architectures of social design BioEssays 29 334 343 10.1002/bies.20549
37. RE Page Jr J Erber 2002 Levels of behavioral organization and the evolution of division of labor Naturwissenschaften 89 91 106 10.1007/s00114-002-0299-x
38. RE Page Jr MK 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 Behav Ecol Sociobiol 36 135 144 10.1007/BF00170718
39. RE Page Jr MK Fondrk GJ Hunt E Guzman-Novoa MA Humphries K Nguyen AS Greene 2000 Genetic dissection of honeybee (Apis mellifera L.) foraging behavior J Hered 91 474 479 10.1093/jhered/91.6.474
40. RE Page Jr J Gadau M Beye 2002 The emergence of hymenopteran genetics Genetics 160 375 379
41. T Pankiw 2003 Directional change in a suite of foraging behaviors in tropical and temperate evolved honey bees (Apis mellifera L.) Behav Ecol Sociobiol 54 458 464 10.1007/s00265-003-0640-1
42. PC Phillips 1999 From complex traits to complex alleles Trends Genet 15 6 8 10.1016/S0168-9525(98)01622-9
43. J Ragoussis GP Elvidge K Kaur S Colella 2006 Matrix-assisted laser desorption/ionisation, time-of-flight mass spectrometry in genomics research PLOS Genet 2 920 929 10.1371/journal.pgen.0020100
44. LYM Rayburn HC Gooding SP Choksi D Maloney AR Kidd DE Siekhaus M Bender 2003 amontillado, the Drosophila homolog of the prohormone processing protease PC2, is required during embryogenesis and early larval development Genetics 163 227 237
45. GE Robinson 2002 Genomics and integrative analyses of division of labor in honeybee colonies Am Nat 160 S160 S172 10.1086/342901
46. GE Robinson Z-Y Huang 1998 Colony integration in honey bees: genetic, endocrine and social control of division of labor Apidology 29 159 170 10.1051/apido:19980109
47. GE Robinson RD Fernald DF Clayton 2008 Genes and social behavior Science 322 896 900 10.1126/science.1159277
48. O Rueppell T Pankiw DI Nielson MK Fondrk M Beye RE Page Jr 2004 The genetic architecture of the behavioral ontogeny of foraging in honey bee workers Genetics 167 1767 1779 10.1534/genetics.103.021949
49. O Rueppell SBC Chandra T Pankiw MK Fondrk M Beye GJ Hunt RE Page Jr 2006 The genetic architecture of sucrose responsiveness in the honey bee (Apis mellifera L.) Genetics 172 243 251 10.1534/genetics.105.046490
50. O Rueppell RE Page Jr MK Fondrk 2006 Male behavioural maturation rate responds to selection on pollen hoarding in honeybees Anim Behav 71 227 234 10.1016/j.anbehav.2005.05.008
51. O Rueppell C Bachelier MK Fondrk RE Page Jr 2007 Regulation of life history determines lifespan of worker honey bees (Apis mellifera L.) Exp Gerontol 42 1020 1032 10.1016/j.exger.2007.06.002
52. O Rueppell R Linford P Gardner J Coleman K Fine 2008 Aging and demographic plasticity in response to experimental age structures in honeybees (Apis mellifera L.) Behav Ecol Sociobiol 62 1621 1631 10.1007/s00265-008-0591-7
53. O Rüppell T Pankiw RE Page Jr 2004 Pleiotropy, epistasis and new QTL: the genetic architecture of honey bee foraging behavior J Hered 95 481 491 10.1093/jhered/esh072
54. M Schuelke 2000 An economic method for the fluorescent labeling of PCR fragments Nat Biotechnol 18 233 234 10.1038/72708
55. MD Schug EE Regulski A Pearce SG Smith 2004 Isolation and characterization of dinucleotide repeat microsatellites in Drosophila ananassae Genet Res 83 19 29 10.1017/S0016672303006542
56. DJ Schulz ZY Huang GE Robinson 1998 Effects of colony food shortage on behavioral development in honey bees Behav Ecol Sociobiol 42 295 303 10.1007/s002650050442
57. M Sen-Sarma CW Whitfield GE Robinson 2007 Species differences in brain gene expression profiles associated with adult behavioral maturation in honey bees BMC Genomics 8 202 10.1186/1471-2164-8-202
58. M Shapira CK Thompson H Soreq GE Robinson 2001 Changes in neuronal acetylcholinesterase gene expression and division of labor in honey bee colonies J Mol Neurosci 17 1 12 10.1385/JMN:17:1:1
59. M Solignac F Mougel D Vautrin M Monnerot JM Cornuet 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 10.1186/gb-2007-8-4-r66
60. JP Sullivan O Jassim SE Fahrbach GE Robinson 2000 Juvenile hormone paces behavioral development in the adult worker honey bee Horm Behav 37 1 14 10.1006/hbeh.1999.1552
61. P Tomancak A Beaton R Weiszmann E Kwan S Shu SE Lewis S Richards M Ashburner V Hartenstein SE Celniker GM Rubin 2002 Systematic determination of patterns of gene expression during Drosophila embryogenesis Genome Biol 3 research0088.1 research0088.14
62. Van Ooijen JW, Boer MP, Jansen RC, Maliepaard C (2002) MapQTL 4.0, software for the calculation of QTL positions on genetic maps. Plant Research International, Wageningen, The Netherlands
63. A Vasemagi CR Primmer 2005 Challenges for identifying functionally important genetic variation: the promise of combining complementary research strategies Mol Ecol 14 3623 3642 10.1111/j.1365-294X.2005.02690.x
64. Wang Y, Amdam GV, Rueppell O, Wallrichs M, Fondrk MK, Kaftanoglu O, Page RE Jr (2009) PDK1 and HR46 gene homologs tie social behavior to ovary signals. PLoS ONE 4:e4899. doi: 10.1371/journal.pone.0004899
65. ML Wayne LM McIntyre 2002 Combining mapping and arraying: an approach to candidate gene identification Proc Natl Acad Sci USA 99 14903 14906 10.1073/pnas.222549199
66. CW Whitfield A-M Cziko GE Robinson 2003 Gene expression profiles in the brain predict behavior in individual honey bees Science 302 296 299 10.1126/science.1086807
67. CW Whitfield SK Behura SH Berlocher AG Clark JS Johnston WS Sheppard DR Smith AV Suarez D Weaver ND Tsutsui 2006 Thrice out of Africa: ancient and recent expansions of the honey bee, Apis mellifera Science 314 642 645 10.1126/science.1132772
68. CW Whitfield Y Ben-Shahar C Brillet I Leoncini D Crauser Y LeConte S Rodriguez-Zas GE Robinson 2006 Genomic dissection of behavioral maturation in the honey bee Proc Natl Acad Sci USA 103 16068 16075 10.1073/pnas.0606909103
69. RJ Wilson JL Goodman VB Strelets FlyBase Consortium 2008 FlyBase: integration and improvements to query tools Nucleic Acids Res 36 D588 D593 10.1093/nar/gkm930