The effects of mating and instrumental insemination on queen honey bee flight behaviour and gene expression

Insect Molecular Biology

Volumn 19, Issue 2, 2010, Pages 153-162

  Kocher, S D ^a   Tarpytt, D R ^a   Grozinger, C M ^a,b  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Behavior; Gene expression; Genomics; Honey bee; Instrumental insemination; Reproduction

Indexed keywords

VITELLOGENIN;

ANIMAL; ARTICLE; ARTIFICIAL INSEMINATION; BEE; BIOLOGICAL MODEL; BRAIN; COMPARATIVE STUDY; DNA MICROARRAY; DROSOPHILA MELANOGASTER; FEMALE; FLYING; GENE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETICS; MALE; METABOLISM; PHYSIOLOGY; SEXUAL BEHAVIOR; SEXUAL MATURATION; SPECIES DIFFERENCE;

ANIMALS; BEES; BRAIN; DROSOPHILA MELANOGASTER; FEMALE; FLIGHT, ANIMAL; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENES, INSECT; INSEMINATION; INSEMINATION, ARTIFICIAL; MALE; MODELS, BIOLOGICAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SEXUAL BEHAVIOR, ANIMAL; SEXUAL MATURATION; SPECIES SPECIFICITY; VITELLOGENINS;

APIS MELLIFERA; DROSOPHILA MELANOGASTER; HEXAPODA;

EID: 77952633295     PISSN: 09621075     EISSN: 13652583     Source Type: Journal    
DOI: 10.1111/j.1365-2583.2009.00965.x     Document Type: Article

References (47)

1. Amdam, G.V., Csondes, A., Fondrk, M.K. and Page, R.E., Jr (2006) Complex social behaviour derived from maternal reproductive traits. Nature 439: 76-78.
2. Cobey, S.W. (2007) Comparison studies of instrumentally insemi nated and naturally mated honey bee queens and factors affecting their performance. Apidologie 38: 390-410.
3. Dennis, G., Jr, Sherman, B.T., Hosack, D.A., Yang, J., Gao, W., Lane, H.C. et al. (2003) DAVID: Database for annotation, visu alization, and integrated discovery. Genome Biol 4: R60.
4. Engels, W. and Imperatriz-Fonseca, V.L. (1990) Caste develop ment, reproductive strategies and control of fertility in honey bees and stingless bees. In Social Insects: An Evolutionary Approach to Caste and Reproduction (Engels, W., ed.), pp. 167-230. Springer-Verlag, Heidelberg.
5. Engels, W., Gongalves, L.S. and Engles, E. (1976) Effects of carbon dioxide on vitellogenin metabolism in unmated queen honeybees. J Apicultural Res 15: 3-10.
6. Grozinger, C.M., Sharabash, N.M., Whitfield, C.W. and Robinson, G.E. (2003) Pheromone-mediated gene expression in the honey bee brain. Proc Natl Acad Sci USA 100: 14519-14525.
7. Grozinger, C.M., Fan, Y., Hoover, S.E. and Winston, M.L. (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.
8. Harris, J.W., Woodring, J. and Harbo, J.R. (1996) Effects of carbon dioxide on levels of biogenic amines in the brains of queenless worker and virgin queen honey bees (Apis mel-lifera). J Apicultural Res 35: 69-78.
9. Huang da, W., Sherman, B.T. and Lempicki, R.A. (2009) System atic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
10. Hunt, G.J., Amdam, G.V., Schlipalius, D., Emore, C., Sardesai, N., Williams, C.E. et al. (2007) Behavioral genomics of hon eybee foraging and nest defense. Naturwissenschaften 94:247-267.
11. Kaftanoglu, O. and Peng, Y.S. (1982) Effects of insemination on the initiation of oviposition in the queen honey bee. J Apicul-tural Res 1 : 3-6.
12. Keeling, C.I., Slessor, K.N., Higo, H.A. and Winston, M.L. (2003) New components of the honey bee (Apis mellifera L.) queen retinue pheromone. Proc Natl Acad Sci USA 100: 4486-4491.
13. Kocher, S.D., Richard, F.J., Tarpy, D.R. and Grozinger, C.M. (2008) Genomic analysis of post-mating changes in the honey bee queen (Apis mellifera). BMC Genomics 9: 232.
14. Kocher, S.D., Richard, F.J., Tarpy, D.R. and Grozinger, C.M. (2009) Queen reproductive state modulates pheromone production and queen-worker interactions in honey bees. Behav Ecol 0: 1007-1014.
15. Lai, C.Q., Parnell, L.D., Lyman, R.F., Ordovas, J.A. and Mackay, T.F.C. (2007) Candidate genes affecting Drosophila life span identified by integrating microarray gene expression analysis and QTL mapping. Mech Ageing Dev 1 8: 237-249.
16. Laidlaw, J.H.H. and Page, R.E., Jr (1997) Queen Rearing and Bee Breeding. Wicwas, Cheshire, CT.
17. Lawniczak, M.K.N. and Begun, D.J. (2004) A genome-wide analysis of courting and mating responses in Drosophila melanogaster females. Genome 47: 900-910.
18. Lawniczak, M.K.N., Barnes, A.I., Linklater, J.R., Boone, J.M., Wigby, S. and Chapman, T. (2007) Mating and immunity in invertebrates. Trends Ecol Evol : 48-55.
19. Lodesani, M. and Vecchi, M.A. (1996) A study on the develop ment of the ovaries of queen bees ( Apis mellifera ligustica) instrumentally and naturally mated. Apicol Mod 87: 65-70.
20. McGraw, L.A., Gibson, G., Clark, A.G. and Wolfner, M.F. (2004) Genes regulated by mating, sperm or seminal proteins in mated female Drosophila melanogaster. Curr Biol 14: 1509 1514.
21. McGraw, L.A., Clark, A.G. and Wolfner, M.F. (2008) Post-mating gene expression profiles of female Drosophila melanogaster in response to time and to four male accessory gland proteins. Genetics 179: 1395-1408.
22. Mack, P.D., Kapelnikov, A., Heifetz, Y. and Bender, M. (2006) Mating-responsive genes in reproductive tissues of female Drosophila melanogaster. Proc Natl Acad Sci USA 103: 10358-10363.
23. Mackensen, O. (1947) Effect of carbon dioxide on initial oviposi-tion of artificially inseminated and virgin queen bees. J Econ Entomol 40: 344-349.
24. Nijhout, H.F. (1984) Abdominal stretch reception in Dipetalogaster- Maximus (Hemiptera, Reduviidae). J Insect Physiol 30: 629-633.
25. Plettner, E., Slessor, K.N., Winston, M.L., Robinson, G.E. and Page, R.E., Jr (1993) Mandibular gland components and ovarian development as measures of caste differentiation in the honey bee (Apis mellifera L). J Insect Physiol 39: 235 240.
26. Plettner, E., Otis, G.W., Wimalaratne, P.D.C., Winston, M.L., Slessor, K.N., Pankiw, T. etal. (1997) Species- and caste-determined mandibular gland signals in honeybees (Apis). J Chem Ecol 23: 363-377.
27. Roberts, W.C. (1944) Multiple mating of queen bees proved by progeny and flight tests. Glean Bee Cult 72: 255-260.
28. Robinson, G.E. and Vargo, E.L. (1997) Juvenile hormone in adult eusocial Hymenoptera: Gonadotropin and behavioral pace maker. Arch Insect Biochem Physiol 35: 559-583.
29. Rogers, D.W., Whitten, M.M.A., Thailayil, J., Soichot, J., Levashina, E.A. and Catteruccia, F. (2008) Molecular and cellular components of the mating machinery in Anopheles gambiae females. Proc Natl Acad Sci USA 105: 19390 19395.
30. Schluns, H., Moritz, R.F.A., Neumann, P., Kryger, P. and Koeni-ger, G. (2005) Multiple nuptial flights, sperm transfer and the evolution of extreme polyandry in honey bee queens. Anim Behav 70: 125-131.
31. Seeley, T.D. and Tarpy, D.R. (2007) Queen promiscuity lowers disease within honeybee colonies. Proc Biol Sci 274: 67-72.
32. Stearns, S.C. (1992) The Evolution of Life Histories. Oxford Uni versity Press, New York, NY.
33. Sturn, A., Quackenbush, J. and Trajanoski, Z. (2002) Genesis: Cluster analysis of microarray data. Bioinformatics 18: 207 208.
34. Sugawara, T. (1979) Stretch reception in bursa copulatrix of the butterfly, Pieris rapae crucivora, and its role in behaviour. J Comp Physiol 130: 191-199.
35. Suzuki, R. and Shimodaira, H. (2006) Pvclust: An R package for assessing the uncertainty in hierarchical clustering. Bioinfor- matics 22: 1540-1542.
36. Tanaka, E.D. and Hartfelder, K. (2004) The initial stages of oogenesis and their relation to differential fertility in the honey bee (Apis mellifera) castes. Arthropod Struct Dev 33: 431 442.
37. Tarpy, D.R. (2000) Behavioral and evolutionary mechanisms of polyandryin honeybees (Apis mellifera). PhD thesis, Univer sity of California, Davis, CA.
38. Tarpy, D.R., Nielsen, R. and Nielsen, D.I. (2004) A scientific note on the revised estimates of effective paternity frequency in Apis. Insectes Sociaux 51: 203-204.
39. Tarpy, D.R. and Page, R.E. (2000) No behavioral control over mating frequency in queen honey bees (Apis mellifera L.): implications for the evolution of extreme polyandry. Am Nat 155: 820-827.
40. Tarpy, D.R. and Page, R.E., Jr (2001) The curious promiscuity of queen honey bees (Apis mellifera): Evolutionary and behav ioral mechanisms. Ann Zool Fenn 38: 255-265.
41. Valle, D. (1993) Vitellogenesis in insects and other groups - a review. Mem Inst Oswaldo Cruz 88: 1-26.
42. Whitfield, C.W., Cziko, A.M. and Robinson, G.E. (2003) Gene expression profiles in the brain predict behavior in individual honey bees. Science 302: 296-299.
43. Whitfield, C.W., Ben-Shahar, Y., Brillet, C., Leoncini, I., Crauser, D., Leconte, Y. et al. (2006) Genomic dissection of behavioral maturation in the honey bee. Proc Natl Acad Sci USA 103: 16068-16075.
44. Williams, J. and Harbo, J.R. (1982) Bioassays for diluents of honey bee semen. Ann Entomol Soc Am 75: 457-459.
45. Winston, M.L. (1991) The Biology of the Honey Bee. Harvard University Press, Cambridge, MA.
46. Wolfner, M.F. (1997) Tokens of love: Functions and regulation of Drosophila male accessory gland products. Insect Biochem Mol Biol 27: 179-192.
47. Wolfner, M.F. (2002) The gifts that keep on giving: Physiological functions and evolutionary dynamics of male seminal proteins in Drosophila. Heredity88: 85-93.