Thelytokous parthenogenesis in unmated queen honeybees (Apis mellifera capensis): Central fusion and high recombination rates

Genetics

Volumn 180, Issue 1, 2008, Pages 359-366

  Oldroyd, Benjamin P ^a   Allsopp, Michael H ^b   Gloag, Rosalyn S ^a   Lim, Julianne ^a   Jordan, Lyndon A ^a   Beekman, Madeleine ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b PLANT PROTECTION RESEARCH INSTITUTE   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

APIS MELLIFERA CAPENSIS; ARTICLE; CONTROLLED STUDY; DIPLOIDY; EGG LAYING; FEMALE; GAMETE; GENE FUSION; GENE LOCUS; GENETIC RECOMBINATION; HAPLOIDY; HETEROZYGOSITY; HOMOZYGOSITY; HONEYBEE; NONHUMAN; PARTHENOGENESIS; PRIORITY JOURNAL; PROGENY; QUEEN (INSECT); SEX DETERMINATION; THELYTOKY; ANIMAL; BEE; BIOLOGICAL MODEL; DNA SEQUENCE; GENDER AND SEX; GENETIC LINKAGE; GENETICS; HETEROZYGOTE; MALE; SOUTH AFRICA;

APIS MELLIFERA;

DNA; MICROSATELLITE DNA;

ANIMALS; BEES; DNA; FEMALE; HETEROZYGOTE; LINKAGE (GENETICS); MALE; MICROSATELLITE REPEATS; MODELS, GENETIC; PARTHENOGENESIS; RECOMBINATION, GENETIC; SEQUENCE ANALYSIS, DNA; SEX DETERMINATION (GENETICS); SOUTH AFRICA;

EID: 56049111634     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.108.090415     Document Type: Article

References (49)

1. ALLSOPP, M. H., 1993 Summarized overview of the Capensis problem. S. Afr. Bee J. 65: 127-136.
2. ANDERSON, R. H., 1963 The laying worker in the Cape honeybee Apis mellifera capensis. J. Apic. Res. 2: 85-92.
3. BAUDRY, E., P. KRYGER, M. ALLSOPP, N. KOENIGER, D. VAUTRIN et al., 2004 Whole genome scan in thelytokous-laying workers of the Cape honey bee (Apis mellifera capensis): central fusion, reduced recombination rates and centromere mapping using half-tetrad analysis. Genetics 167: 243-252.
4. BELSHAW, R., and D. L. J. QUICKE, 2003 The cytogenetics of thelytoky in a predominantly asexual parasitoid wasp with covert sex. Genome 46: 170-173.
5. BEYE, M., M. HASSELMANN, M. K. FONDRK, R. E. PAGE and S. W. OMHOLT, 2003 The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114: 419-429.
6. CALDERONE, N. W., and L. P. S. KUENEN, 2001 Effects of Western honey bee (Hymenoptera: Apidae) colony, cell type, and larval sex on host acquisition by female Varroa destructor (Acdari: Varroidae). J. Econ. Entomol. 95: 1022-1030.
7. CREWE, R., and M. ALLSOPP, 1994 Sex and the single queen: recent experiments with capensis and scutellata queens. S. Afr. Bee J. 66: 58-62.
8. DADE, H. A., 1977 Anatomy and Dissection of the Honeybee. International Bee Research Association, London.
9. DIETEMANN, V., J. PFLUGFELDER, S. HÄRTEL, P. NEUMANN and R. CREWE, 2006 Social parasitism by honeybee workers (Apis mellifera capensis Esch.): evidence for pheromonal resistance to host queen's signals. Behav. Ecol. Sociobiol. 60: 785-793.
10. DZIERZON, J., 1845 Gutachten über die von Herrn Direktor Stöhr im ersten und zweiten Kapitel des General-Gutachtens aufgestellten Fragen. Eichstädter Bienenzeitung 1: 109-113, 119-121.
11. ESTOUP, A., M. SOLIGNAC and J.-M. CORNUET, 1994 Precise assessment of the number of patrilines and of genetic relatedness in honey bee colonies. Proc. R. Soc. Lond. Ser. B 258: 1-7.
12. FOURNIER, D., A. ESTOUP, R. M. ORIVEL, J. FOUCAUD, H. JOURDAN et al., 2005 Clonal reproduction by males and females in the little fire ant. Nature 435: 1230-1234.
13. HARBO, J. R., 1979 The rate of depletion of spermatozoa in the queen honeybee spermatheca. J. Apic. Res. 18: 204-207.
14. HARBO, J. R., 1986 Propagation and instrumental insemination, pp. 361-389 in Bee Genetics and Breeding, edited by T. E. RINDERER. Academic Press, Orlando, FL.
15. HASSELMANN, M., and M. BEYE, 2004 Signatures of selection among sex determining alleles of the honey bee. Proc. Natl. Acad. Sci. USA 101: 4888-4893.
16. HASSELMANN, M., and M. BEYE, 2006 Pronounced differences of recombination activity at the sex determination locus of the honeybee, a locus under strong balancing selection. Genetics 174: 1469-1480.
17. JONES, J., M. MYERSCOUGH, S. GRAHAM and B. P. OLDROYD, 2004 Honey bee nest thermoregulation: diversity promotes stability. Science 305: 402-404.
18. JORDAN, L. A., M. H. ALLSOPP, B. P. OLDROYD, T. C. WOSSLER and M. BEEKMAN, 2008 Cheating honeybee workers produce royal offspring. Proc. R. Soc. Lond. Ser. B 275: 345-351.
19. KOENIGER, N., 1970 Factors determining the laying of drone and worker eggs by the queen honey bee. Bee World 51: 166-169.
20. LAIDLAW, H. H., and R. E. J. PAGE, 1997 Queen Rearing and Bee Breeding. Wicwas Press, Cheshire, UK.
21. LATTORFF, H. M. G., R. F. A. MORITZ and S. FUCHS, 2005 A single locus determines thelytokous parthenogenesis of laying honeybee workers (Apis mellifera capensis). Heredity 94: 533-537.
22. LATTORFF, H. M. G., R. F. A. MORITZ, R. M. CREWE and M. SOLIGNAC, 2007 Control of reproductive dominance by the thelytoky gene in honeybees. Biol. Lett. 3: 292-295.
23. MACKENSEN, O., 1943 The occurrence of parthenogenetic females in some strains of honey-bees. J. Econ. Entomol. 36: 465-467.
24. MACKENSEN, O., 1947 Effect of carbon dioxide on initial oviposition of artificially inseminated and virgin queen honey bees. J. Econ. Entomol. 40: 344-349.
25. MATTILA, H. R., and T. D. SEELEY, 2007 Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317: 362-364.
26. MORITZ, R. F. A., and M. HABERL, 1994 Lack of meiotic recombination in thelytocous parthenogenesis of of laying workers of Apis mellifera capensis (the Cape honeybee). Heredity 73: 98-102.
27. MORITZ, R. F. A., P. KRYGER and M. H. ALLSOPP, 1996 Competition for royalty in bees. Nature 384: 31.
28. NACHTSHEIM, H., 1913 Cytologische studien über die geschlechtsbestimmung bie der honigbiene (Apis mellifera L.). Arch. Zellforsch. 11: 119-241.
29. NEUMANN, P., S. E. RADLOFF, R. F. A. MORITZ, H. R. HEPBURN and S. L. REECE, 2001 Social parasitism by honeybee workers (Apis mellifera capensis Escholtz): host finding and resistance of hybrid host colonies. Behav. Ecol. 12: 419-428.
30. OLDROYD, B. P., and J. H. FEWELL, 2007 Genetic diversity promotes homeostasis in insect colonies. Trends Ecol. Evol. 22: 408-413.
31. ONIONS, G. W., 1912 South African 'fertile worker bees'. Agric. J. Union S. Afr. 1: 720-728.
32. PEARCY, M., S. ARON, C. DOUMS and L. KELLER, 2004 Conditional use of sex and parthenogenesis for worker and queen production in ants. Science 306: 1780-1783.
33. PEARCY, M., O. HARDY and S. ARON, 2006 Thelytokous parthenogenesis and its consequences on inbreeding in an ant. Heredity 96: 377-382.
34. PETRUNKEWITSCH, A., 1901 Die Richt ungskörper und ihr Schicksal im befruchteten und ubenfruchteten Bienenei. Zool. Jahrb. Abt. Anat. Ontog. Tiere. 14: 573-608.
35. RATNIEKS, F. L. W., and L. KELLER, 1998 Queen control of egg fertilization in the honey bee. Behav. Ecol. Sociobiol. 44: 57-61.
36. RIZET, G., and C. ENGELMANN, 1949 Contribution à l'étude génétique d'un Ascomycète tétrasporé: Podospora anserina (Ces.) Rehm. Rev. Cytol. Biol. Veg. 11: 201-304.
37. SANDER, K., 1985 Fertilization and egg cell activation in insects, pp. 409-430 in Biology of Fertilization, edited by C. B. METZ and A. MONROY. Academic Press, Orlando, FL.
38. SASAKI, K., and Y. OBARU, 2002 Egg activation and timing of sperm acceptance by an egg in honeybees (Apis mellifera L.). Insect Soc. 49: 234-240.
39. SEELEY, T. D., and D. R. TARPY, 2007 Queen promiscuity lowers disease within honeybee colonies. Proc. R. Soc. Lond. Ser. B 274: 67-72.
40. SOLIGNAC, M., D. VAUTRIN, A. LOISEAU, F. MOUGEL, E. BAUDRY et al., 2003 Five hundred and fifty microsatellite markers for the study of the honeybee (Apis mellifera L.) genome. Mol. Ecol. Notes 3: 307-311.
41. SOLIGNAC, M., F. MOUGEL, D. VAUTRIN, M. MONNEROT and J.-M. 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.
42. SUOMALAINEN, E., A. SAURA and J. LOKKI, 1987 Cytology and Evolution in Parthenogenesis. CRC Press, Boca Raton, FL.
43. TUCKER, K. W., 1958 Automictic parthenogenesis in the honey bee. Genetics 43: 299-316.
44. VERMA, L. R., and F. RUTTNER, 1983 Cytological analysis of the thelytokous parthenogenesis in the Cape honeybee (Apis mellifera capensis Escholtz). Apidologie 14: 47-57.
45. WALSH, P. S., D. A. METZGER and R. HIGUCHI, 1991 Chelex (R)100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10: 507.
46. WARMELO, D. S., 1912 South African fertile-worker bees and parthenogenesis. Agric. J. Union S. Afr. 3: 786-789.
47. WINSTON, M. L., 1987 The Biology of the Honey Bee. Harvard University Press, Cambridge, MA.
48. WOYKE, J., 1963 What happens to diploid drone larvae in a honeybee colony? J. Apic. Res. 2: 73-75.
49. YU, R., and S. W. OMHOLT, 1999 Early developmental processes in the fertilized honeybee (Apis mellifera) oocyte. J. Insect Physiol. 45: 763-767.