The genetic basis of transgressive ovary size in honeybee workers

Genetics

Volumn 183, Issue 2, 2009, Pages 693-707

  Linksvayer, Timothy A ^a   Rueppell, Olav ^b   Siegel, Adam ^a   Kaftanoglu, Osman ^a   Page Jr , Robert E ^a   Amdam, Gro V ^a,c  

^a ARIZONA STATE UNIVERSITY   (United States)

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

^c NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

ARTICLE; CHROMOSOME 11; CHROMOSOME 2; FEMALE; FORAGING BEHAVIOR; GENE FREQUENCY; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENE MAPPING; GENE STRUCTURE; GENETIC ASSOCIATION; HONEYBEE; INSECT GENETICS; MATING; NECTAR; NONHUMAN; ORGAN SIZE; OVARY; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; SOCIAL ENVIRONMENT; SPECIES DIFFERENCE;

ANIMALS; BEES; BEHAVIOR, ANIMAL; CARBOHYDRATES; CHROMOSOME MAPPING; CROSSES, GENETIC; FEMALE; GENES, INSECT; GENOME, INSECT; LOD SCORE; MALE; NECTAR; OVARY; PHENOTYPE; QUANTITATIVE TRAIT LOCI; REPRODUCTION;

APIS MELLIFERA; APOIDEA; HEXAPODA;

EID: 70649111377     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.109.105452     Document Type: Article

References (97)

1. ALLSOPP, M. H., J. N. M. CALIS and W. J. BOOT, 2003 Differential feeding of worker larvae affects caste characters in the Cape honeybee, Apis mellifera capensis. Behav. Ecol. Sociobiol. 54: 555-561.
2. AMDAM, G. V., K. NORBERG, M. K. FONDRK and R. E. PAGE, 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.
3. AMDAM, G. V., A. CSONDES, M. K. FONDRK and R. E. PAGE, 2006 Complex social behaviour derived from maternal reproductive traits. Nature 439: 76-78.
4. AMDAM, G. V., K. E. IHLE and R. E. PAGE, 2009. Regulation of honey bee (Apis mellifera) life histories by vitellogenin, in Hormones, Brain and Behavior, Ed 2, edited by S. FAHRBACH. Elsevier, San Diego, CA (in press).
5. ANDERSON, K. E., T. A. LINKSVAYER and C. R. SMITH, 2008 The causes and consequences of genetic caste determination in ants (Hymenoptera: Formicidae). Myrmecol. News 11: 119-132.
6. BARCHUK, A. R., A. S. CRISTINO, R. KUCHARSKI, L. F. COSTA, Z. L. SIMOES et al., 2007 Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. BMC Dev. Biol. 7: 70.
7. BEEKMAN, M., J. N. M. CALIS and W. J. BOOT, 2000 Parasitic honeybees get royal treatment. Nature 404: 723.
8. BEETSMA, J., 1985 Feeding-behavior of nurse bees, larval food composition and caste differentiation in the honey bee (Apis mellifera L). Fortschritte der Zoologie 31: 407-410.
9. BENDER, L. B., P. J. KOOH and M. A. MUSKAVITCH, 1993 Complex function and expression of Delta during Drosophila oogenesis. Genetics 133: 967-978.
10. BERGLAND, A. O., A. GENISSEL, S. V. NUZHDIN and M. TATAR, 2008 Quantitative trait loci affecting phenotypic plasticity and the allometric relationship of ovariole number and thorax length in Drosophila melanogaster. Genetics 180: 567-582.
11. BEYE, M., I. GATTERMEIER, M. HASSELMANN, T. GEMPE, M. SCHIOETT et al., 2006 Exceptionally high levels of recombination across the honey bee genome. Genome Res. 16: 1339-1344.
12. CAKOUROS, D., T. J.DAISH, K.MILLS and S. KUMAR, 2004 An arginine-histone methyltransferase, CARMER, coordinates ecdysone-mediated apoptosis in Drosophila cells. J. Biol. Chem. 279: 18467-18471.
13. CAPELLA, I. C. S., and K. HARTFELDER, 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.
14. CAPELLA, I. C. S., and K. HARTFELDER, 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.
15. CHAUD-NETTO, J., and O. C. BUENO, 1979 Number of ovarioles in workers of Apis mellifera adansonii and Apis mellifera ligustica: a comparative study. J. Apicultural Res. 18: 260-263.
16. CHINTAPALLI, V. R., J. WANG and J. A. T. DOW, 2007 Using FlyAtlas to identify better Drosophila models of human disease. Nat. Genet. 39: 715-720.
17. CHURCHILL, G. A., and R. W. DOERGE, 1994 Empirical threshold values for quantitative trait mapping. Genetics 138: 963-971. (Pubitemid 24337818)
18. DARVASI, A., and M. SOLLER, 1994 Selective DNA pooling for determination of linkage between a molecular marker and a quantitative trait locus. Genetics 138: 1365-1373.
19. DEDEJ, S., K. HARTFELDER, P. AUMEIER, P. ROSENKRANZ and W. ENGELS, 1998 Caste determination is a sequential process: effect of larval age at grafting on ovariole number, hind leg size and cephalic volatiles in the honey bee (Apis mellifera carnica). J. Apicultural Res. 37: 183-190. (Pubitemid 128374265)
20. DEGRANDI-HOFFMAN, G., M. CHAMBERS, J. E. HOOPER and S. S. SCHNEIDER, 2004 Description of an intermorph between a worker and queen in African honey bees Apis mellifera scutellata (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 97: 1299-1305.
21. DEKKERS, J. C. M., 2000 Quantitative trait locus mapping based on selective DNA pooling. J. Anim. Breed. Genet. 117: 1-16.
22. DINIZ, J. A. F., O. C. BUENO, J. CHAUDNETTO and O. MALASPINA, 1993 Heritability of the number of ovarioles in honey bee workers (Apis mellifera L) (Hym, Apidae). Revista Brasileira De Genetica 16: 917-921. (Pubitemid 24033145)
23. DUPUIS, J., and D. SIEGMUND, 1999 Statistical methods for mapping quantitative trait loci from a dense set of markers. Genetics 151: 373-386. (Pubitemid 29031902)
24. EVANS, J. D., and D. E. WHEELER, 2001 Gene expression and the evolution of insect polyphenisms. Bioessays 23: 62-68. (Pubitemid 32100502)
25. FALCONER, D. S., and T. F. C. MACKAY, 1996 Introduction to Quantitative Genetics, Ed. 4. Prentice Hall, New York.
26. FRANSSON, A., A. RUUSALA and P. ASPENSTROEM, 2003 Atypical Rho GTPases have roles in mitochondrial homeostasis and apoptosis. J. Biol. Chem. 278: 6495-6502.
27. GRANADINO, B., A. SANJUAN, P. SANTAMARIA and L. SANCHEZ, 1992 Evidence of a dual function in Fl(2)D, a gene needed for sex-lethal expression in Drosophila melanogaster. Genetics 130: 597-612.
28. GRENIER, A. M., and P. NARDON, 1994 The genetic control of ovariole number in Sitophilus oryzae L (Coleoptera, Curculionidae) is temperature sensitive. Genet. Select. Evol. 26: 413-430.
29. HARTFELDER, K., and W. ENGELS, 1998 Social insect polymorphism: hormonal regulation of plasticity in development and reproduction in the honeybee. Curr. Top. Dev. Biol. 40: 45-77.
30. HODIN, J., and L. M. RIDDIFORD, 2000 Different mechanisms underlie phenotypic plasticity and interspecific variation for a reproductive character in drosophilids (Insecta: Diptera). Evolution 54: 1638-1653.
31. HÖLLDOBLER, B., and E. O. WILSON, 1990 The Ants. Harvard University Press, Cambridge, MA.
32. HONEYBEE GENOME SEQUENCING CONSORTIUM, 2006 Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443: 931-949.
33. HOOGENDOORN, B., N. NORTON, G. KIROV, N. WILLIAMS, M. L. HAMSHERE et al., 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.
34. HUNT, G. J., and R. E. PAGE, 1995 Linkage map of the honey bee, Apis mellifera, based on RAPD markers. Genetics 139: 1371-1382.
35. HUNT, G. J., G. V. AMDAM, D. SCHLIPALIUS, C. EMORE, N. SARDESAI et al., 2007 Behavioral genomics of honeybee foraging and nest defense. Naturwissenschaften 94: 247-267.
36. HUNT, G. J., E. GUZMAN-NOVOA, M. K. FONDRK and R. E. PAGE, 1998 Quantitative trait loci for honey bee stinging behavior and body size. Genetics 148: 1203-1213.
37. HUNT, G. J., R. E. PAGE, M. K. FONDRK and C. J. DULLUM, 1995 Major quantitative trait loci affecting honey bee foraging behavior. Genetics 141: 1537-1545.
38. JORDAN, L. A., M. H. ALLSOPP, B. P. OLDROYD, T. C. WOSSLER and M. BEEKMAN, 2008 Cheating honeybee workers produce royal offspring. Proc. Biol. Sci. 275: 345-351.
39. KAPIL, R. P., 1962 Anatomy and histology of the female reproductive system of Apis indica F. (Hymenoptera, Apidae). Insectes Sociaux 9: 145-163.
40. KOROL, A., Z. FRENKEL, L. COHEN, E. LIPKIN and M. SOLLER, 2007 Fractioned DNA pooling: a new cost-effective strategy for fine mapping of quantitative trait loci. Genetics 176: 2611-2623. (Pubitemid 47360687)
41. KUCHARSKI, R., J. MALESZKA, S. FORET and R. MALESZKA, 2008 Nutritional control of reproductive status in honeybees via DNA methylation. Science 319: 1827-1830.
42. LANDER, E. S., and D. BOTSTEIN, 1989 Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121: 185-199.
43. LINKSVAYER, T. A., 2006 Direct, maternal, and sibsocial genetic effects on individual and colony traits in an ant. Evolution 60: 2552-2561.
44. LINKSVAYER, T. A., 2007 Ant species differences determined by epistasis between brood and worker genomes. PLoS ONE 2: e994.
45. LINKSVAYER, T. A., M. K. FONDRK and R. E. PAGE, JR., 2009 Honey bee social regulatory networks are shaped by colony-level selection. Am. Nat. 173: E99-E107.
46. LISI, S., I. MAZZON and K. WHITE, 2000 Diverse domains of THREAD/DIAP1 are required to inhibit apoptosis induced by REAPER and HID in Drosophila. Genetics 154: 669-678.
47. LUSCHNIG, S., J. KRAUSS, K. BOHMANN, I. DESJEUX and C. NUSSLEIN-VOLHARD, 2000 The Drosophila SHC adaptor protein is required for signaling by a subset of receptor tyrosine kinases. Mol. Cell 5: 231-241.
48. MACKAY, T. F. C., 2001 The genetic architecture of quantitative traits. Annu. Rev. Genet. 35: 303-339.
49. MAKERT, G. R., R. J. PAXTON and K. HARTFELDER, 2006 Ovariole number: a predictor of differential reproductive success among worker subfamilies in queenless honeybee (Apis mellifera L.) colonies. Behav. Ecol. Sociobiol. 60: 815-825.
50. MATOVA, N., S. MAHAJAN-MIKLOS, M. S. MOOSEKER and L. COOLEY, 1999 Drosophila quail, a villin-related protein, bundles actin filaments in apoptotic nurse cells. Development 126: 5645-5657.
51. MAZARS, A., F. LALLEMAND, C. PRUNIER, J. MARAIS, N. FERRAND et al., 2001 Evidence for a role of the JNK cascade in Smad7-mediated apoptosis. J. Biol. Chem. 276: 36797-36803.
52. MICHENER, C. D., 1974 The Social Behavior of the Bees. Harvard University Press, Cambridge, MA.
53. MICHENER, C. D., 2003 The Bees of the World. Johns Hopkins University Press, Baltimore, MD.
54. MICHENER, C. D., and D. J. BROTHERS, 1974 Were workers of eusocial Hymenoptera initially altruistic or oppressed? Proc. Natl. Acad, Sci. USA 71: 671-674.
55. MUNOZ-DESCALZO, S., J. TEROL and N. PARICIO, 2005 Cabut, a C2H2 zinc finger transcription factor, is required during Drosophila dorsal closure downstream of JNK signaling. Dev. Biol. 287: 168-179.
56. ORGOGOZO, V., K. W. BROMAN and D. L. STERN, 2006 High-resolution quantitative trait locus mapping reveals sign epistasis controlling ovariole number between two Drosophila species. Genetics 173: 197-205.
57. PAGE, R. E., and G. E. ROBINSON, 1994 Reproductive competition in queenless honey bee colonies (Apis mellifera L). Behav. Ecol. Sociobiol. 35: 99-107.
58. PANKIW, T., 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.
59. PANKIW, T., and R. E. PAGE, 2000 Response thresholds to sucrose predict foraging division of labor in honeybees. Behav. Ecol. Sociobiol. 47: 265-267.
60. PANKIW, T., K. D. WADDINGTON and R.E. PAGE, 2001 Modulation of sucrose response thresholds in honey bees (Apis mellifera L.): influence of genotype, feeding, and foraging experience. J. Comp. Physiol. A 187: 293-301.
61. PANKIW, T., M. NELSON, R.E. PAGE and M. K. FONDRK, 2004 The communal crop: modulation of sucrose response thresholds of pre-foraging honey bees with incoming nectar quality. Behav. Ecol. Sociobiol. 55: 286-292.
62. PATEL, A., M. K. FONDRK, O. KAFTANOGLU, C. EMORE, G. HUNT et al., 2007 The making of a queen: TOR pathway is a key player in diphenic caste development. PLoS ONE 2: e509.
63. RACHINSKY, A., and K. HARTFELDER, 1995 Caste development of honeybees (Apis mellifera): juvenile hormone turns on ecdysteroids. Naturwissenschaften 82: 378-379.
64. REGINATO, R. D., and C. CRUZ-LANDIM, 2001 Differentiation of the worker's ovary in Apis mellifera L. (Hymenoptera, Apidae) during life of the larvae. Invert. Reprod. Dev. 39: 127-134.
65. RICHARD, D. S., R. RYBCZYNSKI, T. G. WILSON, Y. WANG, M. L. WAYNE 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 chico(1) insulin signaling mutation is autonomous to the ovary. J. Insect Physiol. 51: 455-464.
66. RIESEBERG, L. H., M. A. ARCHER and R. K. WAYNE, 1999 Transgressive segregation, adaptation and speciation. Heredity 83: 363-372.
67. RODRIGUEZ, A., P. CHEN, H. OLIVER and J. M. ABRAMS, 2002 Unrestrained caspace-dependent cell death caused by loss of Diap1 function requires the Drosophila Apaf-1 homolog, Dark. EMBO J. 21: 2189-2197.
68. RUEPPELL, O., 2009 Characterization of quantitative trait loci for the age of first foraging in honey bee workers. Behav. Genet. 39: 541-553.
69. RUEPPELL, O., T. PANKIW and R. E. PAGE, JR., 2004 Pleiotropy, epistasis and new QTL: the genetic architecture of honey bee foraging behavior. J. Hered. 95: 481-491.
70. RUTTNER, F., and B. HESSE, 1981 Specific differences in the development of ovaries and egg-laying of queenless workers of several races of the honeybee, Apis mellifera L. Apidologie 12: 159-183.
71. SEELEY, T. D., 1997 Honey bee colonies are group-level adaptive units. Am. Nat. 150: S22-S41.
72. SHERMAN, P. W., E. A. LACEY, H. K. REEVE and L. KELLER, 1995 The eusociality continuum. Behav. Ecol. 6: 102-108.
73. SHIRAIWA, T., E. NITASAKA and T. YAMAZAKI, 2000 Geko, a novel gene involved in olfaction in Drosophila melanogaster. J. Neurogenet. 14: 145-164. (Pubitemid 30643400)
74. 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.
75. STARMER, W. T., M. POLAK, L. L. WOLF and J. S. F. BARKER, 1998 Reproductive characteristics of the flower breeding Drosophila hibisci bock (Drosophilidae) in eastern Australia: genetic and environmental determinants of ovariole number. Evolution 52: 806-815.
76. THULLER, R. H. C., O. MALASPINA, O. C. BUENO and J. CHAUD-NETTO, 1996 Number of ovarioles in workers descendent from crossings between Africanized and Italian honeybees (Apis mellifera L.): comparing stock, inbred and F1 colonies. Anais da Sociedade Entomologica do Brasil 25: 501-506.
77. THULLER, R. H. C., O. MALASPINA, O. C. BUENO and J. CHAUD-NETTO, 1998 Number of ovarioles in workers descendent from crossings between Africanized and Italian honeybees, Apis mellifera L.: comparison among backcrosses and ancestors colonies. Anais da Sociedade Entomologica do Brasil 27: 237-243.
78. TOMANCAK, P., A. BEATON, R. WEISZMANN, E. KWAN, S. SHU et al., 2002 Systematic determination of patterns of gene expression during Drosophila embryogenesis. Genome Biology 3: research0088.0081-0088.0014.
79. TSURUDA, J., G. V. AMDAM and R. E. PAGE, 2008 Sensory response system of social behavior tied to female reproductive traits. PLoS ONE 3: e3397.
80. TU, M. P., and M. TATAR, 2003 Juvenile diet restriction and the aging and reproduction of adult Drosophila melanogaster. Aging Cell 2: 327-333.
81. VELTHUIS, H. H., 1970 Ovarian development in Apis mellifera worker bees. Entomologia Experimentalis et Applicata 13: 377-394.
82. VELTHUIS, H. H. W., J. CLEMENT, R. A. MORSE and F. M. LAIGO, 1971 The ovaries of Apis dorsata from the Philippines. J. Apicultural Res. 10: 63-66.
83. WANG, J., K. J. KOEHLER and J. C. M. DEKKERS, 2007 Interval mapping of quantitative trait loci with selective DNA pooling data. Genet. Select. Evol. 39: 685-709.
84. WARD, E. J., H. R. SHCHERBATA, S.H. REYNOLDS, K. A. FISCHER, S. D. HATFIELD et al., 2006 Stem cells signal to the niche through the Notch pathway in the Drosophila ovary. Curr. Biol. 16: 2352-2358.
85. WAYNE, M. L., J. B. HACKETT, C. L. DILDA, S. V. NUZHDIN, E. G. PASYUKOVA et al., 2001 Quantitative trait locus mapping of fitness-related traits in Drosophila melanogaster. Genet. Res. 77: 107-116.
86. WAYNE, M. L., J. B. HACKETT and T. F. C. MACKAY, 1997 Quantitative genetics of ovariole number in Drosophila melanogaster. 1. Segregating variation and fitness. Evolution 51: 1156-1163.
87. WEAVER, N., 1957 Experiments on dimorphism in the female honey bee. J. Econ. Entomol. 50: 759-761.
88. WHEELER, D. E., 1986 Developmental and physiological determinants of caste in social Hymenoptera: evolutionary implications. Am. Nat. 128: 13-34.
89. WHEELER, D. E., N. BUCK and J. D. EVANS, 2006 Expression of insulin pathway genes during the period of caste determination in the honey bee, Apis mellifera. Insect Mol. Biol. 15: 597-602.
90. WHITFIELD, C. W., S. K. BEHURA, S. H. BERLOCHER, A. G. CLARK, J. S. JOHNSTON et al., 2006a Thrice out of Africa: ancient and recent expansions of the honey bee, Apis mellifera. Science 314: 642-645.
91. WHITFIELD, C. W., Y. BEN-SHAHAR, C. BRILLET, I. LEONCINI, D. CRAUSER et al., 2006b Genomic dissection of behavioral maturation in the honey bee. Proc. Natl. Acad. Sci. USA 103: 16068-16075.
92. WINSTON, M. L., 1987 The Biology of the Honey Bee. Harvard University Press, Cambridge, MA.
93. WINSTON, M. L., O. R. TAYLOR and G. W. OTIS, 1983 Some differences between temperate European and tropical African and South American honeybees. Bee World 64: 12-21.
94. WOYKE, J., 1971 Correlations between the age at which honeybee brood was grafted, characteristics of the resultant queens and result of insemination. J. Apicultural Res. 10: 45-55.
95. XU, S. Z., 2003 Theoretical basis of the Beavis effect. Genetics 165: 2259-2268.
96. ZAYED, A., and C. W. WHITFIELD, 2008 A genome-wide signature of positive selection in ancient and recent invasive expansions of the honey bee Apis mellifera. Proc. Natl. Acad. Sci. USA 105: 3421-3426.
97. ZHAO, T., T. GU, H. C. RICE, K. L. MCADAMS, K. M. ROARK et al., 2008 A Drosophila gain-of-function screen for candidate genes involved in steroid-dependent neuroendocrine cell remodeling. Genetics 178: 883-901.