Intracolonial genetic variability in honeybee larval resistance to the chalkbrood and American foulbrood parasites

Insectes Sociaux

Volumn 56, Issue 3, 2009, Pages 233-240

  Invernizzi, C ^a   Penagaricano F ^a   Tomasco, I H ^a  

^a UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

Author keywords

Disease; Genetic diversity; Honeybees; Polyandry

Indexed keywords

EVOLUTIONARY BIOLOGY; FUNGUS; GENETIC VARIATION; HONEYBEE; LARVAL DEVELOPMENT; PARASITE; POLYANDRY;

APIS MELLIFERA; ASCOSPHAERA APIS; BACTERIA (MICROORGANISMS); FUNGI; HEXAPODA; HYMENOPTERA; PAENIBACILLUS; PAENIBACILLUS LARVAE;

EID: 76049085762     PISSN: 00201812     EISSN: 14209098     Source Type: Journal    
DOI: 10.1007/s00040-009-0016-2     Document Type: Article

References (71)

1. Baalen M. van and Beekman M. 2006. The costs and benefits of genetic heterogeneity in resistance against parasites in social insects. Am. Nat. 167: 568-577.
2. Baer B. and Schmid-Hempel P. 1999. Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature397: 151-154.
3. Baer B. and Schmid-Hempel P. 2001. Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris. Evolution55: 1639-1643.
4. Baer B. and Schmid-Hempel P. 2003. Bumblebee workers from different sire groups vary in susceptibility to parasite infection. Ecol. Lett. 6: 106-110.
5. Bailey L. and Ball B. V. 1991. Honey Bee Pathology. Academic Press, London. 208 pp.
6. Beekman M. and Ratnieks F. L. W. 2003. Power over reproduction in the social Hymenoptera. Phil. Trans. R. Soc. Lond. 358: 1741-1753.
7. Beekman M. and Oldroyd B. P. 2008. When workers disunite: intraspecific parasitism by eusocial bees. Annu. Rev. Entomol. 53: 19-37.
8. Boomsma J. J. and Grafen A. 1991. Colony-level sex ratio selection in the eusocial Hymenoptera. J. Evol. Biol. 3: 383-407.
9. Boomsma J. J. and Ratnieks F. L. W. 1996. Paternity in social Hymenoptera. Philos. Trans. R. Soc. Lond. B351: 947-975.
10. Cole B. J. and Wiernasz D. C. 1999. The selective advantage of low relatedness. Science285: 891-893.
11. Cole B. J. and Wiernasz D. C. 2000. Colony size and reproduction in the western harvester ant, Pogonomyrmex occidentalis. Insect. Soc. 47: 249-255.
12. Crozier R. H. and Page R. E. 1985. On being the right size: male contributions and multiple mating in social Hymenoptera. Behav. Ecol. Sociobiol. 18: 105-115.
13. Crozier R. H. and Pamilo P. 1996. Evolution of Social Insect Colonies: Sex Allocation and Kin Selection. Oxford University Press, Oxford. 306 pp.
14. Crozier R. H. and Fjerdingstad E. J. 2001. Polyandry in social Hymenoptera - disunity in diversity? Ann. Zool. Fenn. 38: 267-285.
15. Costa J. T. and Ross K. G. 2003. Fitness effects of group merging in a social insect. Proc. R. Soc. Lond. B270: 1697-1702.
16. Denny A. J., Franks N. R., Powell S. and Edwards K. J. 2004. Exceptionally high levels of multiple mating in an army ant. Naturwissenschaften91: 396-399.
17. Ebert D. and Hamilton W. D. 1996. Sex against virulence: the coevolution of parasitic diseases. Trends Ecol. Evol. 11: 79-82.
18. Estoup A., Solignac M. and Cournet J. M. 1994. Precise assessment of the number of patrilines and of genetic relatedness in honeybee colonies. Proc. R. Soc. Lond. B258: 1-7.
19. Evans J. D. and Armstrong T. N. 2006. Antagonistic interactions between honey bee bacterial symbionts and implications for disease. BMC Ecol. 6: 4.
20. Fjerdingstad E. J. and Boomsma J. J. 2000. Queen mating frequency and relatedness in young Atta sexdens colonies. Insect. Soc. 47: 354-356.
21. Fuchs S. and Schade V. 1994. Lower performance in honeybee colonies of uniform paternity. Apidologie25: 155-168.
22. Gilliam M., Taber S. III, Lorenz B. and Prest D. B. 1988. Factors affecting development of chalkbrood disease in colonies of honey bees, Apis mellifera, fed pollen contaminated with Ascosphaera apis. J. Invert. Pathol. 52: 314-325.
23. Goodisman M. A. D., Kovaks J. L. and Hoffman E. A. 2007. The significance of multiple mating in the social wasp Vespula maculifrons. Evolution61: 2260-2267.
24. Hamilton W. D. 1964. The genetical evolution of social behavior, I and II. J. Theor. Biol. 7: 1-52.
25. Hamilton W. D. 1972. Altruism and related phenomena, mainly in social insects. Annu. Rev. Ecol. Syst. 3: 193-232.
26. Hamilton W. D. 1987. Kinship, recognition, disease, and intelligence: constraints of social evolution. In: Animal Societies: Theory and Facts (Ito Y., Brown J. L. and Kikkawa J., Eds), Japanese Scientific Society Press, Tokyo. pp 81-102.
27. Hamilton W. D., Axelrod R. and Tanese R. 1990. Sexual reproduction as an adaptation to resist parasites (a review). Proc. Natl. Acad. Sci. USA87: 3566-3573.
28. Harati H. S. and Spivak M. 2001. Influence of colony genotypic composition on the performance of hygienic behaviour in the honeybee, Apis mellifera L. Anim. Behav. 62: 57-66.
29. Hughes W. O. H., Eilenberg J. and Boomsma J. J. 2002. Trade-offs in group living: transmission and disease resistance in leaf-cutting ants. Proc. R. Soc. Lond. B269: 1811-1819.
30. Hughes W. O. H. and Boomsma J. J. 2004. Genetic diversity and disease resistance in leaf-cutting ant societies. Evolution58: 1251-1260.
31. Hughes W. O. H. and Boomsma J. J. 2006. Does genetic diversity hinder parasite evolution in social insect colonies? J. Evol. Biol. 19: 132-143.
32. Hughes W. O. H., Oldroyd B. P., Beekman M. and Ratnieks F. L. W. 2008. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science320: 1213-1216.
33. Jennions M. D. and Petrie M. 2000. Why do females mate multiply? A review of the genetic benefits. Biol. Rev. 75: 21-64.
34. Keller L. and Revee H. K. 1994. Genetic variability, queen number, and polyandry in social Hymenoptera. Evolution48: 694-704.
35. Kraus B. and Page R. E. Jr. 1998. Parasites, pathogens, and polyandry in social insects. Am. Nat. 151: 383-391.
36. Kronauer D. J. C., Schöning C., Pedersen J. S., Boomsma J. J. and Gadau J. 2004. Extreme queen-mating frequency and colony fission in African army ants. Mol. Ecol. 13: 2381-2388.
37. Liersch S. and Schmid-Hempel P. 1998. Genetic variation within social insect colonies reduces parasite load. Proc. R. Soc. Lond. B265: 221-225.
38. Mattila H. R. and Seeley T. D. 2007. Genetic diversity in honey bee colonies enhances productivity and fitness. Science317: 362-364.
39. Maynard Smith J. 1971. What use is sex? J. Theor. Biol. 30: 319-335.
40. Miller S. A., Dikes D. D. and Polesky H. F. 1988. A simple salting out procedure for extracting DNA for human nucleated cells. Nucleic Acids Res. 16: 215.
41. Murakami T., Higashi S. and Windsor D. 2000. Mating frequency, colony size, polyethism and sex ratio in fungus-growing ants (Attini). Behav. Ecol. Sociobiol. 48: 276-284.
42. Neumann P. and Moritz R. F. A. 2000. Testing genetic variance hypotheses for the evolution of polyandry in the honeybee (Apis mellifera L.). Insect. Soc. 47: 271-279.
43. Oldroyd B. P., Rinderer T. E. and Buco S. M. 1992. Intra-colonial foraging specialism by honey bees (Apis mellifera). Behav. Ecol. Sociobiol. 30: 291-295.
44. Ortius-Lechner D., Maile R., Morgan E. D., Petersen H. C. and Boomsma J. J. 2003. Lack of patriline-specific differences in chemical composition of the metapleural gland secretion in Acromyrmex octospinosus. Insect. Soc. 50: 113-119.
45. Page R. E. 1986. Sperm utilization in social insects. Ann. Rev. Entomol. 31: 297-320.
46. Page R. E., Robinson G. E., Fondrk M. K. and Nasr M. E. 1995. Effects of worker genotypic diversity on honey bee colony development and behavior (Apis mellifera L.). Behav. Ecol. Sociobiol. 36: 387-396.
47. Palmer K. A. and Oldroyd B. P. 2000. Evolution of multiple mating in the genus Apis. Apidologie31: 235-248.
48. Palmer K. A. and Oldroyd B. P. 2003. Evidence for intra-colonial genetic variance in resistance to American foulbrood of honey bees (Apis mellifera): further support for the parasite/pathogen hypothesis for the evolution of polyandry. Naturwissenschaften90: 265-268.
49. Ratnieks F. L. W. 1988. Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am. Nat. 132: 217-236.
50. Ratnieks F. L. W., Foster K. R. and Wenseleers T. 2006. Conflict resolution in insect societies. Annu. Rev. Entomol. 51: 581-608.
51. Reber A., Castella G., Christe P. and Chapuisat M. 2008. Experimentally increased group diversity improves disease resistance in an ant species. Ecol. Lett. 11: 682-689.
52. Rehindt F. E., Gadau J., Strehl C. P. and Hölldobler B. 2004. Extremely high mating frequency in the Florida harvester ant (Pogonomyrmex badius). Behav. Ecol. Sociobiol. 56: 219-225.
53. Robinson G. E. and Page R. E. 1995. Genotypic constraints on plasticity for corpse removal in honey bee colonies. Anim. Behav. 49: 867-876.
54. Ross K. G. 1986. Kin selection and the problem of sperm utilization in social insects. Nature323: 798-800.
55. Rosset H., Keller L. and Chapuisat M. 2005. Experimental manipulation of colony genetic diversity had no effect on short-term task efficiency in the Argentine ant Linepithema humile. Behav. Ecol. Sociobiol. 58: 87-98.
56. Sanguinetti C. J., Días Neto E., Simpson A. J. 1994. Rapid silver staining and recovery of PCR products separated on polyacrylamide gels. Biotechniques17: 914-921.
57. Schmid-Hempel P. 1994. Infection and colony variability in social insects. Philos. Trans. R. Soc. Lond. B346: 313-321.
58. Schmid-Hempel P. 1998. Parasites in Social Insects. Princeton University Press,. Princeton, NJ. 392 pp.
59. Schmid-Hempel P. and Crozier R. H. 1999. Polyandry versus polygyny versus parasites. Philos. Trans. R. Soc. Lond. B354: 507-515.
60. Seeley T. D. and Tarpy D. R. 2007. Queen promiscuity lowers disease within honeybee colonies. Proc. R. Soc. Lond. B274: 67-72.
61. Sherman P. W., Seeley T. D. and Reeve H. K. 1988. Parasites, pathogens, and polyandry in social Hymenoptera. Am. Nat. 131: 602-610.
62. Sherman P. W., Seeley T. D. and Reeve H. K. 1998. Parasites, pathogens, and polyandry in honey bees. Am. Nat. 151: 392-396.
63. Shykoff J. A. and Schmid-Hempel P. 1991. Parasites and the advantage of genetic variability within social insect colonies. Proc. R. Soc. Lond. B243: 55-58.
64. Strassmann J. 2001. The rarity of multiple mating by females in the social Hymenoptera. Insect. Soc. 48: 1-13.
65. Sumner S., Hughes W. O. H., Pedersen J. S. and Boomsma J. J. 2004. Ant parasite queens revert to mating singly. Nature428: 35-36.
66. Sundström L. 1994. Sex ratio bias, relatedness asymmetry and queen mating frequency in ants. Nature367: 266-268.
67. Sundström L. and Ratnieks F. L. W. 1998. Sex ratio conflicts, mating frequency, and queen fitness in the ant Formica truncorum. Behav. Ecol. 9: 116-121.
68. Tarpy D. R. 2003. Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc. R. Soc. Lond. B270: 99-103.
69. Tarpy D. R. and Seeley T. D. 2006. Lower disease infections in honeybee (Apis mellifera) colonies headed by polyandrous vs. monoandrous queen. Naturwissenschaften93: 195-199.
70. Trivers R. L. and Hare H. 1976. Haplodiploidy and the evolution of social insects. Science191: 249-263.
71. Wiernasz D. C., Perroni C. L. and Cole B. J. 2004. Polyandry and fitness in the western harvester ant, Pogonomyrmex occidentalis. Mol. Ecol. 13: 1601-1606.