Caste-specific expression of genetic variation in the size of antibiotic-producing glands of leaf-cutting ants

Proceedings of the Royal Society B: Biological Sciences

Volumn 277, Issue 1681, 2010, Pages 609-615

  Hughes, W O H ^a,b   Bot, A N M ^c   Boomsma, J J ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c AARHUS UNIVERSITY   (Denmark)

Author keywords

Castes; Genetic diversity; Heritability; Parasite resistance; Phenotypic plasticity

Indexed keywords

ALLOMETRY; ANT; ANTIBIOTICS; ANTIPARASITE DEFENSE; CASTE; ENVIRONMENTAL CONDITIONS; GENETIC VARIATION; HERITABILITY; PARASITE RESISTANCE; PHENOTYPIC PLASTICITY; SOCIAL INSECT;

ACROMYRMEX; ACROMYRMEX ECHINATIOR; ACROMYRMEX OCTOSPINOSUS; ATTA; HEXAPODA;

EID: 76249104955     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2009.1415     Document Type: Article

References (48)

1. Baer, B. & Schmid-Hempel, P. 2003 Bumblebee workers from different sire groups vary in susceptibility to parasite infection. Ecohgy Letters 6, 106-110. (doi:10.1046/ J.1461-0248.2003.00411.X) (Pubitemid 36463398)
2. Baer, B., Armitage, S. A. O. & Boomsma, J. J. 2006 Sperm storage induces an immunity cost in ants. Nature 441, 872-875. (doi:10.1038/nature04698) (Pubitemid 43910420)
3. Boomsma, J. J. & Ratnieks, F. L. W 1996 Paternity in eusocial Hymenoptera. Phil. Trans. R. Soc. Lond. B 351, 947-975. (doi:10.1098/rstb.l996. 0087)
4. Bot, A. N. M. & Boomsma, J. J. 1996 Variable metapleural gland size-allometries in Acromyrmex leafcutter ants (Hymenoptera: Formicidae). J. Kansas Entomol. Soc. 69, 375-383.
5. Bot, A. N. M., Obermayer, M. L., Holldobler, B. & Boomsma, J. J. 2001 Functional morphology of the metapleural gland in the leaf-cutting ant Acromyrmex octospinosus. Insectes Soc. 48, 63-66. (doi:10.1007/ PL00001747)
6. Bot, A. N. M., Ortius-Lechner, D., Finster, K., Maile, R. & Boomsma, J. J. 2002 Variable sensitivity of fungi and bacteria to compounds produced by the metapleural glands of leaf-cutting ants. Insectes Soc. 49, 363-370. (doi: 10.1007/PL00012660) (Pubitemid 35374439)
7. Carius, H. J., Little, T. J. & Ebert, D. 2001 Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution 55, 1136-1145. (Pubitemid 32665223)
8. Decanini, L. I., Collins, A. M. & Evans, J. D. 2007 Variation and heritability in immune gene expression by diseased honeybees. J Hered. 98, 195-201. (doi:10.1093/jhered/ esm008)
9. Ebert, D. 1998 Evolution-experimental evolution of parasites. Science 282, 1432-1435. (doi:10.1126/science.282. 5393.1432)
10. Fernandez-Marin, H., Zimmerman, J., Rehner, S. & Wcislo, W. 2006 Active use of the metapleural glands by ants in controlling fungal infection. Proc. R. Soc. B 273, 1689-1695. (doi:10.1098/rspb.2006.3492) (Pubitemid 46931057)
11. Fernandez-Marin, H., Zimmerman, J. K., Nash, D. R., Boomsma, J. J. & Wcislo, W. T 2009 Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants. Proc. R. Soc. B 276, 2263-2269. (doi:10.1098/rspb.2009.0184)
12. Fisher, R. A. 1930 The genetical theory of natural selection. Oxford, UK: Clarendon Press.
13. Holldobler, B. & Wilson, E. O. 1990 The ants. Cambridge, MA: Belknap Press.
14. Hughes, W. O. H. & Boomsma, J. J. 2004 Genetic diversity and disease resistance in leaf-cutting ant societies. Evolution 58, 1251-1260. (Pubitemid 38826278)
15. Hughes, W. O. H. & Boomsma, J. J. 2006 Does genetic diversity hinder parasite evolution in social insect colonies? J Evol. Biol. 19, 132-143. (doi:10.1111/j.1420-9101. 2005.00979.x)
16. Hughes, W. O. H. & Boomsma, J. J. 2007 Genetic polymorphism in leaf-cutting ants is phenotypically plastic. Proc. R. Soc. B 274, 1625-1630. (doi:10.1098/rspb.2007. 0347)
17. Hughes, W. O. H. & Boomsma, J. J. 2008 Genetic royal cheats in leaf-cutting ant societies. Proc. Natl Acad. Sci. USA 105, 5150-5153. (doi:10.1073/pnas.0710262105)
18. Hughes, W. O. H., Eilenberg, J. & Boomsma, J. J. 2002 Trade-offs in group living: transmission and disease resistance in leaf-cutting ants. Proc. R. Soc. Lond. B 269, 1811-1819. (doi:10.1098/rspb.2002.2113) (Pubitemid 35015035)
19. Hughes, W. O. H., Sumner, S., Van Borm, S. & Boomsma, J. J. 2003 Worker caste polymorphism has a genetic basis in Acromyrmex leaf-cutting ants. Proc. Natl Acad. Sci. USA 100, 9394-9397. (doi:10.1073/pnas. 1633701100) (Pubitemid 37033939)
20. Hughes, W. O. H., Oldroyd, B. P., Beekman, M. & Ratnieks, F. L. W 2008a Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213-1216. (doi:10.1126/science.H56108) (Pubitemid 351929509)
21. Hughes, W. O. H., Pagliarini, R., Madsen, H. B., Dijkstra, M. J. & Boomsma, J. J. 2008b Antimicrobial defence shows an abrupt evolutionary transition in the fungusgrowing ants. Evolution 62, 1252-1257. (doi:10.1111/ J.1558-5646.2008.00347.X) (Pubitemid 351623934)
22. Jaccoud, D. B., Hughes, W. O. H. & Jackson, C. W. 1999 The epizootiology of a Metarhizium infection in mini-nests of the leaf-cutting ant Atta sexdens rubropihsa. Entomol. Exp. Appl. 93, 51-61. (doi: 10.1023/ A:1003830625680)
23. Kermarrec, A., Febvay, G. & Decharme, M. 1986 Protection of leaf-cutting ants from biohazards: is there a future for microbiological control? In Fire ants and leaf-cutting ants: biology and management (eds C. S. Lofgren & R. K. Vander Meer), pp. 338-355. Boulder, CO: Westview Press.
24. Kover, P. X. & Schaal, B. A. 2002 Genetic variation for disease resistance and tolerance among Arabidopsis thaliana accessions. Proc. Natl Acad. Sci. USA 99, 11 270-11 274. (doi:10.1073/pnas.l02288999)
25. Kraaijeveld, A. R. & Godfray, H. C. J. 1997 Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389, 278-280. (doi: 10.1038/38483)
26. Little, T. J. & Ebert, D. 1999 Associations between parasitism and host genotype in natural populations of Daphnia (Crustacea: Cladocera). J. Anim. Ecol. 68, 134-149. (doi:10.1046/j.l365-2656.1999.00271.x) (Pubitemid 29053587)
27. Little, T. J. & Ebert, D. 2000 The cause of parasitic infection in natural populations of Daphnia (Crustacea: Cladocera): the role of host genetics. Proc. R. Soc. Lond. B 267, 2037-2042. (doi:10.1098/rspb.2000.1246) (Pubitemid 30828827)
28. Little, T. J. & Ebert, D. 2001 Temporal patterns of genetic variation for resistance and infectivity in a Daphniamicroparasite system. Evolution 55, 1146-1152. (Pubitemid 32665224)
29. Navajas, M., Migeon, A., Alaux, C., Martin-Magniette, M. L., Robinson, G. E., Evans, J. D., Cros-Arteil, S., Crauser, D. & Le Conte, Y. 2008 Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection. BMC Genom. 9, 301. (doi:10.1186/1471-2164-9-301) (Pubitemid 351984741)
30. Ortius-Lechner, D., Gertsch, P. J. & Boomsma, J. J. 2000a Variable microsatellite loci for the leaf cutter ant Acromyrmex echinatior and their applicability to related species. Mol. Ecol 9, 114-116. (doi:10.1046/j.l365294X. 2000.00764-5.X) (Pubitemid 30115689)
31. Ortius-Lechner, D., Maile, R., Morgan, E. D. & Boomsma, J. J. 2000b Metapleural gland secretion of the leaf-cutter ant Acromyrmex octospinosus: new compounds and their functional significance. J. Chem. Ecol. 26, 1667-1683. (doi:10.1023/A:1005543030518) (Pubitemid 30491047)
32. Ortius-Lechner, D., Maile, R., Morgan, E. D., Petersen, H. C. & Boomsma, J. J. 2003 Lack of patriline-specific differences in chemical composition of the metapleural gland secretion in Acromyrmex octospinosus. Insectes Soc. 50, 113-119. (doi:10.1007/s00040-003-0640-l)
33. Oster, G. F. & Wilson, E. O. 1978 Caste and ecohgy in the social insects. Princeton, NJ: Princeton University Press.
34. Pigliucci, M. 2005 Evolution of phenotypic plasticity: where are we going now? Trends Ecol. Evol. 20, 481-486.
35. Poulsen, M., Bot, A. N. M., Currie, C. R. & Boomsma, J. J. 2002a Mutualistic bacteria and a possible trade-off between alternative defence mechanisms in Acromyrmex leaf-cutting ants. Insectes Soc. 49, 15-19. (doi:10.1007/ S00040-002-8271-8275) (Pubitemid 34290175)
36. Poulsen, M., Bot, A. N. M., Nielsen, M. G. & Boomsma, J. J. 20026 Experimental evidence for the costs and hygienic significance of the antibiotic metapleural gland secretion in leaf-cutting ants. Behav. Ecol. Sociobiol. 52, 151-157. (doi: 10.1007/S00265-002-0489-8)
37. Poulsen, M., Hughes, W. O. H. & Boomsma, J. J. 2006 Differential resistance and the importance of antibiotic production in Acromyrmex echinatior leaf-cutting ant castes towards the entomopathogenic fungus Aspergillus nomius. Insectes Soc. 53, 349-355. (doi: 10.1007/s00040006-0880-y)
38. Reeson, A. F., Wilson, K., Gunn, A., Hails, R. S. & Goulson, D. 1998 Baculovirus resistance in the noctuid Spodoptera exempta is phenotypically plastic and responds to population density. Proc. R. Soc. Lond. B 265, 1787-1791. (doi:10.1098/rspb.l998.0503) (Pubitemid 28451352)
39. Rolff, J. & Siva-Jothy, M. T 2003 Invertebrate ecological immunology. Science 301, 472-475. (doi:10.1126/ science. 1080623)
40. Spivak, M. & Reuter, G. S. 2001 Varroa destructor infestation in untreated honey bee (Hymenoptera: Apidae) colonies selected for hygienic behavior. J. Econ. Entomol. 94, 326-331. (Pubitemid 33749917)
41. Sumner, S., Hughes, W O. H. & Boomsma, J. J. 2003 Evidence for differential selection and potential adaptive evolution in the worker caste of an inquiline social parasite. Behav. Ecol. Sociobiol. 54, 256-263. (doi:10.1007/ S00265-003-0633-640)
42. Sumner, S., Hughes, W. O. H., Pedersen, J. S. & Boomsma, J. J. 2004 Ant parasite queens revert to mating singly. Nature 428, 35-36. (doi:10.1038/428035a)
43. Vijendravarma, R. K., Kraaijeveld, A. R. & Godfray, H. C. J. 2009 Experimental evolution shows Drosophila melanogaster resistance to a microsporidian pathogen has fitness costs. Evolution 63, 104-114. (doi:10.1111/ J.1558-5646.2008.00516.X)
44. Villesen, P., Murakami, T., Schultz, T. R. & Boomsma, J. J. 2002 Identifying the transition between single and multiple mating of queens in fungus-growing ants. Proc. R. Soc. Lond. B 269, 1541-1548. (doi:10.1098/ rspb.2002.2044)
45. Weber, N. A. 1972 Gardening ants: the attines. Mem. Am. Phil. Soc. 92, 1-146.
46. Wetterer, J. K. 1999 The ecology and evolution of worker size-distribution in leaf-cutting ants (Hymenoptera: Formicidae). Sociobiohgy 34, 119-144.
47. Wilson, E. O. 1980 Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta). I. The overall pattern in A. sexdens. Behav. Ecol. Sociobiol. 7, 143-156. (doi: 10.1007/BF00299520)
48. Wilson, K., Thomas, M. B., Blanford, S., Doggett, M., Simpson, S. J. & Moore, S. L. 2002 Coping with crowds: density-dependent disease resistance in desert locusts. Proc. Natl Acad. Sci. USA 99, 5471-5475. (doi:10.1073/pnas.082461999)