Experimentally increased group diversity improves disease resistance in an ant species

Ecology Letters

Volumn 11, Issue 7, 2008, Pages 682-689

  Reber, Anabelle ^a   Castella, Grégoire ^a   Christe, Philippe ^a   Chapuisat, Michel ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Formica selysi; Genetic diversity; Metarhizium anisopliae; Parasite resistance; Queen number; Social evolution; Social immunity; Social insects

Indexed keywords

MICROSATELLITE DNA;

ANT; DEFENSE MECHANISM; DISEASE RESISTANCE; EVOLUTION; EXPERIMENTAL STUDY; FUNGUS; GENETIC VARIATION; IMMUNITY; MONOGYNY; QUEEN; SOCIAL INSECT; SURVIVAL;

ANIMAL; ANT; ARTICLE; FEMALE; GENETIC VARIABILITY; GENETICS; GENOTYPE; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; MALE; METARHIZIUM; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; ANTS; FEMALE; GENOTYPE; HOST-PATHOGEN INTERACTIONS; IMMUNITY, NATURAL; MALE; METARHIZIUM; MICROSATELLITE REPEATS; VARIATION (GENETICS);

FORMICA SELYSI; HEXAPODA; METARHIZIUM ANISOPLIAE;

EID: 44649179231     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/j.1461-0248.2008.01177.x     Document Type: Article

References (48)

1. Anderson, R.M. May, R.M. (1985). Vaccination and herd immunity to infectious diseases. Nature, 318, 323 329.
2. van Baalen, M. Beekman, M. (2006). The costs and benefits of genetic heterogeneity in resistance against parasites in social insects. Am. Nat., 167, 568 577.
3. Baer, B. Schmid-Hempel, P. (1999). Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature, 397, 151 154.
4. Baer, B. Schmid-Hempel, P. (2001). Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris. Evolution, 55, 1639 1643.
5. Boomsma, J.J., Schmid-Hempel, P. Hughes, W.O.H. (2005). Life histories and parasite pressure across the major groups of social insects. In : Insect Evolutionary Ecology (eds Fellowes, M.D.E., Holloway, G.J. Rolff, J.). CABI Publishing, Wallingford, pp. 139 175.
6. Bourke, A.F.G. Franks, N.R. (1995). Social Evolution in Ants. Princeton University Press, Princeton, NJ.
7. Brown, M.J.F. Schmid-Hempel, P. (2003). The evolution of female multiple mating in social hymenoptera. Evolution, 57, 2067 2081.
8. Calleri, D.V., Rosengaus, R.B. Traniello, J.F.A. (2005). Disease and colony foundation in the dampwood termite Zootermopsis angusticollis: the survival advantage of nestmate pairs. Naturwissenschaften, 92, 300 304.
9. Calleri, D.V., Reid, E.M., Rosengaus, R.B., Vargo, E.L. Traniello, J.F.A. (2006). Inbreeding and disease resistance in a social insect: effects of heterozygosity on immunocompetence in the termite Zootermopsis angusticollis. Proc. R Soc. Lond. B, 273, 2633 2640.
10. Chapuisat, M., Bocherens, S. Rosset, H. (2004). Variable queen number in ant colonies: no impact on queen turnover, inbreeding, and population genetic differentiation in the ant Formica selysi. Evolution, 58, 1064 1072.
11. Chapuisat, M., Oppliger, A., Magliano, P. Christe, P. (2007). Wood ants use resin to protect themselves against pathogens. Proc. R Soc. Lond. B, 274, 2013 2017.
12. Crozier, R.H. Fjerdingstad, E.J. (2001). Polyandry in social Hymenoptera - disunity in diversity? Ann. Zool. Fenn., 38, 267 285.
13. Crozier, R.H. Page, R.E. (1985). On being the right size: male contributions and multiple mating in social Hymenoptera. Behav. Ecol. Sociobiol., 18, 105 115.
14. Crozier, R.H. Pamilo, P. (1996). Evolution of Social Insect Colonies: Sex Allocation and kin Selection. Oxford University Press, Oxford.
15. Curran, J., Driver, F., Ballard, J.W.O. Milner, R.J. (1994). Phylogeny of Metarhizium: analysis of ribosomal DNA-sequence data. Mycol. Res., 98, 547 552.
16. Fernandez-Marin, H., Zimmerman, J.K., Rehner, S.A. Wcislo, W.T. (2006). Active use of the metapleural glands by ants in controlling fungal infection. Proc. R Soc. Lond. B, 273, 1689 1695.
17. Hamilton, W.D. (1964). The genetical evolution of social behaviour. II. J. Theor. Biol., 7, 17 52.
18. Hamilton, W.D. (1987). Kinship, recognition, disease, and intelligence: constraints of social evolution. In : Animal Societies: Theories and Facts (eds Ito, Y., Brown, J.L. Kikkawa, J.). Japan Sci. Soc. Press, Tokyo, pp. 81 102.
19. Hughes, W.O.H. Boomsma, J.J. (2004). Genetic diversity and disease resistance in leaf-cutting ant societies. Evolution, 58, 1251 1260.
20. Hughes, W.O.H. Boomsma, J.J. (2006). Does genetic diversity hinder parasite evolution in social insect colonies? J. Evol. Biol., 19, 132 143.
21. 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.
22. Hughes, W.O.H., Thomsen, L., Eilenberg, J. Boomsma, J.J. (2004). Diversity of entomopathogenic fungi near leaf-cutting ant nests in a neotropical forest, with particular reference to Metarhizium anisopliae var. anisopliae. J. Invertebr. Pathol., 85, 46 53.
23. 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 rubropilosa. Entomol. Exp. Appl., 93, 51 61.
24. Keller, S., Kessler, P. Schweizer, C. (2003). Distribution of insect pathogenic soil fungi in Switzerland with special reference to Beauveria brongniartii and Metarhizium anisopliae. Biocontrol, 48, 307 319.
25. Kraus, B. Page, R.E. (1998). Parasites, pathogens, and polyandry in social insects. Am. Nat., 151, 383 391.
26. Lacey, L.A. (1997). Manual of Techniques in Insect Pathology. Academic Press, San Diego.
27. Lewis, K. (1998). Pathogen resistance as the origin of kin altruism. J. Theor. Biol., 193, 359 363.
28. Liersch, S. Schmid-Hempel, P. (1998). Genetic variation within social insect colonies reduces parasite load. Proc. R Soc. Lond. B, 265, 221 225.
29. Oldroyd, B.P. Fewell, J.H. (2007). Genetic diversity promotes homeostasis in insect colonies. Trends Ecol. Evol., 22, 408 413.
30. Palmer, K.A. 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. Naturwissenschaften, 90, 265 268.
31. Robinson, G.E. (1992). Regulation of division of labor in insect societies. Annu. Rev. Entomol., 37, 637 665.
32. Rosengaus, R.B. Traniello, J.F.A. (1993). Disease risk as a cost of outbreeding in the termite Zootermopsis angusticollis. Proc. Natl Acad. Sci. USA, 90, 6641 6645.
33. Rosengaus, R.B. Traniello, J.F.A. (2001). Disease susceptibility and the adaptive nature of colony demography in the dampwood termite Zootermopsis angusticollis. Behav. Ecol. Sociobiol., 50, 546 556.
34. Rosengaus, R.B., Maxmen, A.B., Coates, L.E. Traniello, J.F.A. (1998). Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera : Termopsidae). Behav. Ecol. Sociobiol., 44, 125 134.
35. Rosengaus, R.B., Lefebvre, M.L. Traniello, J.F.A. (2000). Inhibition of fungal spore germination by Nasutitermes: Evidence for a possible antiseptic role of soldier defensive secretions. J. Chem. Ecol., 26, 21 39.
36. Rosset, H. Chapuisat, M. (2006). Sex allocation conflict in ants: when the queen rules. Curr. Biol., 16, 328 331.
37. Rosset, H. Chapuisat, M. (2007). Alternative life-histories in a socially polymorphic ant. Evol. Ecol., 21, 577 588.
38. Rosset, H., Schwander, T. Chapuisat, M. (2007). Nestmate recognition and levels of aggression are not altered by changes in genetic diversity in a socially polymorphic ant. Anim. Behav., 74, 951 956.
39. Schmid-Hempel, P. Crozier, R.H. (1999). Polyandry versus polygyny versus parasites. Philos. Trans. R Soc. Lond. B, 354, 507 515.
40. Schwander, T., Rosset, H. Chapuisat, M. (2005). Division of labour and worker size polymorphism in ant colonies: the impact of social and genetic factors. Behav. Ecol. Sociobiol., 59, 215 221.
41. Seeley, T.D. Tarpy, D.R. (2007). Queen promiscuity lowers disease within honeybee colonies. Proc. R Soc. Lond. B, 274, 67 72.
42. Sherman, P.W., Seeley, T.D. Reeve, H.K. (1988). Parasites, pathogens, and polyandry in social Hymenoptera. Am. Nat., 131, 602 610.
43. Shykoff, J.A. Schmid-Hempel, P. (1991). Parasites and the advantage of genetic variability within social insect colonies. Proc. R Soc. Lond. B, 243, 55 58.
44. Strassmann, J. (2001). The rarity of multiple mating by females in the social Hymenoptera. Ins. Soc., 48, 1 13.
45. Tarpy, D.R. (2003). Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc. R Soc. Lond. B, 270, 99 103.
46. Tarpy, D.R. Seeley, T.D. (2006). Lower disease infections in honeybee (Apis mellifera) colonies headed by polyandrous vs monandrous queens. Naturwissenschaften, 93, 195 199.
47. Thorne, B.L. Traniello, J.F.A. (2003). Comparative social biology of basal taxa of ants and termites. Annu. Rev. Entomol., 48, 283 306.
48. Traniello, J.F.A., Rosengaus, R.B. Savoie, K. (2002). The development of immunity in a social insect: evidence for the group facilitation of disease resistance. Proc. Natl Acad. Sci. USA, 99, 6838 6842.