Reproductive conflicts affect labor and immune defense in the queenless ant Diacamma sp. "nilgiri"

Evolution

Volumn 62, Issue 1, 2008, Pages 123-134

  Bocher, Aurélie ^a   Doums, Claudie ^b   Millot, Laurence ^a   Tirard, Claire ^a  

^a Laboratoire de Parasitologie Evolutive CNRS UMR 7103 UFR 927   (France)

^b UPMC University Paris 06   (France)

Author keywords

Aggressions; Antibacterial response; Cost of conflicts; Immunocompetence; Immunosuppression; Regulation of reproduction; Stress

Indexed keywords

AGGRESSION; ANT; DEFENSE MECHANISM; FITNESS; IMMUNE RESPONSE; IMMUNOCOMPETENCE; REPRODUCTION; REPRODUCTIVE STRATEGY;

AGGRESSION; ANIMAL; ANIMAL BEHAVIOR; ANT; ARTICLE; ESCHERICHIA COLI; GENETIC SELECTION; MICROBIOLOGY; PHYSIOLOGY; REPRODUCTION;

AGGRESSION; ANIMALS; ANTS; BEHAVIOR, ANIMAL; ESCHERICHIA COLI; REPRODUCTION; SELECTION (GENETICS);

BACTERIA (MICROORGANISMS); DIACAMMA; ESCHERICHIA COLI; FORMICIDAE; HYMENOPTERA;

EID: 37749013433     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2007.00273.x     Document Type: Article

References (77)

1. Adamo, S. A. 2004. How should behavioural ecologists interpret measurements of immunity Anim. Behav. 68 : 1443 1449.
2. Adamo, S. A., M. Jensen, and M. Younger. 2001. Changes in lifetime immunocompetence in male and female Gryllus texensis (formerly G. integer): trade-offs between immunity and reproduction. Anim. Behav. 62 : 417 425.
3. Ahtiainen, J. J., R. V. Alatalo, R. Kortet, and M. J. Rantala. 2006. Immune function, dominance and mating success in drumming amle wolf spiders Hygrolycosa rubrofasciata. Behav. Ecol. Sociobiol. 60 : 826 832.
4. Apanius, V. 1998. Stress and immune response. Pp. 133 154 in A. P. Møller, M. Milinski and P. J. B. Slater, eds. Stress and behavior. Academic Press, San Diego, CA.
5. Baer, B., S. A. O. Armitage, and J. J. Boomsma. 2006. Sperm storage induces an immunity cost in ants. Nature 441 : 872 875.
6. Barnes, A. I., and M. T. Siva-Jothy. 2000. Density-dependent prophylaxis in the mealworm beetle Tenebrio molitor L. (Coleoptera: Tenebrionidae): cuticular melanization is an indicator of investment in immunity. Proc. R. Soc. Biol. Sci. B 267 : 177 182.
7. Baudry, E., C. Peeters, L. Brazier, M. Veuille, and C. Doums. 2003. Shift in the behaviours regulating monogyny is associated with high genetic differentiation in the queenless ant Diacamma ceylonense. Ins. Soc. 50 : 390 397.
8. Bourke, A. F. G., and G. L. Chan. 1999. Queen-worker conflict over sexual production and colony maintenance in perennial social insects. Am. Nat. 154 : 417 426.
9. Bourke, A. F. G., and N. R. Franks. 1995. Social evolution in ants. Princeton Univ. Press, Princeton, NJ.
10. Brey, P. T., W. Lee, M. Yamakawa, Y. Koizumi, S. Perrot, M. François, and M. Ashida. 1993. Role of the integument in insect immunity: epicuticular abrasion and induction of cecropin synthesis in cuticular epithelial cells. Proc. Natl. Acad. Sci. USA 90 : 6275 6279.
11. Calleri, D. V., R. B. Rosengaus, and J. F. A. Traniello. 2007. Immunity and reproduction during colony foundation in the dampwood termite, Zootermopsis angusticollis. Physiol. Entomol. 32 : 136 142.
12. Choe, J., and D. Perlman. 1997. Social conflict and cooperation among founding queens in ants (Hymenoptera: Formicidae). Pp. 392 406 in J. Choe and B. Crespi, eds. The evolution of social behavior in insects and arachnids. Cambridge Univ. Press, Cambridge.
13. Clarke, F. M., and C. G. Faulkes. 1997. Dominance and queen succession in captive colonies of the eusocial naked mole-rat, Heterocephalus glaber. Proc. R. Soc. Lond. B 264 : 993 1000.
14. Cole, B. 1986. The social Behaviour of Leptothorax allardycei (Hymenoptera, formicidae): time budgets and the evolution of worker reproduction. Behav. Ecol. Sociobiol. 18 : 165 173.
15. Creel, S. 2001. Social dominance and stress hormones. Trends. Ecol. Evol. 16 : 491 497.
16. Creel, S. 2005. Dominance, aggression, and glucocorticoid levels in social carnivores. J. Mammal. 86 : 255 264.
17. Crozier, R. H., and P. Pamilo. 1996. Evolution of social insect colonies. Oxford Univ. Press, Oxford.
18. Cuvillier-Hot, V., A. Lenoir, R. Crewe, C. Malosse, and C. Peeters. 2004a. Fertility signaling and reproductive skew in queenless ants. Anim. Behav. 68 : 1209 1219.
19. Cuvillier-Hot, V., A. Lenoir, and C. Peeters. 2004b. Reproductive monopoly enforce by sterile police workers in queenless ant. Behav. Ecol. 15 : 970 975.
20. Emlen, S. T. 1995. An evolutionary theory of the family. Proc. Natl. Acad. Sci. USA 92 : 8092 8099.
21. Endler, A., J. Liebig, T. Schmitt, J. E. Parker, G. R. Jones, P. Schreier, and B. Holldobler. 2004. Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect. Proc. Natl. Acad. Sci. USA 101 : 2945 2950.
22. Evans, J. D., and J. S. Pettis. 2005. Colony-level impacts of immune responsiveness in honey bees, Apis mellifera. Evolution 59 : 2270 2274.
23. Field, J., A. Cronin, and C. Bridge. 2006. Future fitness and helping in social queues. Nature 441 : 214 217.
24. Foster, R. L., A. Brunskill, D. Verdirame, and S. O'Donnell. 2004. Reproductive physiology, dominance interactions, and division of labour among bumble bee workers. Physiol. Entomol. 29 : 327 334.
25. Fukumoto, Y., T. Abe, and A. Taki. 1989. A novel form of colony organization in the "queenless" ant Diacamma rugosum. Physiol. Ecol. Japan 26 : 55 61.
26. Gadagkar, R. 1991. Belongaster, Mischocyttarus, Parapolybia, and independant-founding Ropalidia. Pp. 149 190 in K. G. R. R. W. Matthews, ed. The social biology of wasps. Cornell Univ. Press, Ithaca, New York.
27. Gillespie, J., M. R. Kanost, and T. Trenczeck. 1997. Biological mediators of insect immunity. Annu. Rev. Entomol. 42 : 611 643.
28. Gobin, B., J. Heinze, M. Strätz, and F. Roces. 2003. The energetic cost of reproductive conflicts in the ant Pachycondyla obscuricornis. J. Ins. Physiol. 49 : 747 752.
29. Gorman, M. J., and S. M. Paskewitz. 2000. Persistance of infection in mosquitoes injected with bacteria. J. Invert. Pathol. 75 : 296 297.
30. Goymann, W., and J. C. Wingfield. 2004. Allostatic load, social status and stress hormones: the costs of social status matter. Anim. Behav. 67 : 591 602.
31. Hannonen, M., M. Sledge, S. Turillazzi, and L. Sundstrom. 2002. Queen reproduction, chemical signaling and worker behaviour in polygyne colonies of the ant Formica fusca. Anim. Behav. 64 : 477 485.
32. Hawley, D., K. Lindström, and M. Wikelski. 2006. Experimentally increased social competition compromised humoral responses in house finches. Hormone Behav. 49 : 417 424.
33. Hawley, D. M., C. S. Jennelle, K. V. Sydenstricker, and A. A. Dhondt. 2007. Pathogen resistance and immunocompetence covary with social status in house finches (Carpodacus mexicanus). Funct. Ecol. 21 : 520 527.
34. Heinze, J., B. Holldobler, and C. Peeters. 1994. Conflict and cooperation in ant societies. Naturwissenschaften 81 : 489 497.
35. Karpakakunjaram, V., P. Nair, T. Varghese, G. Royappa, M. Kolatkar, and R. Gadagkar. 2003. Contributions to the biology of the queenless ponerine ant Diacamma ceylonense emery (Formicidae). J. Bombay Nat. Hist. Soc. 100 : 533 543.
36. Keller, L., and E. L. Vargo. 1993. Reproductive structure and reproductive roles in colonies of eusocial insects. Pp. 16 44 in L. Keller, ed. Queen Number and Sociality in Insects. Oxford Univ. Press, Oxford.
37. Koskimäki, J., M. J. Rantala, J. Taskinen, K. Tynkkynen, and J. Suhonen. 2004. Immunocompetence and resource holding potential in the damselfly, Calopteryx virgo L. Behav. Ecol. 15 : 169 173.
38. Lackie, A. M. 1988. Haemocyte behaviour. Adv. Insect Physiol. 21 : 85 178.
39. Lacoste, A., S. K. Malham, A. Cueff, F. Gélébart, and S. A. Poulet. 2001a. Evidence for a form of adrenergic response to stress in the oyster Crassostrea gigas. J. Exp. Biol. 204 : 1247 1255.
40. Lacoste, A., S. K. Malham, A. Cueff, and S. A. Poulet. 2001b. Stress-induced Catecholamines changes in the haemolymph of the oyster Crassostrea gigas. Gen. Comp. Endocrinol. 122 : 181 188.
41. Lacoste, A., S. K. Malham, F. Gélébart, A. Cueff, and S. A. Poulet. 2002. Stress-induced immune changes in the oyster Crassostrea gigas. Dev. Comp. Immunol. 26 : 1 9.
42. Le Moullac, G., C. Soyez, D. Saulnier, D. Ansquer, J. C. Avarre, and P. Levy. 1998. Effect of hypoxic stress on the immune response and the resistance to vibriosis of the shrimp Penaeus stylirostris. Fish Shellfish Immunol. 8 : 621 629.
43. Lochmiller, R. L., and C. Deerenberg. 2000. Trade-offs in evolutionary immunology: just what is the cost of immunity Oikos 88 : 87 98.
44. Malham, S. K., A. Lacoste, F. Gélébart, A. Cueff, and S. A. Poulet. 2003. Evidence for a direct link between stress and immunity in the mollusc Haliotis tuberculata. J. Exp. Zool. A 295A : 136 144.
45. Mock, D. W., and G. A. Parker. 1997. The evolution of sibling rivalry. Oxford Univ. Press, Oxford.
46. Monnin, T., and C. Peeters. 1999. Dominance hierarchy and reproductive conflicts among subordinates in a monogynous queenless ant. Behav. Ecol. 10 : 323 332.
47. Monnin, T., and F. L. W. Ratnieks. 1999. Reproduction versus work in queenless ants: when to join a hierarchy of hopeful reproductives Behav. Ecol. Sociobiol. 46 : 413 422.
48. Monnin, T., C. Malosse, and C. Peeters. 1998. Solid-phase extraction and cuticular hydrocarbon differences related to reproductive activity in queenless ant Dinoponera quadriceps. J. Chem. Ecol. 24 : 473 490.
49. Moret, Y., and P. Schmid-Hempel. 2000. Survival for immunity: the price of immune system activation for bumblebee workers. Science 290 : 1166 1168.
50. Ottaviani, E., and C. Franceschi. 1996. The neuroimmunology of stress from invertebrates to man. Prog. Neurobiol. 48 : 421 440.
51. Pascual, C., A. Sanchez, A. Sanchez, F. Vargas-Albores, G. Le Moullac, and C. Rosas. 2003. Haemolymph metabolic variables and immune response in Litopenaeus setiferus adult males: the effect of an extreme temperature. Aquaculture 218 : 637 650.
52. Peeters, C. 1997. Morphologically 'primitive' ants: comparative review of social characters, and the importance of queen-worker dimorphism. Pp. 372 391 in J. C. Choe and B. J. Crespi, eds. Social behavior in insects and arachnids. Cambridge Univ. Press, Cambridge.
53. Peeters, C., and J. P. J. Billen. 1991. A novel exocrine gland inside the thoracic appendages ('gemmae') of the queenless ant Diacamma australe. Experientia 47 : 229 231.
54. Peeters, C., and S. Higashi. 1989. Reproductive dominance controlled by mutilation in the queenless ant Diacamma australe. Naturwissenschaften 76 : 177 180.
55. Peeters, C., J. Billen, and B. Hôlldobler. 1992. Alternative dominance mechanisms regulating monogyny in the queenless ant genus Diacamma. Naturwissenschaften 79 : 572 573.
56. Perazzolo, L. M., R. Gargioni, P. Ogliari, and M. A. A. Barracco. 2002. Evaluation of some hemato-immunological parameters in the shrimp Farfantepenaeus paulensis submitted to environmental and physiological stress. Aquaculture 214 : 19 33.
57. Peters, J. M., D. C. Queller, F. V. L. Imperatriz, D. W. Roubik, and J. E. Strassmann. 1999. Mate number, kin selection and social conflicts in stingless bees and honeybees. Proc. R. Soc. Biol. Sci. B 266 : 379 384.
58. Plaistow, S. J., Y. Outreman, Y. Moret, and T. Rigaud. 2003. Variation in the risk of being wounded: an overlooked factor in studies of invertebrate immune function Ecol. Lett. 6 : 489 494.
59. Poisbleau, M., H. Fritz, N. Guillon, and O. Chastel. 2005. Linear social dominance hierarchy and corticosterone responses in male mallards and pintails. Hormone Behav. 47 : 485 492.
60. Raberg, L., M. Grahn, D. Hasselquist, and E. Svensson. 1998. On the adaptive significance of stress-induced immunosuppression. Proc. R. Soc. Lond. B 265 : 1637 1641.
61. Rantala, M. J., and R. Kortet. 2004. Male dominance and immunocompetence in a field cricket. Behav. Ecol. 15 : 187 191.
62. Ratnieks, F. L. W. 1988. Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am. Nat. 132 : 217 236.
63. Ratnieks, F., and H. Reeve. 1992. Conflicts in single-queen Hymenopteran societies: the structure of conflict and processes that reduce conflict in advanced eusocial species. J. Theor. Biol. 158 : 33 65.
64. Rolff, J., and M. T. Siva-Jothy. 2003. Invertebrate ecological immunology. Science 301 : 472 475.
65. Röseler, P.-F. 1991. Reproductive competition during colony establishment. Pp. 309 335 in M. R. Ross KG, ed. The social biology of wasps. Cornell Univ. Press, Ithaca, New York.
66. Sands, J., and S. Creel. 2004. Social dominance, aggression and faecal glucocorticoid levels in a wild population of wolves, Canis lupus. Anim. Behav. 67 : 387 396.
67. Schmid-Hempel, P. 1998. Parasites in social insects. Princeton Univ. Press, Princeton, NJ.
68. Schmid-Hempel, P. 2005. Evolutionary ecology of insect immune defense. Annu. Rev. Entomol. 50 : 529 551.
69. Sheldon, B. C., and S. Verhulst. 1996. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11 : 317 321.
70. Sledge, M., F. Boscaro, and S. Turillazi. 2001. Cuticular hydrocarbons and reproductive status in the social wasp Polistes dominulus. Behav. Ecol. Sociobiol. 49 : 401 409.
71. Stefano, G., and M. Salzet. 1999. Invertebrates opioid precursors: evolutionary conservation and the significance of enzymatic processing. Int. Rev. Cytol. 187 : 261 286.
72. Strassmann, J. E., A. Fortunato, R. Cervo, S. Turillazi, J. M. Damon, and D. C. Queller. 2004. The Cost of Queen Loss in the Social Wasp Polistes dominulus (Hymenoptera: Vespidae). J. Kansas Entomol. Soc. 77 : 343 355.
73. Traniello, J. F. A., R. B. Rosengaus, and K. Savoie. 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.
74. Tsuji, K., K. Egashira, and B. Hölldobler. 1999. Regulation of worker reproduction by direct physical contacts in the ant Diacamma sp. from Japan. Anim. Behav. 58 : 337 343.
75. Vainio, L., H. Hakkarainen, M. J. Rantala, and J. Sorvari. 2004. Individual variation in immune function in the ant Formica exsecta: effects of the nest, body size and sex. Evol. Ecol. 18 : 75 84.
76. West-Eberhard, M. J. 1975. The evolution of social behavior by kin selection. Q. Rev. Biol. 50 : 1 33.
77. Zuk, M., and T. S. Johnsen. 2000. Social environment and immunity in male red jungle fowl. Behav. Ecol. 11 : 146 153.