Sexual division of antibacterial resource defence in breeding burying beetles, Nicrophorus vespilloides

Journal of Animal Ecology

Volumn 79, Issue 1, 2010, Pages 35-43

  Cotter, Sheena C ^a   Kilner, Rebecca M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Biparental care; Lysozyme; Partial compensation; Phenotypic plasticity; Social immunity

Indexed keywords

ANTIINFECTIVE AGENT;

BEETLE; CARRION; ENZYME ACTIVITY; IMMUNE SYSTEM; INTRASPECIFIC COMPETITION; MICROBIAL ACTIVITY; PARENTAL CARE; PHENOTYPIC PLASTICITY; RESOURCE USE; SEXUAL CONFLICT;

ANIMAL; ARTICLE; BEETLE; BREEDING; FEMALE; MALE; METABOLISM; MICROBIOLOGY; REPRODUCTION; SEXUAL BEHAVIOR; SEXUAL DEVELOPMENT;

ANIMALS; ANTI-INFECTIVE AGENTS; BEETLES; BREEDING; FEMALE; MALE; REPRODUCTION; SEX CHARACTERISTICS; SEXUAL BEHAVIOR, ANIMAL;

BACTERIA (MICROORGANISMS); COLEOPTERA; FUNGI; HEXAPODA; NICROPHORUS VESPILLOIDES;

EID: 72449134889     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/j.1365-2656.2009.01593.x     Document Type: Article

References (70)

1. Adamo, S.A., Jensen, M. Younger, M. (2001) Changes in lifetime immunocompetence in male and female Gryllus texensis (formerly G integer): trade-offs between immunity and reproduction. Animal Behaviour, 62, 417 425.
2. Anderson, R.S. Cook, M.L. (1979) Induction of lysozyme-like activity in the hemolymph and hemocytes of an insect, Spodoptera eridania. Journal of Invertebrate Pathology, 33, 197 203.
3. Barbero, F., Thomas, J.A., Bonelli, S., Balletto, E. Schönrogge, K. (2009) Queen ants make distinctive sounds that are mimicked by a butterfly social parasite. Science, 323, 782 785.
4. Bartlett, J. Ashworth, C.M. (1988) Brood size and fitness in Nicrophorus vespilloides (Coleoptera, Silphidae). Behavioral Ecology and Sociobiology, 22, 429 434.
5. Boman, H.G. Hultmark, D. (1987) Cell-free immunity in insects. Annual Review of Microbiology, 41, 103 126.
6. Brandt, M., Heinze, J., Schmitt, T. Foitzik, S. (2005) A chemical level in the coevolutionary arms race between an ant social parasite and its hosts. Journal of Evolutionary Biology, 18, 576 586.
7. Cardoza, Y.J., Klepzig, K.D. Raffa, K.F. (2006) Bacteria in oral secretions of an endophytic insect inhibit antagonistic fungi. Ecological Entomology, 31, 636 645.
8. Chapuisat, M., Oppliger, A., Magliano, P. Christe, P. (2007) Wood ants use resin to protect themselves against pathogens. Proceedings of the Royal Society of London. Series B: Biological Sciences, 274, 2013 2017.
9. Chase, I.D. (1980) Cooperative and non-cooperative behavior in animals. The American Naturalist, 115, 827 857.
10. Cotter, S.C., Kruuk, L.E.B. Wilson, K. (2004) Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. Journal of Evolutionary Biology, 17, 421 429.
11. Cotter, S., Myatt, J., Benskin, C. Wilson, K. (2008a) Selection for cuticular melanism reveals immune function and life-history trade-offs in Spodoptera littoralis. Journal of Evolutionary Biology, 21, 1744 1754.
12. Cotter, S.C., Beveridge, M. Simmons, L.W. (2008b) Male morph predicts investment in larval immune function in the dung beetle, Onthophagus taurus. Behavioral Ecology, 19, 331 337.
13. Cremer, S., Armitage, S.A.O. Schmid-Hempel, P. (2007) Social immunity. Current Biology, 17, R693 R702.
14. Curio, E. Onnebrink, H. (1995) Brood defense and brood size in the great tit (Parus major) - a test of a model of unshared parental investment. Behavioral Ecology, 6, 235 241.
15. Currie, C.R., Scott, J.A., Summerbell, R.C. Malloch, D. (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature, 398, 701 704.
16. Davies, N.B. (2000) Cuckoos, Cowbirds and Other Cheats. Academic Press, London.
17. Davies, N.B., Bourke, A.F.G. Brooke, M.D. (1989) Cuckoos and parasitic ants - interspecific brood parasitism as an evolutionary arms-race. Trends in Ecology & Evolution, 4, 274 278.
18. Fetherston, I.A., Scott, M.P. Traniello, J.F.A. (1990) Parental care in burying beetles - the organisation of male and female brood care behavior. Ethology, 85, 177 190.
19. Fetherston, I.A., Scott, M.P. Traniello, J.F.A. (1994) Behavioral compensation for mate loss in the burying beetle Nicrophorus orbicollis. Animal Behaviour, 47, 777 785.
20. Freitak, D., Wheat, C.W., Heckel, D.G. Vogel, H. (2007) Immune system responses and fitness costs associated with consumption of bacteria in larvae of Trichoplusia ni. BMC Biology, 5, 56.
21. Gill, S.A. Sealy, S.G. (2004) Functional reference in an alarm signal given during nest defence: seet calls of yellow warblers denote brood-parasitic brown-headed cowbirds. Behavioral Ecology and Sociobiology, 56, 71 80.
22. Gillespie, J.P., Kanost, M.R. Trenczek, T. (1997) Biological mediators of insect immunity. Annual Review of Entomology, 42, 611 643.
23. Haine, E.R., Pollitt, L.C., Moret, Y., Siva-Jothy, M.T. Rolff, J. (2008) Temporal patterns in immune responses to a range of microbial insults (Tenebrio molitor). Journal of Insect Physiology, 54, 1090 1097.
24. Hart, B.L. (2005) The evolution of herbal medicine: behavioural perspectives. Animal Behaviour, 70, 975 989.
25. Hinde, C.A. (2006) Negotiation over offspring care? A positive response to partner-provisioning rate in great tits. Behavioral Ecology, 17, 6 12.
26. Hoback, W.W., Bishop, A.A., Kroemer, J., Scalzitti, J. Shaffer, J.J. (2004) Differences among antimicrobial properties of carrion beetle secretions reflect phylogeny and ecology. Journal of Chemical Ecology, 30, 719 729.
27. Houston, A.I., McCleery, R.H. Davies, N.B. (1985) Territory size, prey renewal and feeding rates - interpretation of observations on the pied wagtail (Motacilla alba) by simulation. Journal of Animal Ecology, 54, 227 239.
28. Jenkins, E.V., Morris, C. Blackman, S. (2000) Delayed benefits of paternal care in the burying beetle Nicrophorus vespilloides. Animal Behaviour, 60, 443 451.
29. Johnstone, R.A. Hinde, C.A. (2006) Negotiation over offspring care - how should parents respond to each other's efforts? Behavioral Ecology, 17, 818 827.
30. Korner, P. Schmid-Hempel, P. (2004) In vivo dynamics of an immune response in the bumble bee Bombus terrestris. Journal of Invertebrate Pathology, 87, 59 66.
31. Kurtz, J., Wiesner, A., Gotz, P. Sauer, K.P. (2000) Gender differences and individual variation in the immune system of the scorpionfly Panorpa vulgaris (Insecta: Mecoptera). Developmental and Comparative Immunology, 24, 1 12.
32. Lazarus, J. Inglis, I.R. (1986) Shared and unshared parental investment, parent offspring conflict and brood size. Animal Behaviour, 34, 1791 1804.
33. Lessells, C.M. (2006) The evolutionary outcome of sexual conflict. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 361, 301 317.
34. Matsuura, K. (2006) Termite-egg mimicry by a sclerotium-forming fungus. Proceedings of the Royal Society of London. Series B: Biological Sciences, 273, 1203 1209.
35. Matsuura, K., Yashiro, T., Shimizu, K., Tatsumi, S. Tamura, T. (2009) Cuckoo fungus mimics termite eggs by producing the cellulose-digesting enzyme beta-glucosidase. Current Biology, 19, 30 36.
36. McKean, K.A. Nunney, L. (2005) Bateman's principle and immunity: phenotypically plastic reproductive strategies predict changes in immunological sex differences. Evolution, 59, 1510 1517.
37. McNamara, J.M., Gasson, C.E. Houston, A.I. (1999) Incorporating rules for responding into evolutionary games. Nature, 401, 368 371.
38. McNamara, J.M., Houston, A.I., Szekely, T. Webb, J.N. (2002) Do parents make independent decisions about desertion? Animal Behaviour, 64, 147 149.
39. Moret, Y. Schmid-Hempel, P. (2001) Entomology - immune defence in bumble-bee offspring. Nature, 414, 506 506.
40. Muller, J.K., Eggert, A.K. Sakaluk, S.K. (1998) Carcass maintenance and biparental brood care in burying beetles: are males redundant? Ecological Entomology, 23, 195 200.
41. Muller, J.K., Braunisch, V., Hwang, W.B. Eggert, A.K. (2007) Alternative tactics and individual reproductive success in natural associations of the burying beetle, Nicrophorus vespilloides. Behavioral Ecology, 18, 196 203.
42. Nappi, A.J. Vass, E. (1993) Melanogenesis and the generation of cytotoxic molecules during insect cellular immune-reactions. Pigment Cell Research, 6, 117 126.
43. Palomino, J.J., Martin-Vivaldi, M., Soler, M. Soler, J.J. (1998) Females are responsible for ejection of cuckoo eggs in the rufous bush robin. Animal Behaviour, 56, 131 136.
44. Panaitof, S.C., Scott, M.P. Borst, D.W. (2004) Plasticity in juvenile hormone in male burying beetles during breeding: physiological consequences of the loss of a mate. Journal of Insect Physiology, 50, 715 724.
45. Povey, S.R., Cotter, S.C., Simpson, S.J., Lee, K. Wilson, K. (2009) Can the protein costs of bacterial resistance be offset by altered feeding behaviour? Journal of Animal Ecology, 78, 437 446.
46. Pukowski, E. (1933) Okoloische untersuchungen an Necrophorus. Zeitschrift fur Morphologie und Oekologie der Tiere, 27, 518 586.
47. Rantala, M.J. Kortet, R. (2003) Courtship song and immune function in the field cricket Gryllus bimaculatus. Biological Journal of the Linnean Society, 79, 503 510.
48. Rantala, M.J., Roff, D.A. Rantala, L.M. (2007) Forceps size and immune function in the earwig Forficula auricularia L. Biological Journal of the Linnean Society, 90, 509 516.
49. Rasa, O.A.E. Heg, D. (2004) Individual variation and prior experience affect the discrimination of a brood-parasite by its subsocial beetle host. Behavioral Ecology and Sociobiology, 57, 155 163.
50. Reyer, H.U., Fischer, W., Steck, P., Nabulon, T. Kessler, P. (1998) Sex-specific nest defense in house sparrows (Passer domesticus) varies with badge size of males. Behavioral Ecology and Sociobiology, 42, 93 99.
51. Rolff, J. Siva-Jothy, M.T. (2002) Copulation corrupts immunity: a mechanism for a cost of mating in insects. Proceedings of the National Academy of Sciences of the United States of America, 99, 9916 9918.
52. Rowley, A.F., Brookman, J.L. Ratcliffe, N.A. (1990) Possible involvement of the prophenoloxidase system of the locust, Locusta migratoria, in antimicrobial activity. Journal of Invertebrate Pathology, 56, 31 38.
53. Rozen, D.E., Engelmoer, D.J.P. Smiseth, P.T. (2008) Antimicrobial strategies in burying beetles breeding on carrion. Proceedings of the National Academy of Sciences of the United States of America, 105, 17890 17895.
54. Ruusila, V. Poysa, H. (1998) Shared and unshared parental investment in the precocial goldeneye (Aves: Anatidae). Animal Behaviour, 55, 307 312.
55. Sanz, J.J., Kranenbarg, S. Tinbergen, J.M. (2000) Differential response by males and females to manipulation of partner contribution in the great tit (Parus major). Journal of Animal Ecology, 69, 74 84.
56. Scott, M.P. (1989) Male parental care and reproductive success in the burying beetle, Nicrophorus orbicollis. Journal of Insect Behavior, 2, 133 137.
57. Scott, M.P. (1990) Brood guarding and the evolution of male parental care in burying beetles. Behavioral Ecology and Sociobiology, 26, 31 39.
58. Scott, M.P. (1998) The ecology and behavior of burying beetles. Annual Review of Entomology, 43, 595 618.
59. Scott, M.P. Panaitof, S.C. (2004) Social stimuli affect juvenile hormone during breeding in biparental burying beetles (Silphidae: Nicrophorus). Hormones and Behavior, 45, 159 167.
60. Scott, J.J., Oh, D.C., Yuceer, M.C., Klepzig, K.D., Clardy, J. Currie, C.R. (2008) Bacterial protection of beetle-fungus mutualism. Science, 322, 63 63.
61. Smiseth, P.T. Moore, A.J. (2004) Behavioral dynamics between caring males and females in a beetle with facultative biparental care. Behavioral Ecology, 15, 621 628.
62. Smiseth, P.T., Dawson, C., Varley, E. Moore, A.J. (2005) How do caring parents respond to mate loss? Differential response by males and females. Animal Behaviour, 69, 551 559.
63. Stienen, E.W.M. Brenninkmeijer, A. (1999) Keep the chicks moving: how Sandwich terns can minimize kleptoparasitism by black-headed gulls. Animal Behaviour, 57, 1135 1144.
64. Taylor, I.R. (1979) Kleptoparasitic behavior of the arctic skua Stercorarius parasiticus with 3 species of tern. Ibis, 121, 274 282.
65. Trumbo, S.T. (2006) Infanticide, sexual selection and task specialization in a biparental burying beetle. Animal Behaviour, 72, 1159 1167.
66. Turillazzi, S., Cervo, R. Cavallari, I. (1990) Invasion of the nest of Polistes dominulus by the social parasite Sulcopolistes sulcifer (Hymenoptera, vespidae). Ethology, 84, 47 59.
67. Ward, R.J.S. (2007) Ageing and reproductive strategies in the Burying Beetle Nicrophorus vespilloides. PhD thesis, University of Cambridge, Cambridge.
68. Welbergen, J.A. Davies, N.B. (2009) Strategic variation in mobbing as a front line defense against brood parasitism. Current Biology, 324, 1318 1320.
69. West, K.J. Alexander, R.D. (1963) Sub-social behavior in a burrowing cricket Anurogryllus muticus (De Greer). Orthoptera: Gryllidae. Ohio Journal of Science, 63, 19 24.
70. Wilson, K. Cotter, S.C. (2009) Density-dependent prophylaxis in insects. Phenotypic Plasticity of Insects: Mechanisms and Consequences (eds T.N. Ananthakrishnan D.W. Whitman 137 176. Science Publishers Inc., Plymouth, UK.