Sexual dimorphism in life history: Age, survival, and reproduction in male and female field crickets teleogryllus commodus under seminatural conditions

American Naturalist

Volumn 173, Issue 6, 2009, Pages 792-802

  Zajitschek, Felix ^a,b   Bonduriansky, Russell ^a   Zajitschek, Susanne R K ^a,b   Brooks, Robert C ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b CNRS   (France)

Author keywords

Field enclosures; Insects; Mortality rates; Reproductive aging; Senescence; Sex differences

Indexed keywords

AGING; CRICKET; LIFE HISTORY TRAIT; LONGEVITY; MORTALITY; REPRODUCTIVE EFFORT; REPRODUCTIVE STRATEGY; RESOURCE ALLOCATION; SENESCENCE; SEX-RELATED DIFFERENCE; SEXUAL DIMORPHISM; SURVIVAL; TRADE-OFF;

ANIMALIA; GRYLLINAE; HEXAPODA; TELEOGRYLLUS COMMODUS;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; FEMALE; GRYLLIDAE; LONGEVITY; MALE; OVIPARITY; PHYSIOLOGY; SEXUAL BEHAVIOR; SEXUAL DEVELOPMENT;

ANIMALS; FEMALE; GRYLLIDAE; LONGEVITY; MALE; MODELS, BIOLOGICAL; OVIPARITY; SEX CHARACTERISTICS; SEXUAL BEHAVIOR, ANIMAL;

EID: 66149168021     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/598486     Document Type: Article

References (92)

1. Abrams, P. A. 1993. Does increased mortality favor the evolution of more rapid senescence? Evolution 47:877-887.
2. Andersson, M. 1994. Sexual selection. Princeton University Press, Princeton, NJ.
3. Bailey, W. J., and S. Haythornthwake. 1998. Risks of calling by the field cricket Teleogryllus oceanicus: potential predation by Australian long-eared bats. Journal of Zoology 244:505-513.
4. Baudisch, A. 2005. Hamilton's indicators of the force of selection. Proceedings of the National Academy of Sciences of the USA 102: 8263-8268.
5. Beck, C. A., W. D. Bowen, and S. J. Iverson. 2003. Sex differences in the seasonal patterns of energy storage and expenditure in a phocid seal. Journal of Animal Ecology 72:280-291.
6. Bentsen, C. L., J. Hunt, M. D. Jennions, and R. Brooks. 2006. Complex multivariate sexual selection on male acoustic signaling in a wild population of Teleogryllus commodus. American Naturalist 167:E102-E116.
7. Bonduriansky, R., and C. E. Brassil. 2002. Rapid and costly ageing in wild male flies. Nature 420:377. (Pubitemid 35415639)
8. -. 2005. Reproductive ageing and sexual selection on male body size in a wild population of antler flies (Protopiophila litigata). Journal of Evolutionary Biology 18:1332-1340.
9. Bonduriansky, R., A. Maklakov, F. Zajitschek, and R. Brooks. 2008. Sexual selection, sexual conflict and the evolution of ageing and life span. Functional Ecology 22:443-453. (Pubitemid 351703929)
10. Bronikowski, A. M., and D. E. L. Promislow. 2005. Testing evolutionary theories of aging in wild populations. Trends in Ecology & Evolution 20:271-273.
11. Bryant, M. J., and D. Reznick. 2004. Comparative studies of senescence in natural populations of guppies. American Naturalist 163: 55-68.
12. Carey, J. R., P. Liedo, H. G. Müller, J. L. Wang, and J. M. Chiou. 1998. Relationship of age patterns of fecundity to mortality, longevity, and lifetime reproduction in a large cohort of Mediterranean fruit fly females. Journals of Gerontology Series A 53:B245-B251.
13. Charlesworth, B. 2000. Fisher, Medawar, Hamilton and the evolution of aging. Genetics 156:927-931. (Pubitemid 30826475)
14. -. 2001. Patterns of age-specific means and genetic variances of mortality rates predicted by the mutation-accumulation theory of ageing. Journal of Theoretical Biology 210:47-65.
15. Charmantier, A., C. Perrins, R. H. McCleery, and B. C. Sheldon. 2006. Quantitative genetics of age at reproduction in wild swans: support for antagonistic pleiotropy models of senescence. Proceedings of the National. Academy of Sciences of the USA 103: 6587-6592.
16. Chippindale, A. K., D. T. Hoang, P. M. Service, and M. R. Rose. 1994. The evolution of development in Drosophila melanogaster selected for postponed senescence. Evolution 48:1880-1899.
17. Clutton-Brock, T. H., S. J. Hodge, G. Spong, A. F. Russell, N. R. Jordan, N. C. Bennett, L. L. Sharpe, and M. B. Manser. 2006. Intrasexual competition and sexual selection in cooperative mammals. Nature 444:1065-1068. (Pubitemid 46018525)
18. Comfort, A. 1978. The biology of senescence. Elsevier, London.
19. Cordts, R., and L. Partridge. 1996. Courtship reduces longevity of male Drosophila melanogaster. Animal Behaviour 52:269-278.
20. Curtsinger, J. W, H. H. Fukui, A. A. Khazaeli, A. Kirscher, S. D. Pletcher, D. E. L. Promislow, and M. Tatar. 1995. Genetic variation and aging. Annual Review of Genetics 29:553-575.
21. Emlen, J. M. 1970. Age specificity and ecological theory. Ecology 51: 588-601.
22. Glazier, D. S. 1999. Trade-offs between reproductive and somatic (storage) investments in animals: a comparative test of the Van Noordwijk and De Jong model. Evolutionary Ecology 13:539-555.
23. Graves, B. M. 2007. Sexual selection effects on the evolution of senescence. Evolutionary Ecology 21:663-668. (Pubitemid 47305466)
24. Grotewiel, M. S., I. Martin, P. Bhandari, and E. Cook-Wiens. 2005. Functional senescence in Drosophila melanogaster. Ageing Research Reviews 4:372-397.
25. Gustafsson, L., and T. Part. 1990. Acceleration of senescence in the collared flycatcher Ficedula albicollis by reproductive costs. Nature 347:279-281.
26. Hamilton, W. D. 1966. Moulding of senescence by natural selection. Journal of Theoretical Biology 12:12-45.
27. Hansen, T. F., and D. K. Price. 1995. Good genes and old age: do old mates provide superior genes? Journal of Evolutionary Biology 8:759-778.
28. Houle, D. 1991. Genetic covariance of fitness correlates: what genetic correlations are made of and why it matters. Evolution 45:630648.
29. Hughes, K. A. 1995. The evolutionary genetics of male life-history characters in Drosophila melanogaster. Evolution 49:521-537.
30. Hunt, J., R. Brooks, M. D. Jennions, M. J. Smith, C. L. Bentsen, and L. F. Bussière. 2004a. High-quality male field crickets invest heavily in sexual display but die young. Nature 432:1024-1027. (Pubitemid 40052232)
31. Hunt, J., L. F. Bussière, M. D. Jennions, and R. Brooks. 2004b. What is genetic quality? Trends in Ecology & Evolution 19:329-333.
32. Hunt, J., M. D. Jennions, N. Spyrou, and R. Brooks. 2006. Artificial selection on male longevity influences age-dependent reproductive effort in the black field cricket Teleogryllus commodus. American Naturalist 168:E72-E86.
33. Jaccard, J. J., and R. Turrisi. 2003. Interaction effects in multiple regression (quantitative applications in the social sciences). Sage, London.
34. Kaeberlein, T. L., E. D. Smith, M. Tsuchiya, K. L. Welton, J. H. Thomas, S. Fields, B. K. Kennedy, and M. Kaeberlein. 2006. Lifespan extension in Caenorhabditis elegans by complete removal of food. Aging Cell 5:487-494.
35. Kawasaki, N., C. E. Brassil, R. Brooks, and R. Bonduriansky. 2008. Environmental effects on the expression of lifespan and aging: an extreme contrast between wild and captive cohorts of Telostylinus angusticollis (Diptera: Neriidae). American Naturalist 172:346-357.
36. Kirkwood, T. B. L., and S. N. Austad. 2000. Why do we age? Nature 408:233-238.
37. Kokko, H. 1997. Evolutionarily stable strategies of age-dependent sexual advertisement. Behavioral Ecology and Sociobiology 41:99107. (Pubitemid 27378022)
38. -. 1998. Good genes, old age and life-history trade-offs. Evolutionary Ecology 12:739-750.
39. Kokko, H., R. Brooks, J. M. McNamara, and A. I. Houston. 2002. The sexual selection continuum. Proceedings of the Royal Society B: Biological Sciences 269:1331-1340.
40. Kolluru, G. R., M. A. Chappell, and M. Zuk. 2004. Sex differences in metabolic rates in field crickets and their dipteran parasitoids. Journal of Comparative Physiology B 174:641-648.
41. Kotiaho, J. S. 2000. Testing the assumptions of conditional handicap theory: costs and condition dependence of a sexually selected trait. Behavioral Ecology and Sociobiology 48:188-194.
42. Kotiaho, J. S., and L. W. Simmons. 2003. Longevity cost of reproduction for males but no longevity cost of mating or courtship for females in the male-dimorphic dung beetle Onthophagus binodis. Journal of Insect Physiology 49:817-822.
43. Loher, W, and K. Edson. 1973. The effect of mating on egg-production and release in the cricket Teleogryllus commodus. Entomologia Experimentalis et Applicata 16:483-490.
44. Loher, W, I. Ganjian, I. Kubo, D. Stanley-Samuelson, and S. S. Tobe. 1981. Prostaglandins: their role in egg-laying of the cricket Teleogryllus commodus. Proceedings of the National Academy of Sciences of the USA 78:7835-7838.
45. Loison, A., M. Festa-Bianchet, J. M. Gaillard, J. T. Jorgenson, and J. M. Jullien. 1999. Age-specific survival in five populations of ungulates: evidence of senescence. Ecology 80:2539-2554. (Pubitemid 30001003)
46. Maklakov, A. A., S. J. Simpson, F. Zajitschek, M. D. Hall, J. Dessmann, F. Clissold, D. Raubenheimer, R. Bonduriansky, and R. C. Brooks. 2008. Sex-specific fitness effects of nutrient intake on reproduction and lifespan. Current Biology 18:1062-1066.
47. McCulloch, D., and D. Gems. 2003. Evolution of male longevity bias in nematodes. Aging Cell 2:165-173.
48. Messina, F. J., and J. D. Fry. 2003. Environment-dependent reversal of a life history trade-off in the seed beetle Callosobruchus maculatus. Journal of Evolutionary Biology 16:501-509.
49. Møller, A. P., F. De Lope, and N. Saino. 2005. Reproduction and migration in relation to senescence in the barn swallow Hirundo rustica: a study of avian "centenarians." Age 27:307-318.
50. Moore, P. J., and A. J. Moore. 2001. Reproductive aging and mating: the ticking of the biological clock in female cockroaches. Proceedings of the National Academy of Sciences of the USA 98:9171-9176.
51. Murray, A. M., and W. H. Cade. 1995. Differences in age structure among field cricket populations (Orthoptera, Gryllidae): possible influence of a sex-biased parasitoid. Canadian Journal of Zoology 73:1207-1213.
52. Mysterud, A., G. Steinheim, N. G. Yoccoz, O. Holand, and N. C. Stenseth. 2002. Early onset of reproductive senescence in domestic sheep, Ovis aries. Oikos 97:177-183. (Pubitemid 34735646)
53. Norry, F. M., P. Sambucetti, A. C. Scannapieco, and V. Loeschcke. 2006. Altkudinal patterns for longevity, fecundity and senescence in Drosophila buzzatii. Genetica 128:81-93.
54. Nussey, D. H., L. E. B. Kruuk, A. Donald, M. Fowlie, and T. H. Clutton-Brock. 2006. The rate of senescence in maternal performance increases with early-life fecundity in red deer. Ecology Letters 9:1342-1350.
55. Parker, G. A. 2006. Sexual conflict over mating and fertilization: an overview. Philosophical Transactions of the Royal Society B: Biological Sciences 361:235-259. (Pubitemid 44870111)
56. Partridge, L., and N. H. Barton. 1996. On measuring the rate of ageing. Proceedings of the Royal Society B: Biological Sciences 263: 1365-1371.
57. Partridge, L., and D. Gems. 2002. Mechanisms of ageing: public or private? Nature Reviews Genetics 3:165-175.
58. Phelan, J. P., M. A. Archer, K. A. Beckman, A. K. Chippindale, T. J. Nusbaum, and M. R. Rose. 2003. Breakdown in correlations during laboratory evolution. I. Comparative analyses of Drosophila populations. Evolution 57:527-535.
59. Pletcher, S. D. 1999. Model fitting and hypothesis testing for agespecific mortality data. Journal of Evolutionary Biology 12:430439.
60. Pletcher, S. D., A. A. Khazaeli, and J. W Curtsinger. 2000. Why do life spans differ? partitioning mean longevity differences in terms of age-specific mortality parameters. Journals of Gerontology Series A 55:B381-B389.
61. Promislow, D. 2003. Mate choice, sexual conflict, and evolution of senescence. Behavior Genetics 33:191-201. (Pubitemid 36384237)
62. Promislow, D. E. L. 1991. Senescence in natural populations of mammals: a comparative study. Evolution 45:1869-1887.
63. Promislow, D. E. L., R. Montgomerie, and T. E. Martin. 1992. Mortality costs of sexual dimorphism in birds. Proceedings of the Royal Society B: Biological Sciences 250:143-150.
64. Promislow, D. E. L., M. Tatar, A. A. Khazaeli, and J. W. Curtsinger. 1996. Age-specific patterns of genetic variance in Drosophila melanogaster. I. Mortality. Genetics 143:839-848.
65. R Development Core Team. 2007. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org.
66. Rauser, C. L., J. J. Tierney, S. M. Gunion, G. M. Covarrubias, L. D. Mueller, and M. R. Rose. 2000. Evolution of late-life fecundity in Drosophila melanogaster. Journal of Evolutionary Biology 19:289-301.
67. Reed, T. E., L. E. B. Kruuk, S. Wanless, M. Frederiksen, E. J. A. Cunningham, and M. P. Harris. 2008. Reproductive senescence in a long-lived seabird: rates of decline in late-life performance are associated with varying costs of early reproduction. American Naturalist 171:E89-E101.
68. Reid, J. M., E. M. Bignal, S. Bignal, D. I. McCracken, and P. Monaghan. 2003. Age-specific reproductive performance in red-billed choughs Pyrrhocorax pyrrhocorax. patterns and processes in a natural population. Journal of Animal Ecology 72:765-776.
69. Reznick, D., C. Ghalambor, and L. Nunney. 2002. The evolution of senescence in fish. Mechanisms of Ageing and Development 123: 773-789.
70. Reznick, D. N., M. J. Bryant, D. Roff, C. K. Ghalambor, and D. E. Ghalambor. 2004. Effect of extrinsic mortality on the evolution of senescence in guppies. Nature 431:1095-1099.
71. Ricklefs, R. E. 1998. Evolutionary theories of aging: confirmation of a fundamental prediction, with implications for the genetic basis and evolution of life span. American Naturalist 152:24-44.
72. Roff, D. A. 1992. The evolution of life histories: theory and analysis. Chapman & Hall, New York.
73. Rose, M., and B. Charlesworth. 1980. A test of evolutionary theories of senescence. Nature 287:141-142.
74. Rose, M. R. 1994. Evolutionary biology of aging. Oxford University Press, New York.
75. Rowe, L., and D. Houle. 1996. The lek paradox and the capture of genetic variance by condition dependent traits. Proceedings of the Royal Society B: Biological Sciences 263:1415-1421. (Pubitemid 26370894)
76. Sedensky, M. M., and G. Morgan. 2006. Mitochondrial respiration and reactive oxygen species in mitochondrial aging mutants. Experimental Gerontology 41:237-245.
77. Stearns, S. C. 1992. The evolution of life histories. Oxford University Press, Oxford.
78. Stearns, S. C., M. Ackermann, M. Doebeli, and M. Kaiser. 2000. Experimental evolution of aging, growth, and reproduction in fruitflies. Proceedings of the National Academy of Sciences of the USA 97:3309-3313. (Pubitemid 30183298)
79. Tatar, M., J. R. Carey, and J. W. Vaupel. 1993. Long-term cost of reproduction with and without accelerated senescence in Callosobruchus maculatus: analysis of age-specific mortality. Evolution 47:1302-1312.
80. Tatar, M., D. E. L. Promislow, A. A. Khazaeli, and J. W. Curtsinger. 1996. Age-specific patterns of genetic variance in Drosophila melanogaster. II. Fecundity and its genetic covariance with age-specific mortality. Genetics 143:849-858.
81. Trivers, R. L. 1972. Parental investment and sexual selection. Pages 136-179 in B. Campbell, ed. Sexual selection and the descent of man, 1871-1971. Aldine-Atherton, Chicago.
82. Tuck, N., I. Gliksman, D. Seslija, D. Milanovic, S. Mikuljanac, and O. Stojkovic. 1996. Laboratory evolution of longevity in the bean weevil (Acanthoscelides obtectus). Journal of Evolutionary Biology 9:485-503.
83. Walker, T. J., and S. Masaki. 1989. Natural history. Pages 1-42 in F. Huber, T. E. Moore, and W. Loher, eds. Cricket behavior and neurobiology. Cornell University Press, Ithaca, NY.
84. Williams, G. C. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:398-411.
85. -. 1966. Natural selection, the costs of reproduction and a refinement of Lack's principle. American Naturalist 100:687-690.
86. -. 1999. The tkhonus error in modern gerontology. Quarterly Review of Biology 74:405-415.
87. Williams, P. D., and T. Day. 2003. Antagonistic pleiotropy, mortality source interactions, and the evolutionary theory of senescence. Evolution 57:1478-1488.
88. Williams, P. D., T. Day, Q. Fletcher, and L. Rowe. 2006. The shaping of senescence in the wild. Trends in Ecology & Evolution 21:458-463.
89. Zajitschek, F., J. Hunt, S. R. K. Zajitschek, M. D. Jennions, and R. Brooks. 2007. No sexual conflict over reproductive fitness or ageing in field crickets. PLoS ONE 2:e155.
90. Zajitschek, F., C. E. Brassil, R. Bonduriansky, and R. Brooks. 2009. Sex effects on life span and senescence in the wild when dates of birth and death are unknown. Ecology (forthcoming).
91. Zuk, M., and G. R. Kolluru. 1998. Exploitation of sexual signals by predators and parasitoids. Quarterly Review of Biology 73:415438. (Pubitemid 128652457)
92. Zwaan, B. J. 1999. The evolutionary genetics of ageing and longevity. Heredity 82:589-597.