Juvenile hormone as a regulator of the trade-off between reproduction and life span in Drosophila melanogaster

Evolution

Volumn 61, Issue 8, 2007, Pages 1980-1991

  Flatt, Thomas ^a,b   Kawecki, Tadeusz J ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

^b BROWN UNIVERSITY   (United States)

Author keywords

Aging; Antagonistic pleiotropy; Cost of reproduction; Drosophila; Experimental evolution; Juvenile hormone; Life span; Reproduction; Trade off

Indexed keywords

JUVENILE HORMONE; METHOPRENE;

AGING; ANTAGONISM; EXPERIMENTAL STUDY; FECUNDITY; FLY; HORMONE; JUVENILE; PHYSIOLOGICAL RESPONSE; PLEIOTROPY; REPRODUCTION; TRADE-OFF;

ANIMAL; ARTICLE; BODY WEIGHT; DROSOPHILA MELANOGASTER; EVOLUTION; GENETIC SELECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIFE CYCLE; LONGEVITY; PHYSIOLOGY; REPRODUCTION;

ANIMALS; BODY WEIGHT; DROSOPHILA MELANOGASTER; EVOLUTION; JUVENILE HORMONES; LIFE CYCLE STAGES; LONGEVITY; METHOPRENE; REPRODUCTION; SELECTION (GENETICS);

DROSOPHILA MELANOGASTER;

EID: 34547686754     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2007.00151.x     Document Type: Article

References (84)

1. Ackermann, M., R. Bijlsma, A. C. James, L. Partridge, B. J. Zwaan, and S. C. Stearns. 2001. Effects of assay conditions in life history experiments with Drosophila melanogaster. J. Evol. Biol. 14 : 199 209.
2. Arantes-Oliveira, N., J. Apfeld, A. Dillin, and C. Kenyon. 2002. Regulation of life-span by germ-line stem cells in Caenorhabditis elegans. Science 295 : 502 505.
3. Barnes, A. I., and L. Partridge. 2003. Costing reproduction. Anim. Behav. 66 : 199 204.
4. Bell, G., and V. Koufopanou. 1986. The cost of reproduction. Pp. 83 131 in R. Dawkins and M. Ridley, eds. Oxford Surv. Evol. Biol. Vol. 3. Oxford Univ. Press, Oxford, U.K.
5. Belles, X., D. Martin, and M. D. Piulachs. 2005. The mevalonate pathway and the synthesis of juvenile hormone in insects. Annu. Rev. Entomol. 50 : 181 199.
6. Broué, F., P. Liere, C. Kenyon, and E.-E. Baulieu. 2007. A steroid hormone that extends the lifespan of Caenorhabditis elegans. Aging Cell 6 : 87 94.
7. Carey, J. R., P. Liedo, D. Orozco, and J. W. Vaupel. 1992. Slowing of mortality rates at older ages in large medfly cohorts. Science 258 : 457 461.
8. Chiang, C. L. 1984. The life table and its applications. Krieger, Malabar, Florida.
9. Chapman, T., L. F. Liddle, J. M. Kalb, M. F. Wolfner, and L. Partridge. 1995. Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373 : 241 244.
10. Cherbas, L., M. M. Koehler, and P. Cherbas. 1989. Effects of juvenile hormone on the ecdysone response of Drosophila Kc cells. Dev. Genet. 10 : 177 188.
11. Clancy, D. J., D. Gems, L. G. Harshman, S. Oldham, H. Stocker, E. Hafen, S. J. Leevers, and L. Partridge. 2001. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292 : 104 106.
12. Curtsinger, J. W., H. H. Fukui, D. R. Townsend, and J. W. Vaupel. 1992. Demography of genotypes: failure of the limited life-span paradigm in Drosophila melanogaster. Science 258 : 461 463.
13. de Jong, G., and A. J. Van Noordwijk. 1992. Acquisition and allocation of resources - genetic (co) variances, selection, and life histories. Am. Nat. 139 : 749 770.
14. Dingle, H., and Winchell, R. 1997. Juvenile hormones as a mediator of plasticity in insect life histories. Arch. Insect Biochem. Physiol. 35 : 359 373.
15. Elandt-Johnson, R., and N. L. Johnson. 1980. Survival models and data analysis. Wiley, New York.
16. Finch, C. E., and M. R. Rose. 1995. Hormones and the physiological architecture of life history evolution. Q. Rev. Biol. 70 : 1 52.
17. Flatt, T. 2004a. Assessing natural variation in genes affecting Drosophila life span. Mech. Ageing Dev. 125 : 155 159.
18. Flatt, T. 2004b. Effects of juvenile hormone on trait architecture in Drosophila melanogaster. Ph.D. Dissertation, Department of Biology, Unit of Ecology and Evolution, University of Fribourg, Switzerland, January 2004. Imprimerie St. Paul (Fribourg), 209 pp.
19. Flatt, T., and T. J. Kawecki. 2004. Pleiotropic effects of methoprene-tolerant (Met), a gene involved in juvenile hormone metabolism, on life history traits in Drosophila melanogaster. Genetica 122 : 141 160.
20. Flatt, T., M.-P. Tu, and M. Tatar. 2005. Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history. BioEssays 27 : 999 1010.
21. Flatt, T., L. L. Moroz, M. Tatar, and A. Heyland. 2006. Comparing thyroid and insect hormone signaling. Integr. Comp. Biol. 46 : 777 794.
22. Fowler, K., and L. Partridge. 1989. A cost of mating in female fruitflies. Nature 338 : 760 761.
23. Fry, C. L. 2006. Juvenile hormone mediates a trade-off between primary and secondary sexual traits in stalk-eyed flies. Evol. Dev. 8 : 191 201.
24. Gäde, G., K. H. Hoffmann, and J. H. Spring. 1997. Hormonal regulation in insects: facts, gaps, and future directions. Physiol. Rev. 77 : 963 1032.
25. Good, T. P., and M. Tatar. 2001. Age-specific mortality and reproduction to adult dietary restriction in Drosophila melanogaster. J. Insect Physiol. 47 : 1467 1473.
26. Harris, R. J. 1985. A primer of multivariate statistics. Academic Press, New York.
27. Harshman, L. G., and A. J. Zera. 2007. The cost of reproduction: the devil in the details. Trends Ecol. Evol. 22 : 80 86.
28. Herman, W. S., and M. Tatar. 2001. Juvenile hormone regulation of aging in the migratory monarch butterfly. Proc. R. Soc. Lond. B 268 : 2509 2514.
29. Hoffmann, K. H. 1995. Oogenesis and the female reproductive tract. Pp. 1 32 in S. R. Leather and J. Hardy, eds. Insect reproduction. CRC Press, New York.
30. Hsin, H., and C. Kenyon. 1999. Signals from the reproductive system regulate the lifespan of C. elegans. Nature 399 : 362 366.
31. Jenkins, N. L., G. McColl, and G. J. Lithgow. 2004. Fitness cost of extended lifespan in Caenorhabditis elegans. Proc. R. Soc. London B 271 : 2523 2526.
32. Ketterson, E. D., and V. Nolan. 1992. Hormones and life histories: an integrative approach. Am. Nat. 140 : S33 S62.
33. Kirkwood, T. B., and M. R. Rose. 1991. Evolution of senescence: late survival sacrificed for reproduction. Philos. Trans. R. Soc. Lond. B 332 : 15 24.
34. Leroi, A. 2001. Molecular signals versus the Loi de Balancement. Trends Ecol. Evol. 16 : 24 29.
35. Mangelsdorf, D. J., C. Thummel, M. Beato, P. Herrlich, G. Schutz, K. Umesono, B. Blumberg, P. Kastner, M. Mark, P. Chambon, and R. M. Evans. 1995. The nuclear receptor superfamily: the second decade. Cell 83 : 835 839.
36. Marden, J. H., B. Rogina, K. L. Montooth, and S. L. Helfand. 2003. Conditional tradeoffs between aging and organismal performance of Indy long-lived mutant flies. Proc. Natl. Acad. Sci. USA 100 : 3369 3373.
37. Motola, D., C. L. Cummins, V. Rottiers, K. Sharma, K. Sunino, E. Xu, R. Auchus, A. Antebi, and D. Mangelsdorf. 2006. Identification of hormonal ligands for DAF-12 that govern dauer formation and reproduction in C. elegans. Cell 124 : 1209 1223.
38. Nijhout, H. F. 1994. Insect hormones. Princeton Univ. Press, Princeton, NJ.
39. Parmar, M. K. B., and D. Machin. 1995. Survival analysis: a practical approach. Wiley, Chichester, U.K.
40. Partridge, L., and K. Fowler. 1990. Nonmating costs of exposure to males in female Drosophila melanogaster. J. Insect Physiol. 36 : 419 425.
41. Partridge, L., D. Gems, and D. J. Withers. 2005. Sex and death: what is the connection? Cell 120 : 461 472.
42. Partridge, L., A. Green, and K. Fowler. 1987. Effects of egg-production and of exposure to males on female survival in Drosophila melanogaster. J. Insect Physiol. 33 : 745 749.
43. Partridge, L., N. Prowse, and P. Pignatelli. 1999. Another set of responses and correlated responses to selection on age at reproduction in Drosophila melanogaster. Proc. R. Soc. Lond. B 266 : 255 261.
44. Pener, M. P. 1972. The corpus allatum in adult acridids: the inter-relation of its functions and possible correlations with the life cycle. Pp. 135 147 in C. F. Hemming and T. H. C. Taylor, eds. Proc. Int. Study Conf. Curr. Fut. Prob. Acridol. Centre for Overseas Pest Research, London, U.K.
45. Pletcher, S. D. 1999. Model fitting and hypothesis testing for age-specific mortality data. J. Evol. Biol. 12 : 430 439.
46. Rantala, M. J., A. Vainikka, and R. Kortet. 2003. The role of juvenile hormone in immune function and pheromone production trade-offs: a test of the immunocompetence handicap principle. Proc. R. Soc. Lond. B 270 : 2257 2261.
47. Reznick, D. 1985. Costs of reproduction - an evaluation of the empirical evidence. Oikos 44 : 257 267.
48. Reznick, D. 1992. Measuring the costs of reproduction. Trends Ecol. Evol. 7 : 42 45.
49. Richard, D. S., R. Rybczynski, T. G. Wilson, Y. Wang, M. L. Wayne, Y. Zhou, L. Partridge, and L. G. Harshman. 2005. Insulin signaling is necessary for vitellogenesis in Drosophila melanogaster independent of the roles of juvenile hormone and ecdysteroids: female sterility of the chico1 insulin signaling mutation is autonomous to the ovary. J. Insect Physiol. 51 : 455 464.
50. Riddiford, L. M., and M. Ashburner. 1991. Effects of juvenile hormone mimics on larval development and metamorphosis of Drosophila melanogaster. Gen. Comp. Endocrin. 82 : 172 183.
51. Roff, D. A. 1992. The evolution of life histories: Theory and analysis. Chapman & Hall. New York.
52. Rolff, J., and M. T. Siva-Jothy. 2002. Copulation corrupts immunity: a mechanism for a cost of mating in insects. Proc. Natl. Acad. Sci. USA 99 : 9916 9918.
53. Rose, M. R. 1984. Laboratory evolution of postponed senescence in Drosophila melanogaster. Evolution 38 : 1004 1010.
54. Rose, M. R., and T. J. Bradley. 1998. Evolutionary physiology of the cost of reproduction. Oikos 83 : 443 451.
55. Sall, J., L. Creighton, and A. Lehman. 2004. JMP Start Statistics, 3rd ed. Thomson Learning, SAS Institute, Cary, NC Duxbury Press, Pacific Grove, CA.
56. Salmon, A. B., D. B. Marx, and L. G. Harshman. 2001. A cost of reproduction in Drosophila melanogaster: stress susceptibility. Evolution 55 : 1600 1608.
57. Schwartz, M. W., S. C. Woods, D. Porte, R. J. Seeley, and D. G. Baskin. 2000. Central nervous system control of food intake. Nature 404 : 661 671.
58. Sgro, C. M., and L. Partridge. 1999. A delayed wave of death from reproduction in Drosophila. Science 286 : 2521 2524.
59. Silbermann, R., and M. Tatar. 2000. Reproductive costs of heat shock protein in transgenic Drosophila melanogaster. Evolution 54 : 2038 2045.
60. Stearns, S. C. 1989. Trade-offs in life-history evolution. Funct. Ecol. 3 : 259 268.
61. Stearns, S. C. 1992. The evolution of life histories. Oxford Univ. Press, Oxford, U.K.
62. Stearns, S. C., and L. Partridge. 2001. The genetics of aging in Drosophila. Pp. 353 368 in E. J. Masoro and S. N. Austad, eds. Handbook of the biology of aging, 5th ed. Academic Press (Elsevier), San Diego, CA.
63. Tatar, M. 2007. Diet restriction in Drosophila melanogaster: design and analysis. Interdiscip. Top. Gerontol. 35 : 115 136.
64. Tatar, M., and J. R. Carey. 1995. Nutrition mediates reproductive trade-offs with age-specific mortality in the beetle Callosobruchus maculatus. Ecology 76 : 2066 2073.
65. Tatar, M., and C.-M. Yin. 2001. Slow aging during insect reproductive diapause: why butterflies, grasshoppers and flies are like worms. Exp. Geront. 36 : 723 738.
66. Tatar, M., A. Bartke, and A. Antebi. 2003. The endocrine regulation of aging by insulin-like signals. Science 299 : 1346 1351.
67. Tatar, M., S. A. Chien, and N. K. Priest. 2001b. Negligible senescence during reproductive dormancy in Drosophila melanogaster. Am. Nat. 158 : 248 258.
68. Tatar, M., A. Kopelman, D. Epstein, M.-P. Tu, C.-M. Yin, and R. S. Garofalo. 2001a. A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292 : 107 110.
69. Tu, M.-P., and M. Tatar. 2003. Juvenile diet restriction and the aging and reproduction of adult Drosophila melanogaster. Aging Cell 2 : 327 333.
70. Tu, M.-P., T. Flatt, and M. Tatar. 2006. Juvenile and steroid hormones in Drosophila melanogaster longevity. Pp. 415 448 in E. J. Masoro and S. N. Austad, eds. Handbook of the biology of aging, 6th ed. Academic Press (Elsevier), San Diego, CA.
71. Tu, M.-P., C. M. Yin, and M. Tatar. 2005. Mutations in insulin signaling pathway alter juvenile hormone synthesis in Drosophila melanogaster. Gen. Comp. Endocrin. 142 : 347 356.
72. van Noordwijk, A., and G. de Jong. 1986. Acquisition and allocation of resources: their influence on variation in life history tactics. Am. Nat. 128 : 137 142.
73. von Ende, C. N. 2001. Repeated-measures analysis: growth and other time-dependent measures. Pp. 134 157 in S. M. Scheiner and J. Gurevitch, eds. Design and analysis of ecological experiments, 2nd ed. Oxford Univ. Press, Oxford, U.K.
74. Walker, D. W., G. McColl, N. L. Jenkins, J. Harris, and G. J. Lithgow. 2000. Evolution of lifespan in C. elegans. Nature 405 : 296 297.
75. Williams, G. C. 1966. Natural selection, the costs of reproduction, and a refinement of Lack's principle. Am. Nat. 100 : 687 690.
76. Wilson, T. G. 2004. The molecular site of action of juvenile hormone and juvenile hormone insecticides during metamorphosis: how these compounds kill insects. J. Insect Physiol. 50 : 111 121.
77. Wilson, T. G., and D. Chaykin. 1985. Toxicity of methoprene to Drosophila melanogaster (Diptera: Drosophilidae): a function of larval culture density. J. Econ. Entom. 78 : 1208 1211.
78. Wilson, T. G., and J. Fabian. 1986. A Drosophila melanogaster mutant resistant to a chemical analog of juvenile hormone. Dev. Biol. 118 : 190 201.
79. Wilson, T. G., S. DeMoor, and J. Lei. 2003. Juvenile hormone involvement in Drosophila melanogaster male reproduction as suggested by the Methoprene-tolerant27 mutant phenotype. Insect Biochem. Mol. Biol. 33 : 1167 1175.
80. Wilson, T. G., M. H. Landers, and G. M. Happ. 1983. Precocene I and II inhibition of vitellogenic oocyte development in Drosophila melanogaster. J. Insect Physiol. 29 : 249 254.
81. Zera, A. J. 2006. Evolutionary genetics of juvenile hormone and ecdysteroid regulation in Gryllus: a case study in the microevolution of endocrine regulation. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 144 : 365 379.
82. Zera, A. J., and L. G. Harshman. 2001. The physiology of life history trade-offs in animals. Annu. Rev. Ecol. Syst. 32 : 95 126.
83. Zera, A. J., and Z. Zhao. 2004. Effect of a juvenile hormone analogue on lipid metabolism in a wing-polymorphic cricket: implications for the endocrine-biochemical bases of life-history trade-offs. Physiol. Biochem. Zool. 77 : 255 266.
84. Zwaan, B., R. Bijlsma, and R. F. Hoekstra. 1995. Direct selection on life span in Drosophila melanogaster. Evolution 49 : 649 659.