Reproductive and post-reproductive life history of wild-caught Drosophila melanogaster under laboratory conditions

Journal of Evolutionary Biology

Volumn 26, Issue 7, 2013, Pages 1508-1520

  Klepsatel, P ^a   Galikova M ^a   De Maio, N ^a   Ricci, S ^b   Schlotterer C ^a   Flatt, T ^a,c  

^a Institut fur Populationsgenetik   (Austria)

^b UNIVERSITY OF PISA   (Italy)

^c Wissenschaftskolleg zu Berlin   (Germany)

Author keywords

Drosophila melanogaster; Individual fecundity; Laboratory conditions; Life history; Post reproductive lifespan; Reproductive senescence; Reproductive success; Wild caught populations

Indexed keywords

BIOACCUMULATION; FECUNDITY; FITNESS; FLY; GENOTYPE; HATCHING; LABORATORY METHOD; LIFE HISTORY TRAIT; MUTATION; REPRODUCTIVE BEHAVIOR; REPRODUCTIVE SUCCESS; SENESCENCE; WILD POPULATION;

AGE; ANIMAL; ARTICLE; BIOLOGICAL MODEL; DROSOPHILA MELANOGASTER; EGG LAYING; FEMALE; FERTILITY; GENETICS; INDIVIDUAL FECUNDITY; LABORATORY; LABORATORY CONDITIONS; LIFE HISTORY; MALE; OVARY; PHENOTYPE; PHYSIOLOGY; POST-REPRODUCTIVE LIFESPAN; REPRODUCTION; REPRODUCTIVE SENESCENCE; REPRODUCTIVE SUCCESS; WILD-CAUGHT POPULATIONS;

DROSOPHILA MELANOGASTER; INDIVIDUAL FECUNDITY; LABORATORY CONDITIONS; LIFE HISTORY; POST-REPRODUCTIVE LIFESPAN; REPRODUCTIVE SENESCENCE; REPRODUCTIVE SUCCESS; WILD-CAUGHT POPULATIONS;

AGE FACTORS; ANIMALS; DROSOPHILA MELANOGASTER; FEMALE; FERTILITY; LABORATORIES; MALE; MODELS, BIOLOGICAL; OVARY; OVIPOSITION; PHENOTYPE; REPRODUCTION;

DROSOPHILA MELANOGASTER;

EID: 84880702159     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12155     Document Type: Article

References (82)

1. Ackermann, M., Bijlsma, R., James, A.C., Partridge, L., Zwaan, B.J. & Stearns, S.C. 2001. Effects of assay conditions in life history experiments with Drosophila melanogaster. J. Evol. Biol. 14: 199-209.
2. Aigaki, T. & Ohba, S. 1984. Individual analysis of age-associated changes in reproductive activity and lifespan of Drosophila virilis. Exp. Gerontol. 19: 13-23.
3. Broekmans, F.J., Knauff, E.A.H., Velde, E.R.T., Macklon, N.S. & Fauser, B.C. 2007. Female reproductive ageing: current knowledge and future trends. Trends Endocrinol. Metab. 18: 58-65.
4. Carey, J.R., Liedo, P., Müller, H.G., Wang, J.L. & Vaupel, J.W. 1998. A simple graphical technique for displaying individual fertility data and cohort survival: case study of 1000 Mediterranean Fruit Fly females. Func. Ecol. 12: 359-363.
5. Charlesworth, B. 1990. Optimization models, quantitative genetics, and mutation. Evolution 44: 520-538.
6. Chippindale, A.K., Leroi, A.M., Kim, S.B. & Rose, M.R. 1993. Phenotypic plasticity and selection in Drosophila life-history evolution. I. Nutrition and the cost of reproduction. J. Evol. Biol. 6: 171-193.
7. Clark, A.G. 1987. Senescence and the genetic-correlation hang-up. Am. Nat. 129: 932-940.
8. Cohen, A.A. 2004. Female post-reproductive lifespan: a general mammalian trait. Biol. Rev. Camb. Philos. Soc. 79: 733-750.
9. David, J.R., Biémont, C. & Fouillet, P. 1974. Sur la forme des courbes de ponte de Drosophila melanogaster et leur adjustment á des modèles mathématiques. Arch. Zool. Exp. Gen. 115: 263-277.
10. David, J.R., Cohet, Y. & Fouillet, P. 1975. The variability between individuals as a measure of senescence: a study of the number of eggs laid and the percentage of hatched eggs in the case of Drosophila melanogaster. Exp. Gerontol. 10: 17-25.
11. Dobzhansky, T., Lewontin, R.C. & Pavlovsky, O. 1964. The capacity for increase in chromosomally polymorphic and monomorphic populations of Drosophila pseudoobscura. Heredity 19: 597-614.
12. Draye, X., Bullens, P. & Lints, F.A. 1994. Geographic variations of life history strategies in Drosophila melanogaster. I. Analysis of wild-caught populations. Exp. Gerontol. 29: 205-222.
13. von Ende, C.N. 2001. Repeated-measures analysis: growth and other time-dependent measures. In: Design and Analysis of Ecological Experiments (S.M. Scheiner & J. Gurevitch, eds), pp. 134-157. Oxford University Press, Oxford.
14. Flatt, T. 2009. Ageing: diet and longevity in the balance. Nature 462: 989-990.
15. Flatt, T. 2011. Survival costs of reproduction in Drosophila. Exp. Gerontol. 46: 369-375.
16. Flatt, T. & Heyland, A. (eds) 2011. Mechanisms of Life History Evolution - The Genetics and Physiology of Life History Traits and Trade-Offs. Oxford University Press, Oxford.
17. Flatt, T. & Schmidt, P.S. 2009. Integrating evolutionary and molecular genetics of aging. Biochim. Biophys. Acta 1790: 951-962.
18. Flatt, T., Min, K.J., D'Alterio, C., Villa-Cuesta, E., Cumbers, J., Lehmann, R. et al. 2008. Drosophila germ-line modulation of insulin signaling and lifespan. Proc. Natl. Acad. Sci. USA 105: 6368-6373.
19. Frankham, R. & Loebel, D.A. 1992. Modeling problems in conservation genetics using captive Drosophila populations: rapid genetic adaptation to captivity. Zoo Biol. 11: 333-342.
20. Giesel, J.T. 1986. Genetic correlation structure of life history variables in outbred, wild Drosophila melanogaster: effects of photoperiod regimen. Am. Nat. 128: 593-603.
21. Giesel, J.T., Murphy, P.A. & Manlove, M.N. 1982. The influence of temperature on genetic interrelationships of life history traits in a population of Drosophila melanogaster: what tangled data sets we weave. Am. Nat. 119: 464.
22. Grandison, R.C., Piper, M.D.W. & Partridge, L. 2009. Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature 462: 1061-1065.
23. Gruntenko, N.E., Bownes, M., Terashima, J., Sukhanova, M. & Raushenbach, I.Y. 2003. Heat stress affects oogenesis differently in wild-type Drosophila virilis and a mutant with altered juvenile hormone and 20-hydroxyecdysone levels. Insect Mol. Biol. 12: 393-404.
24. Harshman, L.G. & Hoffmann, A.A. 2000. Laboratory selection experiments using Drosophila: what do they really tell us? Trends Ecol. Evol. 15: 32-36.
25. Hawkes, K., O'Connell, J.F., Jones, N.G.B., Alvarez, H. & Charnov, E.L. 1998. Grandmothering, menopause, and the evolution of human life histories. Proc. Natl. Acad. Sci. USA 95: 1336-1339.
26. Houle, D. 1991. Genetic covariance of fitness correlates: what genetic correlations are made of and why it matters. Evolution 45: 630-648.
27. Houle, D. 2001. Characters as the units of evolutionary change. In: The Character Concept in Evolutionary Biology (G.P. Wagner, eds), pp. 109-140. Academic Press, San Diego.
28. Houle, D. & Rowe, L. 2003. Natural selection in a bottle. Am. Nat. 161: 50-67.
29. Houle, D., Hughes, K.A., Hoffmaster, D.K., Ihara, J., Assimacopoulos, S., Canada, D. et al. 1994. The effects of spontaneous mutation on quantitative traits. I. Variances and covariances of life history traits. Genetics 138: 773-785.
30. Hughes, S.E., Evason, K., Xiong, C.J. & Kornfeld, K. 2007. Genetic and pharmacological factors that influence reproductive aging in nematodes. PLoS Genet. 3: 254-265.
31. Khazaeli, A.A. & Curtsinger, J.W. 2010a. Post-reproductive survival and the Faulkner Effect in Drosophila melanogaster. Dros. Inf. Serv. 93: 154-155.
32. Khazaeli, A.A. & Curtsinger, J.W. 2010b. Life history variation in an artificially selected population of Drosophila melanogaster: pleiotropy, superflies, and age-specific adaptation. Evolution 64: 3409-3416.
33. Khazaeli, A.A. & Curtsinger, J.W. 2013. Pleiotropy and Life History Evolution in Drosophila melanogaster: Uncoupling Life Span and Early Fecundity. J. Gerontol. A Biol. Sci. Med. Sci. 68: 546-553.
34. Kindlmann, P., Dixon, A.F.G. & Dostálková, I. 2001. Role of ageing and temperature in shaping reaction norms and fecundity functions in insects. J. Evol. Biol. 14: 835-840.
35. King, R.C. 1970. Ovarian Development in Drosophila melanogaster. Academic Press, New York, NY.
36. Kirkwood, T.B.L. & Shanley, D.P. 2010. The connections between general and reproductive senescence and the evolutionary basis of menopause. Ann. N. Y. Acad. Sci. 1204: 21-29.
37. Kuo, T.-H., Yew, J.Y., Fedina, T.Y., Dreisewerd, K., Dierick, H.A. & Pletcher, S.D. 2012. Aging modulates cuticular hydrocarbons and sexual attractiveness in Drosophila melanogaster. J. Exp. Biol. 215: 814-821.
38. Linnen, C., Tatar, M. & Promislow, D. 2001. Cultural artifacts: a comparison of senescence in natural, laboratory-adapted and artificially selected lines of Drosophila melanogaster. Evol. Ecol. Res. 3: 877-888.
39. Luckinbill, L.S., Arking, R., Clare, M.J., Cirocco, W.C. & Buck, S.A. 1984. Selection for Delayed Senescence in Drosophila melanogaster. Evolution 38: 996-1003.
40. Luo, S. & Murphy, C.T. 2011. Caenorhabditis elegans reproductive aging: regulation and underlying mechanisms. Genesis 49: 53-65.
41. Luo, S., Shaw, W.M., Ashraf, J. & Murphy, C.T. 2009. TGF-beta Sma/Mab signaling mutations uncouple reproductive aging from somatic aging. PLoS Genet. 5: e1000789.
42. Luo, S., Kleemann, G.A., Ashraf, J.M., Shaw, W.M. & Murphy, C.T. 2010. TGF-beta and insulin signaling regulate reproductive aging via oocyte and germline quality maintenance. Cell 143: 299-312.
43. Margolis, J. & Spradling, A. 1995. Identification and behavior of epithelial stem-cells in the Drosophila ovary. Development 121: 3797-3807.
44. Matos, M., Rose, M.R., Rocha Pité, M.T., Rego, C. & Avelar, T. 2000. Adaptation to the laboratory environment in Drosophila subobscura. J. Evol. Biol. 13: 9-19.
45. McCall, K. 2004. Eggs over easy: cell death in the Drosophila ovary. Dev. Biol. 274: 3-14.
46. Mueller, L.D., Rauser, C.L. & Rose, M.R. 2007. An evolutionary heterogeneity model of late-life fecundity in Drosophila. Biogerontology 8: 147-161.
47. Mueller, L.D., Shahrestani, P. & Rauser, C.L. 2009. Predicting death in female Drosophila. Exp. Gerontol. 44: 766-772.
48. Nelder, J.A. & Mead, R. 1965. A simplex method for function minimization. Computer J. 7: 308-313.
49. van Noordwijk, A. & de Jong, G. 1986. Acquisition and allocation of resources: their influence on variation in life history tactics. Am. Nat. 128: 137-142.
50. Novoseltsev, V.N., Arking, R., Novoseltseva, J.A. & Yashin, A.I. 2002. Evolutionary optimality applied to Drosophila experiments: hypothesis of constrained reproductive efficiency. Evolution 56: 1136-1149.
51. Novoseltsev, V.N., Novoseltseva, J.A. & Yashin, A.I. 2003. What does a fly's individual fecundity pattern look like? The dynamics of resource allocation in reproduction and ageing. Mech. Ageing Dev. 124: 605-617.
52. Novoseltsev, V.N., Arking, R., Carey, J.R., Novoseltseva, J.A. & Yashin, A.I. 2004. How an individual fecundity pattern looks in Drosophila and medflies. Ann. N. Y. Acad. Sci. 1019: 577-580.
53. Novoseltsev, V.N., Arking, R., Carey, J.R., Novoseltseva, J.A. & Yashin, A.I. 2005. Individual fecundity and senescence in Drosophila and medfly. J. Gerontol. A Biol. Sci. Med. Sci. 60: 953-962.
54. Paaby, A.B. & Schmidt, P.S. 2009. Dissecting the genetics of longevity in Drosophila melanogaster. Fly 3: 29-38.
55. Pan, L., Chen, S.Y., Weng, C.J., Call, G., Zhu, D.X., Tang, H. et al. 2007. Stem cell aging is controlled both intrinsically and extrinsically in the Drosophila ovary. Cell Stem Cell 1: 458-469.
56. Partridge, L., Prowse, N. & Pignatelli, P. 1999. Another set of responses and correlated responses to selection on age at reproduction in Drosophila melanogaster. Proc. R. Soc. Lond. B Biol. Sci. 266: 255-261.
57. Partridge, L., Gems, D. & Withers, D.J. 2005. Sex and death: what is the connection? Cell 120: 461-472.
58. Pekkala, N., Kotiaho, J.S. & Puurtinen, M. 2011. Laboratory relationships between adult lifetime reproductive success and fitness surrogates in a Drosophila littoralis population. PLoS ONE 6: e24560.
59. Pletcher, S.D., Houle, D. & Curtsinger, J.W. 1998. Age-specific properties of spontaneous mutations affecting mortality in Drosophila melanogaster. Genetics 148: 287-304.
60. Prasad, N.G. & Joshi, A. 2003. What have two decades of laboratory life-history evolution studies on Drosophila melanogaster taught us? J. Genet. 82: 45-76.
61. Promislow, D.E. & Tatar, M. 1998. Mutation and senescence: where genetics and demography meet. Genetica 102-103: 299-314.
62. Rauser, C.L., Abdel-Aal, Y., Shieh, J.A., Suen, C.W., Mueller, L.D. & Rose, M.R. 2005. Lifelong heterogeneity in fecundity is insufficient to explain late-life fecundity plateaus in Drosophila melanogaster. Exp. Gerontol. 40: 660-670.
63. Reznick, D., Nunney, L. & Tessier, A. 2000. Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol. Evol. 15: 421-425.
64. Reznick, D., Bryant, M. & Holmes, D. 2006. The evolution of senescence and post-reproductive lifespan in guppies (Poecilia reticulata). PLoS Biol. 4: e7.
65. Rogina, B., Wolverton, T., Bross, T.G., Chen, K., Muller, H.G. & Carey, J.R. 2007. Distinct biological epochs in the reproductive life of female Drosophila melanogaster. Mech. Ageing Dev. 128: 477-485.
66. Rose, M.R. 1984. Genetic covariation in Drosophila life history: untangling the data. Am. Nat. 123: 565-569.
67. Rose, M.R., Passananti, H.B. & Matos, M. 2004. Methuselah Flies - A Case Study in the Evolution of Aging. World Scientific, Singapore.
68. Rosewell, J. & Shorrocks, B. 1987. The implication of survival rates in natural populations of Drosophila - capture recapture experiments on domestic Species. Biol. J. Linn. Soc. 32: 373-384.
69. Schmidt, P.S. & Paaby, A.B. 2008. Reproductive diapause and life-history clines in North American populations of Drosophila melanogaster. Evolution 62: 1204-1215.
70. Service, P.M. & Rose, M.R. 1985. Genetic covariation among life-history components: the effects of novel environments. Evolution 39: 943-945.
71. Sgrò, C.M. & Partridge, L. 2000. Evolutionary responses of the life history of wild-caught Drosophila melanogaster to two standard methods of laboratory culture. Am. Nat. 156: 341-353.
72. Shanley, D.P. & Kirkwood, T.B.L. 2001. Evolution of the human menopause. BioEssays 23: 282-287.
73. Shanley, D.P., Sear, R., Mace, R. & Kirkwood, T.B. 2007. Testing evolutionary theories of menopause. Proc. R. Soc. Lond. B Biol. Sci. 274: 2943-2949.
74. Stearns, S.C. 1992. The Evolution of Life Histories. Oxford University Press, Oxford.
75. Stearns, S.C. & Partridge, L. 2001. The genetics of aging in Drosophila. In: Handbook of the Biology of Aging (E. Masoro & S. Austad, eds), pp. 353-368. Academic Press, San Diego.
76. Stearns, S.C., Ackermann, M., Doebeli, M. & Kaiser, M. 2000. Experimental evolution of aging, growth, and reproduction in fruitflies. Proc. Natl. Acad. Sci. USA 97: 3309-3313.
77. Tatar, M., Bartke, A. & Antebi, A. 2003. The endocrine regulation of aging by insulin-like signals. Science 299: 1346-1351.
78. Tokunaga, C. 1970. The effects of low temperature and aging on nondisjunction in Drosophila. Genetics 65: 75-94.
79. Tully, T. & Lambert, A. 2011. The evolution of postreproductive life span as an insurance against indeterminacy. Evolution 65: 3013-3020.
80. Velde, E.R.T. & Pearson, P.L. 2002. The variability of female reproductive ageing. Hum. Reprod. Update 8: 141-154.
81. Zhao, R., Xuan, Y., Li, X. & Xi, R. 2008. Age-related changes of germline stem cell activity, niche signaling activity and egg production in Drosophila. Aging Cell 7: 344-354.
82. Zwaan, B., Bijlsma, R. & Hoekstra, R.F. 1995. Direct selection on life span in Drosophila melanogaster. Evolution 49: 649-659.