Applying the genetic theories of ageing to the cytoplasm: Cytoplasmic genetic covariation for fitness and lifespan

Journal of Evolutionary Biology

Volumn 22, Issue 4, 2009, Pages 818-827

  Dowling, D K ^a   Maklakov, A A ^b,c   Friberg, U ^d   Hailer, F ^e  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UPPSALA UNIVERSITY   (Sweden)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e DEPARTMENT OF PALEOBIOLOGY   (United States)

Author keywords

Ageing; Antagonistic pleiotropy; Cytoplasm; Drosophila melanogaster; Mitochondria; MtDNA; Mutation accumulation; Senescence

Indexed keywords

MITOCHONDRIAL DNA;

AGING; CYTOPLASM; FITNESS; FLY; GENETIC VARIATION; MITOCHONDRIAL DNA; MUTATION; PLEIOTROPY; SENESCENCE;

AGING; ANIMAL; ARTICLE; CYTOPLASM; DROSOPHILA MELANOGASTER; FEMALE; GENETIC VARIABILITY; GENETICS; LONGEVITY; PHYSIOLOGY; REPRODUCTION; TIME;

AGING; ANIMALS; CYTOPLASM; DNA, MITOCHONDRIAL; DROSOPHILA MELANOGASTER; FEMALE; GENETIC VARIATION; LONGEVITY; REPRODUCTION; TIME FACTORS;

DROSOPHILA MELANOGASTER;

EID: 62449285598     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2009.01692.x     Document Type: Article

References (71)

1. Ballard, J.W.O. Whitlock, M.C. 2004. The incomplete natural history of mitochondria. Mol. Ecol. 13 : 729 744.
2. Barnard, G.A. 1984. Comparing the means of two independent samples. Appl. Stat. 33 : 266 271.
3. Berlin, S., Tomaras, D. Charlesworth, B. 2007. Low mitochondrial variability in birds may indicate Hill-Robertson effects on the W chromosome. Heredity 99 : 389 396.
4. Brand, M.D. 2000. Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Exp. Gerontol. 35 : 811 820.
5. Charlesworth, B. 2001. Patterns of age-specific means and genetic variances of mortality rates predicted by the mutation-accumulation theory of ageing. J. Theor. Biol. 210 : 47 65.
6. Clancy, D.J. 2008. Variation in mitochondrial genotype has substantial lifespan effects which may be modulated by nuclear background. Aging Cell 7 : 795 804.
7. Clark, A.G. 1985. Natural selection with nuclear and cytoplasmic transmission. II. Tests with Drosophila from diverse populations. Genetics 111 : 97 112.
8. Clark, A.G. 1987. Senescence and the genetic-correlation hang-up. Am. Nat. 129 : 932 940.
9. Clark, M.E., Anderson, C.L., Cande, J. Karr, T.L. 2005. Widespread prevalence of Wolbachia in laboratory stocks and the implications for Drosophila research. Genetics 170 : 1667 1675.
10. Curtsinger, J.W. Khazaeli, A.A. 2002. Lifespan, QTLs, age-specificity, and pleiotropy in Drosophila. Mech. Ageing Dev. 123 : 81 93.
11. Curtsinger, J.W., Service, P.W. Prout, T. 1994. Antagonistic pleiotropy, reversal of dominance, and genetic polymorphism. Am. Nat. 144 : 210 228.
12. Dowling, D.K., Friberg, U., Hailer, F. Arnqvist, G. 2007. Intergenomic epistasis for fitness: within-population interactions between cytoplasmic and nuclear genes in Drosophila melanogaster. Genetics 175 : 235 244.
13. Dowling, D.K., Friberg, U. Lindell, J. 2008. Evolutionary implications of non-neutral mitochondrial genetic variation. Trends Ecol. Evol. 23 : 546 554.
14. Ferguson, M., Mockett, R.J., Shen, Y., Orr, W.C. Sohal, R.S. 2005. Age-associated decline in mitochondrial respiration and electron transport in Drosophila melanogaster. Biochem. J. 390 : 501 511.
15. Finch, C.E. 1990. Longevity, Senescence, and the Genome. University of Chicago Press, Chicago.
16. Gregorius, H.R. Ross, M.D. 1984. Selection with gene-cytoplasm interaction. I. Maintenance of cytoplasm polymorphisms. Genetics 107 : 165 178.
17. Hamilton, W.D. 1966. The moulding of senescence by natural selection. J. Theor. Biol. 12 : 12 45.
18. Harman, D. 1972. The biologic clock: the mitochondria? J. Am. Geriatr. Soc. 20 : 145 147.
19. Hedrick, P.W. 1999. Antagonistic pleiotropy and genetic polymorphism: a perspective. Heredity 82 : 126 133.
20. Hill, W.G. Robertson, A. 1966. The effect of linkage on limits to artificial selection. Genet. Res. 8 : 269 294.
21. Holland, B. Rice, W.R. 1999. Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proc. Natl Acad. Sci. USA 96 : 5083 5088.
22. Houle, D., Hughes, K.A., Hoffmaster, D.K., Ihara, J., Assimacopoulos, S., Canada, D. Charlesworth, B. 1994. The effects of spontaneous mutation on quantitative traits. I. Variances and covariances of life history traits. Genetics 138 : 773 785.
23. Hughes, K.A. 1995. The evolutionary genetics of male life history characters in Drosophila melanogaster. Evolution 49 : 521 537.
24. Hughes, K.A. Reynolds, R.M. 2005. Evolutionary and mechanistic theories of aging. Annu. Rev. Entomol. 50 : 421 445.
25. Hughes, K.A., Alipaz, J.A., Drnevich, J.M. Reynolds, R.M. 2002. A test of evolutionary theories of aging. Proc. Natl Acad. Sci. USA 99 : 14286 14291.
26. James, A.C. Ballard, J.W.O. 2003. Mitochondrial genotype affects fitness in Drosophila simulans. Genetics 164 : 187 194.
27. Khrapko, K. Vijg, J. 2007. Mitochondrial DNA mutations and ageing: a case closed? Nat. Genet. 39 : 445 446.
28. Khrapko, K., Kraytsberg, Y., de Grey, A.D.N.J., Vijg, J. Schon, E.A. 2006. Does premature ageing of the mtDNA mutator mouse prove that mtDNA mutations are involved in natural ageing? Aging Cell 5 : 279 282.
29. Kondo, R., Satta, Y., Matsuura, E.T., Ishiwa, H., Takahata, N. Chigusa, S.I. 1990. Incomplete maternal transmission of mitochondrial DNA in Drosophila. Genetics 126 : 657 663.
30. Kujoth, G.C., Hiona, A., Pugh, T.D., Someya, S., Panzer, K., Wohlgemuth, S.E., Hofer, T., Seo, A.Y., Sullivan, R., Jobling, W.A., Morrow, J.D., Van Remmen, H., Sedivy, J.M., Yamasoba, T., Tanokura, M., Weindruch, R., Leeuwenburgh, C. Prolla, T.A. 2005. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian ageing. Science 309 : 481 484.
31. Lambert, A.J. Brand, M. 2007. Hot topics: research on mitochondria and aging 2006-2007. Aging Cell 6 : 417 420.
32. Leroi, A.M., Bartke, A., De Benedictis, G., Franceschi, C., Gartner, A., Gonos, E., Fedei, M.E., Kivisild, T., Lee, S., Kartal-Özer, N., Schumacher, M., Sikora, E., Slagboom, E., Tatar, M., Yashin, A.I., Vijg, J. Zwaan, B. 2005. What evidence is there for the existence of individual genes with antagonistic pleiotropic effects? Mech. Ageing Dev. 126 : 421 442.
33. Long, T.A.F., Miller, P.M., Stewart, A.D. Rice, W.R. 2009. Estimating the heritability of female lifetime fecundity in a locally adapted Drosophila melanogaster population. J. Evol. Biol. 22 : 637 643.
34. Lynch, M. 1997. Mutation accumulation in nuclear, organelle, and prokaryotic transfer RNA genes. Mol. Biol. Evol. 14 : 914 925.
35. MacRae, A.F. Anderson, W.W. 1988. Evidence for non-neutrality of mitochondrial DNA haplotypes in Drosophila pseudoobscura. Genetics 120 : 485 494.
36. Maklakov, A.A., Friberg, U., Dowling, D.K. Arnqvist, G. 2006. Within-population variation in cytoplasmic genes affects female life span and ageing in Drosophila melanogaster. Evolution 60 : 2081 2086.
37. Mandavilli, B.S., Santos, J.H. Houten, B.V. 2002. Mitochondrial DNA repair and ageing. Mutat. Res. 509 : 127 151.
38. Medawar, P.B. 1952. An Unsolved Problem of Biology. H.K. Lewis, London.
39. Meiklejohn, C.D., Montooth, K.L. Rand, D.M. 2007. Positive and negative selection on the mitochondrial genome. Trends Genet. 23 : 259 262.
40. Miyo, T. Charlesworth, B. 2004. Age-specific mortality rates of reproducing and non-reproducing males of Drosophila melanogaster. Proc. R. Soc. Lond., B, Biol. Sci. 271 : 2517 2522.
41. Partridge, L. Barton, N.H. 1993. Optimality, mutation and the evolution of ageing. Nature 362 : 305 311.
42. Partridge, L. Gems, D. 2002. Mechanisms of ageing: public or private? Nat. Genet. 3 : 165 175.
43. Pletcher, S.D. 1999. Model fitting and hypothesis testing for age-specific mortality data. J. Evol. Biol. 12 : 430 440.
44. Pletcher, S.D., Houle, D. Curtsinger, J.W. 1998. Age-specific properties of spontaneous mutations affecting mortality in Drosophila melanogaster. Genetics 148 : 287 303.
45. Pletcher, S.D., Houle, D. Curtsinger, J.W. 1999. The evolution of age-specific mortality rates in Drosophila melanogaster: genetic divergence among unselected lines. Genetics 153 : 813 823.
46. Promislow, D.E.L. Tatar, M. 1998. Mutation and senescence: where genetics and demography meet. Genetica 102/103 : 299 314.
47. Rand, D.M. 2001. The units of selection on mitochondrial DNA. Annu. Rev. Ecol. Syst. 32 : 415 448.
48. Rand, D.M., Clark, A.G. Kann, L.M. 2001. Sexually antagonistic cytonuclear fitness interactions in Drosophila melanogaster. Genetics 159 : 173 187.
49. Rand, D.M., Fry, A. Sheldahl, L. 2006. Nuclear-mitochondrial epistasis and Drosophila ageing: introgression of Drosophila simulans mtDNA modifies longevity in D. melanogaster nuclear backgrounds. Genetics 172 : 329 341.
50. Reynolds, R.M., Temiyasathit, S., Reedy, M.M., Ruedi, E.A., Drnevich, J.M., Leips, J. Huges, K.A. 2007. Age specificity of inbreeding load in Drosophila melanogaster and implications for the evolution of late-life mortality plateaus. Genetics 177 : 587 595.
51. Rice, W.R. 1996. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381 : 232 234.
52. Rice, W.R., Linder, J.E., Friberg, U., Lew, T.A., Morrow, E.H. Stewart, A. 2005. Inter-locus antagonistic coevolution as an engine of speciation: assessment with hemiclonal analysis. Proc. Natl Acad. Sci. USA 102 (Suppl. 1 6527 6534.
53. Rose, M.R. 1982. Antagonistic pleiotropy, dominance, and genetic variation. Heredity 48 : 63 78.
54. Rose, M.R. 1984. Genetic covariation in Drosophila life history: untangling the data. Am. Nat. 123 : 565 569.
55. Rose, M.R. 1985. Life history evolution with antagonistic pleiotropy and overlapping generations. Theor. Popul. Biol., 28 : 342 358.
56. Rose, M.R. 1991. Evolutionary Biology of Ageing. Oxford University Press, New York.
57. Rose, M.R. Charlesworth, B. 1981. Genetics of life history in Drosophila melanogaster. I. Sib analysis of adult females. Genetics 97 : 173 186.
58. Schwarze, S.R., Weindruch, R. Aiken, J.M. 1998. Oxidative stress and ageing reduce COX I RNA and cytochrome oxidase activity in Drosophila. Free Radic. Biol. Med. 25 : 740 747.
59. Service, P.M. Rose, M.R. 1985. Genetic covariation among life history components: the effect of novel environments. Evolution 39 : 943 945.
60. Shabalina, S.A., Yampolsky, L.Y. Konrashov, A.S. 1997. Rapid decline of fitness in panmictic populations of Drosophila melanogaster maintained under relaxed natural selection. Proc. Natl Acad. Sci. USA 94 : 13034 13039.
61. Snoke, M.S. Promislow, D.E.L. 2003. Quantitative genetic tests of recent senescence theory: age-specific mortality and male fertility in Drosophila melanogaster. Heredity 91 : 546 556.
62. Sohal, R.S. Weindruch, R. 1996. Oxidative stress, caloric restriction, and ageing. Science 273 : 59 63.
63. Tatar, M., Promislow, D.E.L., Khazaeli, A.A. Curtsinger, J.W. 1996. Age-specific patterns of genetic variance in Drosophila melanogaster. II. Fecundity and its genetic covariance with age-specific mortality. Genetics 143 : 849 858.
64. Trifunovic, A., Wredenberg, A., Falkenberg, M., Spelbrink, J.N., Rovio, A.T., Bruder, C.E., Bohlooly, Y.M., Gidlof, S., Oldfors, A., Wibom, R., Tornell, J., Jacobs, H.T. Larsson, N.G. 2004. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429 : 417 423.
65. Tsaousis, A.D., Martin, D.P., Ladoukakis, E.D., Posada, D. Zouros, E. 2005. Widespread recombination in published animal mtDNA sequences. Mol. Biol. Evol. 22 : 925 933.
66. Vermulst, M., Bielas, J.H., Kujoth, G.C., Ladiges, W.C., Rabinovitch, P.S., Prolla, T.A. Loeb, L.A. 2007. Mitochondrial point mutations do not limit the natural lifespan of mice. Nat. Genet. 39 : 540 543.
67. Wallace, D.C. 1997. Mitochondrial DNA in ageing and disease. Sci. Am. 277 : 40 47.
68. Wayne, M.L., Telonis-Scott, M., Bono, L.M., Harshman, L., Kopp, A., Nuzhdin, S.V. McIntyre, L.M. 2007. Simpler mode of inheritance of transcriptional variation in male Drosophila melanogaster. Proc. Natl Acad. Sci. USA 104 : 18577 18582.
69. Williams, G.C. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11 : 398 411.
70. Yan, L.J., Levine, R.L. Sohal, R.S. 1997. Oxidative damage during ageing targets mitochondrial aconitase. Proc. Natl Acad. Sci. USA 94 : 11168 11172.
71. Zwaan, B.J. 1999. The evolutionary genetics of ageing and longevity. Heredity 82 : 589 597.