Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 2000 Jan;154(1):213–227. doi: 10.1093/genetics/154.1.213

Genotype-environment interaction for quantitative trait loci affecting life span in Drosophila melanogaster.

C Vieira 1, E G Pasyukova 1, Z B Zeng 1, J B Hackett 1, R F Lyman 1, T F Mackay 1
PMCID: PMC1460900  PMID: 10628982

Abstract

The nature of genetic variation for Drosophila longevity in a population of recombinant inbred lines was investigated by estimating quantitative genetic parameters and mapping quantitative trait loci (QTL) for adult life span in five environments: standard culture conditions, high and low temperature, and heat-shock and starvation stress. There was highly significant genetic variation for life span within each sex and environment. In the analysis of variance of life span pooled over sexes and environments, however, the significant genetic variation appeared in the genotype x sex and genotype x environment interaction terms. The genetic correlation of longevity across the sexes and environments was not significantly different from zero in these lines. We estimated map positions and effects of QTL affecting life span by linkage to highly polymorphic roo transposable element markers, using a multiple-trait composite interval mapping procedure. A minimum of 17 QTL were detected; all were sex and/or environment-specific. Ten of the QTL had sexually antagonistic or antagonistic pleiotropic effects in different environments. These data provide support for the pleiotropy theory of senescence and the hypothesis that variation for longevity might be maintained by opposing selection pressures in males and females and variable environments. Further work is necessary to assess the generality of these results, using different strains, to determine heterozygous effects and to map the life span QTL to the level of genetic loci.

Full Text

The Full Text of this article is available as a PDF (267.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arking R. Successful selection for increased longevity in Drosophila: analysis of the survival data and presentation of a hypothesis on the genetic regulation of longevity. Exp Gerontol. 1987;22(3):199–220. doi: 10.1016/0531-5565(87)90040-4. [DOI] [PubMed] [Google Scholar]
  2. Bodnar A. G., Ouellette M., Frolkis M., Holt S. E., Chiu C. P., Morin G. B., Harley C. B., Shay J. W., Lichtsteiner S., Wright W. E. Extension of life-span by introduction of telomerase into normal human cells. Science. 1998 Jan 16;279(5349):349–352. doi: 10.1126/science.279.5349.349. [DOI] [PubMed] [Google Scholar]
  3. Buck S., Nicholson M., Dudas S., Wells R., Force A., Baker G. T., 3rd, Arking R. Larval regulation of adult longevity in a genetically-selected long-lived strain of Drosophila. Heredity (Edinb) 1993 Jul;71(Pt 1):23–32. doi: 10.1038/hdy.1993.103. [DOI] [PubMed] [Google Scholar]
  4. Finch C. E., Tanzi R. E. Genetics of aging. Science. 1997 Oct 17;278(5337):407–411. doi: 10.1126/science.278.5337.407. [DOI] [PubMed] [Google Scholar]
  5. Force A. G., Staples T., Soliman S., Arking R. Comparative biochemical and stress analysis of genetically selected Drosophila strains with different longevities. Dev Genet. 1995;17(4):340–351. doi: 10.1002/dvg.1020170407. [DOI] [PubMed] [Google Scholar]
  6. Gillespie J. H., Turelli M. Genotype-environment interactions and the maintenance of polygenic variation. Genetics. 1989 Jan;121(1):129–138. doi: 10.1093/genetics/121.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gurganus M. C., Fry J. D., Nuzhdin S. V., Pasyukova E. G., Lyman R. F., Mackay T. F. Genotype-environment interaction at quantitative trait loci affecting sensory bristle number in Drosophila melanogaster. Genetics. 1998 Aug;149(4):1883–1898. doi: 10.1093/genetics/149.4.1883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Harrison D. E., Archer J. R. Genetic differences in effects of food restriction on aging in mice. J Nutr. 1987 Feb;117(2):376–382. doi: 10.1093/jn/117.2.376. [DOI] [PubMed] [Google Scholar]
  9. Houle D. Comparing evolvability and variability of quantitative traits. Genetics. 1992 Jan;130(1):195–204. doi: 10.1093/genetics/130.1.195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Houle D., Morikawa B., Lynch M. Comparing mutational variabilities. Genetics. 1996 Jul;143(3):1467–1483. doi: 10.1093/genetics/143.3.1467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hughes K. A., Charlesworth B. A genetic analysis of senescence in Drosophila. Nature. 1994 Jan 6;367(6458):64–66. doi: 10.1038/367064a0. [DOI] [PubMed] [Google Scholar]
  12. Jiang C., Zeng Z. B. Multiple trait analysis of genetic mapping for quantitative trait loci. Genetics. 1995 Jul;140(3):1111–1127. doi: 10.1093/genetics/140.3.1111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Khazaeli A. A., Tatar M., Pletcher S. D., Curtsinger J. W. Heat-induced longevity extension in Drosophila. I. Heat treatment, mortality, and thermotolerance. J Gerontol A Biol Sci Med Sci. 1997 Jan;52(1):B48–B52. doi: 10.1093/gerona/52a.1.b48. [DOI] [PubMed] [Google Scholar]
  14. Kimura K. D., Tissenbaum H. A., Liu Y., Ruvkun G. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science. 1997 Aug 15;277(5328):942–946. doi: 10.1126/science.277.5328.942. [DOI] [PubMed] [Google Scholar]
  15. Kirkwood T. B., Rose M. R. Evolution of senescence: late survival sacrificed for reproduction. Philos Trans R Soc Lond B Biol Sci. 1991 Apr 29;332(1262):15–24. doi: 10.1098/rstb.1991.0028. [DOI] [PubMed] [Google Scholar]
  16. Lai C., Lyman R. F., Long A. D., Langley C. H., Mackay T. F. Naturally occurring variation in bristle number and DNA polymorphisms at the scabrous locus of Drosophila melanogaster. Science. 1994 Dec 9;266(5191):1697–1702. doi: 10.1126/science.7992053. [DOI] [PubMed] [Google Scholar]
  17. Lin K., Dorman J. B., Rodan A., Kenyon C. daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science. 1997 Nov 14;278(5341):1319–1322. doi: 10.1126/science.278.5341.1319. [DOI] [PubMed] [Google Scholar]
  18. Lin Y. J., Seroude L., Benzer S. Extended life-span and stress resistance in the Drosophila mutant methuselah. Science. 1998 Oct 30;282(5390):943–946. doi: 10.1126/science.282.5390.943. [DOI] [PubMed] [Google Scholar]
  19. Lithgow G. J. Invertebrate gerontology: the age mutations of Caenorhabditis elegans. Bioessays. 1996 Oct;18(10):809–815. doi: 10.1002/bies.950181007. [DOI] [PubMed] [Google Scholar]
  20. Lithgow G. J., White T. M., Melov S., Johnson T. E. Thermotolerance and extended life-span conferred by single-gene mutations and induced by thermal stress. Proc Natl Acad Sci U S A. 1995 Aug 1;92(16):7540–7544. doi: 10.1073/pnas.92.16.7540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Long A. D., Lyman R. F., Langley C. H., Mackay T. F. Two sites in the Delta gene region contribute to naturally occurring variation in bristle number in Drosophila melanogaster. Genetics. 1998 Jun;149(2):999–1017. doi: 10.1093/genetics/149.2.999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lyman R. F., Lawrence F., Nuzhdin S. V., Mackay T. F. Effects of single P-element insertions on bristle number and viability in Drosophila melanogaster. Genetics. 1996 May;143(1):277–292. doi: 10.1093/genetics/143.1.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lyman R. F., Mackay T. F. Candidate quantitative trait loci and naturally occurring phenotypic variation for bristle number in Drosophila melanogaster: the Delta-Hairless gene region. Genetics. 1998 Jun;149(2):983–998. doi: 10.1093/genetics/149.2.983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mackay T. F., Langley C. H. Molecular and phenotypic variation in the achaete-scute region of Drosophila melanogaster. Nature. 1990 Nov 1;348(6296):64–66. doi: 10.1038/348064a0. [DOI] [PubMed] [Google Scholar]
  25. McClearn G. E., Johansson B., Berg S., Pedersen N. L., Ahern F., Petrill S. A., Plomin R. Substantial genetic influence on cognitive abilities in twins 80 or more years old. Science. 1997 Jun 6;276(5318):1560–1563. doi: 10.1126/science.276.5318.1560. [DOI] [PubMed] [Google Scholar]
  26. Morris J. Z., Tissenbaum H. A., Ruvkun G. A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature. 1996 Aug 8;382(6591):536–539. doi: 10.1038/382536a0. [DOI] [PubMed] [Google Scholar]
  27. Niedzwiecki A., Kongpachith A. M., Fleming J. E. Aging affects expression of 70-kDa heat shock proteins in Drosophila. J Biol Chem. 1991 May 15;266(14):9332–9338. [PubMed] [Google Scholar]
  28. Nuzhdin S. V., Pasyukova E. G., Dilda C. L., Zeng Z. B., Mackay T. F. Sex-specific quantitative trait loci affecting longevity in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1997 Sep 2;94(18):9734–9739. doi: 10.1073/pnas.94.18.9734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Orr W. C., Sohal R. S. Extension of life-span by overexpression of superoxide dismutase and catalase in Drosophila melanogaster. Science. 1994 Feb 25;263(5150):1128–1130. doi: 10.1126/science.8108730. [DOI] [PubMed] [Google Scholar]
  30. Pasyukova E. G., Nuzhdin S. V. Doc and copia instability in an isogenic Drosophila melanogaster stock. Mol Gen Genet. 1993 Aug;240(2):302–306. doi: 10.1007/BF00277071. [DOI] [PubMed] [Google Scholar]
  31. Promislow D. E., Tatar M., Khazaeli A. A., Curtsinger J. W. Age-specific patterns of genetic variance in Drosophila melanogaster. I. Mortality. Genetics. 1996 Jun;143(2):839–848. doi: 10.1093/genetics/143.2.839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rose M. R., Charlesworth B. Genetics of life history in Drosophila melanogaster. I. Sib analysis of adult females. Genetics. 1981 Jan;97(1):173–186. doi: 10.1093/genetics/97.1.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rose M. R., Charlesworth B. Genetics of life history in Drosophila melanogaster. II. Exploratory selection experiments. Genetics. 1981 Jan;97(1):187–196. doi: 10.1093/genetics/97.1.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rose M., Charlesworth B. A test of evolutionary theories of senescence. Nature. 1980 Sep 11;287(5778):141–142. doi: 10.1038/287141a0. [DOI] [PubMed] [Google Scholar]
  35. Tower J. Aging mechanisms in fruit files. Bioessays. 1996 Oct;18(10):799–807. doi: 10.1002/bies.950181006. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES