BREAKDOWN IN CORRELATIONS DURING LABORATORY EVOLUTION. I. COMPARATIVE ANALYSES OF DROSOPHILA POPULATIONS
John P. Phelan
Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697
University of California Los Angeles, Life Sciences Building, Box 951606, Los Angeles, California 90095–1606; E-mail: [email protected].
Search for more papers by this authorMargaret A. Archer
Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697
Search for more papers by this authorKelly A. Beckman
Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697
Search for more papers by this authorAdam K. Chippindale
Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697
Department of Biology, Queen's University, Kingston, Ontario K7L 3N6 Canada.
Search for more papers by this authorTheodore J. Nusbaum
Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697
Search for more papers by this authorMichael R. Rose
Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697
Search for more papers by this authorJohn P. Phelan
Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697
University of California Los Angeles, Life Sciences Building, Box 951606, Los Angeles, California 90095–1606; E-mail: [email protected].
Search for more papers by this authorMargaret A. Archer
Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697
Search for more papers by this authorKelly A. Beckman
Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697
Search for more papers by this authorAdam K. Chippindale
Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697
Department of Biology, Queen's University, Kingston, Ontario K7L 3N6 Canada.
Search for more papers by this authorTheodore J. Nusbaum
Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697
Search for more papers by this authorMichael R. Rose
Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697
Search for more papers by this authorAbstract
Abstract We provide evidence from comparisons of populations of Drosophila that evolutionary correlations between longevity and stress resistance break down over the course of laboratory evolution. Using 15 distinct evolutionary regimes, we created 75 populations that were differentiated for early fecundity, longevity, starvation resistance, desiccation resistance, and developmental time. In earlier experiments, selection for postponed aging produced increases in stress resistance, whereas selection for increased stress resistance produced increases in longevity. Direct estimates of correlations also indicated an antagonistic relationship between early fecundity on one hand and longevity or stress resistance on the other. Laboratory evolution of extreme values of stress resistance, however, led to a breakdown in these evolutionary relationships. There was no evidence that these significant changes in correlation resulted from genotype-by-environment interactions or inbreeding. These findings suggest that correlations between functional characters are not necessarily durable features of a species, and that short-term evolutionary responses cannot be extrapolated reliably to longer-term evolutionary patterns.
Literature Cited
- Archer, M. A., J. P. Phelan, K. A. Beckman, and M. R. Rose. 2003. Breakdown in correlations during laboratory evolution. II. Selection on stress resistance in Drosophila populations. Evolution. 57: 536–543.
- Ariyo, O. J., and M. A. Ayo-Vaughn 2000. Analysis of genotype x environment interaction of okra (Abelmoschus esculentus (L) Moench). J. Genet. Breed.. 54: 35–40.
- Bohren, B. B., W. G. Hill, and A. Robertson 1966. Some observations on asymmetrical correlated responses to selection. Genet. Res.. 7: 44–57.
- Bulmer, M. G. 1985. The mathematical theory of quantitative genetics. Clarendon Press, Oxford , U.K .
- Burris, M. J., and A. E. Bell 1965. Responses to combined selection for the genetically correlated traits of larval weight and pupal weight in Tribolium castaneum. Genetics. 52: 431–432.
- Chippindale, A. K., A. M. Leroi, S. B. Kim, and M. R. Rose 1993. Phenotypic plasticity and selection in Drosophila life history evolution. I. Nutrition and the cost of reproduction. J. Evol. Biol.. 6: 171–193.
- Chippindale, A. K., J. A. Alipaz, H. Chen, and M. R. Rose 1997. Experimental evolution of accelerated development in Drosoph-ila. 1. Larval development speed and survival. Evolution. 51: 1536–1551.
- Dempster, E. R., I. M. Lerner, and D. C. Lowery 1952. Continuous selection for egg production in poultry. Genetics. 37: 693–708.
- Djawdan, M., A. K. Chippindale, M. R. Rose, and T. J. Bradley 1998. Metabolic reserves and evolved stress resistance in Dro-sophila melanogaster. Physiol. Zool.. 71: 584–594.
- Falconer, D. S., and T. F. C. Mackay 1996. Introduction to quantitative genetics. 4th ed. Longman, Essex , U.K .
- Friars, G. W., B. B. Bohren, and H. E. McKean 1962. Time trends in estimates of genetic parameters in a population of chickens subjected to multiple objective selection. Poult. Sci. 41: 1773–1784.
- Gibbs, A., A. K. Chippindale, and M. R. Rose 1997. Physiological mechanisms of evolved desiccation resistance in Drosophila melanogaster. J. Exp. Biol.. 200: 1821–1832.
- Hutchinson, E. W., and M. R. Rose 1991. Quantitative genetics of postponed aging in Drosophila melanogaster. I. Analysis of out-bred populations. Genetics. 127: 719–727.
- Ives, P. T. 1970. Further studies of the South Amherst population of Drosophila melanogaster. Evolution. 38: 507–518.
- Jazwinski, S. M. 1996. Longevity, genes, and aging. Science. 273: 54–59.
- Kennedy, B. K., N. R. Austriaco, J. S. Zhang, and L. Guarente 1995. Mutation in the silencing gene SIR4 can delay aging in S. cerevisiae. Cell. 80: 485–496.
- Leroi, A. M., M. R. Rose, and G. V. Lauder 1994a. What does the comparative method reveal about adaptation? Am. Nat. 143: 381–402.
- Leroi, A. M., A. K. Chippindale, and M. R. Rose 1994b. Long-term laboratory evolution of a genetic life-history trade-off in Drosophila melanogaster. 1. The role of genotype x environment interaction.. Evolution. 48: 1244–1257.
- Leroi, A. M., W. R. Chen, and M. R. Rose 1994c. Long-term laboratory evolution of a genetic trade-off in Drosophila melanogaster. 2. Stability of genetic correlations. Evolution. 48: 1258–1268.
- Lin, Y. J., L. Seroude, and S. Benzer 1998. Extended life-span and stress resistance in the Drosophila mutant methuselah. Science. 282: 943–946.
- Mousseau, T. A., and H. Dingle 1991. Maternal effects in insect life histories. Annu. Rev. Entomol.. 36: 511–534.
- Morris, C. A., R. L. Baker, S. M. Hickey, D. L. Johnson, N. G. Cullen, and J. A. Wilson 1993. Evidence of genotype by environment interaction for reproductive and maternal traits in beef cattle. Anim. Prod.. 56: 69–83.
- Rose, M. R. 1984a. Genetic covariation in Drosophila life history: untangling the data. Am. Nat.. 123: 565–569.
- 1984b. Laboratory evolution of postponed senescence in Drosophila melanogaster. Evolution. 38: 1004–1010.
- Rose, M. R., and B. Charlesworth 1981. Genetics of life history in Drosophila melanogaster. II. Exploratory selection experiments. Genetics. 97: 187–196.
- Rose, M. R., J. L. Graves, and E. W. Hutchinson 1990. The use of selection to probe patterns of pleiotropy in fitness characters. Pp. 29–42 in F. Gilbert, ed Insect life cycles: genetics, evolution, and coordination. Springer, London .
- Rose, M. R., L. N. Vu, S. U. Park, and J. L. Graves 1992. Selection on stress resistance increases longevity in Drosophila melanogaster. Exp. Gerontol.. 27: 241–250.
- Rose, M. R., T. J. Nusbaum, and A. K. Chippindale 1996. Laboratory evolution: the experimental wonderland and the Cheshire cat syndrome. Pp. 221–241 in M. R. Rose and G. V. Lauder, eds Adaptation. Academic Press, San Diego , CA .
- Scheiner, S. M., and C. A. Istock 1991. Correlational selection on life history traits in the pitcher-plant mosquito. Genetica. 84: 123–128.
- Sen, B. K., and A. Robertson 1964. An experimental examination of methods for the simultaneous selection of two characters using Drosophila melanogaster. Genetics. 50: 199–209.
- Service, P. M., and M. R. Rose 1985. Genetic covariation among life-history components: the effect of novel environments. Evolution. 39: 943–945.
- Service, P. M., E. W. Hutchinson, M. D. MacKinley, and M. R. Rose 1985. Resistance to environmental stress in Drosophila melanogaster selected for postponed senescence. Physiol. Zool.. 58: 380–389.
- Sheridan, A. K., and J. S. F. Barker 1974. Two-trait selection and the genetic correlation. II. Changes in the genetic correlation during two-trait selection. Austr. J. Biol. Sci.. 27: 89–101.
- Slatkin, M., and S. A. Frank 1990. The quantitative genetic consequences of pleiotropy under stabilizing and directional selection. Genetics. 125: 207–213.
- Stearns, S. C., G. de Jong, and R. Newman 1991. The effects of phenotypic plasticity on genetic correlations. Trends Ecol. Evol.. 6: 122–126.
- Turelli, M. 1988. Phenotypic evolution, constant covariances and the maintenance of additive genetic variance. Evolution. 42: 1342–1347.
- Via, S. 1984. The quantitative genetics of polyphagy in an insect herbivore. II. Genetic correlations in larval performance within and among host plants. Evolution. 38: 896–905.
- Vieira, C., E. G. Pasyukova, Z. Zeng, B. Hackett, R. F. Lyman, and T. F. C. Mackay 2000. Genotype-environment interaction for quantitative trait loci affecting life span in Drosophila melanogaster. Genetics. 154: 213–227.
- Wilkinson, G. S., K. Fowler, and L. Partridge 1990. Resistance of genetic correlation structure to directional selection in Dro-sophila melanogaster. Evolution. 44: 1990–2003.
- Wright, S. 1968. Evolution and the genetics of populations. Vol. 1. Genetic and biometric foundations. Univ. of Chicago Press, Chicago , IL .