Eur. J. Entomol. 105 (4): 553-560, 2008 | 10.14411/eje.2008.074

The genetic architecture of extended life span in the seed beetle Acanthoscelides obtectus (Coleoptera: Bruchidae)

Darka ŠEŠLIJA1, Nikola TUCIĆ*,1,2
1 Department of Evolutionary Biology, Institute for Biological Research "Siniša Stankovi c", Blvd Despota Stefana 142, 11060 Belgrade, Serbia; e-mail: ntucic@ibiss.bg.ac.yu
2 Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia

We studied the genetic architecture of the differences in the longevity between lines selected for postponed senescence and a control population of the seed beetle Acanthoscelides obtectus maintained on two hosts. By using lines with increased longevity, which were obtained by selection on natural variation in longevity, we showed that the genetic architecture of seed beetle longevity is complex, with sex-specific effects and variation attributable to many interacting genes, whose expression depend on the host on which the beetles were reared. The nonadditive genetic effects were more strongly expressed when reared on chickpeas, a novel host, than on beans. Outbreeding depression, with respect to longevity, was a consequence of both the intrinsic effect of interactions between genes from different parental sources (disruption of coadapted gene complexes) and the genotype × host interaction (loss of local adaptation).

Keywords: Bruchidae, Acanthoscelides obtectus, ageing, genetic architecture, epistasis, longevity

Received: April 18, 2008; Accepted: June 28, 2008; Published: October 24, 2008

Download citation

References

  1. ALLISON P.D. 1995: Survival Analysis using the SAS System: A Practical Guide, SAS. Institute Inc, Cary, NC
  2. ARMBRUSTER P., BRADSHAW W.E. & HOLZAPFEL C.M. 1997: Evolution of the genetic architecture underlying fitness in the pitcher-plant mosquito, Wyeomyia smithii. Evolution 51: 451-458 Go to original source...
  3. BALDAL E.A., BAKTAWAR W., BRAKEFIELD P.M. & ZWAAN B.J. 2006: Methuselah life history in a variety of conditions, implications for the use of mutatants in longevity research. Exp. Gerontol. 41: 1126-1135 Go to original source...
  4. BIERI J. & KAWECKI T.J. 2003: Genetic architecture of differences between populations of cowpea weevil (Callosobruchus maculatus) evolved in the same environment. Evolution 57: 274-287 Go to original source...
  5. BISBY F.A., BUCKINGHAM J. & HARBORNE J.B. 1994: Phytochemical Dictionary of the Leguminosae. Chapman & Hall, London, vii + 1051 pp
  6. BLOWS M.W. & HOFFMANN A.A. 1996: Evidence for an association between nonadditive genetic variation and extreme expression of a trait. Am. Nat. 148: 576-587 Go to original source...
  7. BLOWS M.W. & SOKOLOWSKI M.B. 1995: The expression of additive and nonadditive genetic variation under stress. Genetics 140: 1149-1159
  8. BRADSHAW W.E. & HOLZAPFEL C.M. 2000: The evolution of genetic architectures and the divergence of natural populations. In Wolf J.B., Brodie E.D. & Wade M.J. (eds): Epistasis and the Evolutionary Process. Oxford University Press, New York, pp. 245-263
  9. CARLBORG O., JACOBSON L., AHGREN P., SIEGEL P. & ANDERSON L. 2006: Epistasis and the release of genetic variation during long-term selection. Nature Genet. 38: 418-420 Go to original source...
  10. CARROLL S.P., DINGLE H., FAMULA T.R. & FOX C.W. 2001: Genetic architecture of adaptive differentiation in evolving host races of the soapberry bug, Jadera haematoloma. Genetica 112: 257-272 Go to original source...
  11. CARROLL S.P., DINGLE H.G. & FAMULA T.R. 2003: Rapid appearance of epistasis during adaptive divergence following colonization. Proc. R. Soc. Lond. (B) 270: S80-S83 Go to original source...
  12. CHARLESWORTH B. 1994: Evolution in Age-structured Populations. Cambridge University Press, London, xiii + 306 pp
  13. COCKERHAM C.C. 1980: Random and fixed effects in plant genetics. Theor. Appl. Genet. 56: 119-131 Go to original source...
  14. CURRAN S.P. & RUVKUN G. 2007: Lifespan regulation by evolutionarily conserved genes essential for viability. PloS Genet. 3: e56, doi: 10.1371/journal.pgen.0030056 Go to original source...
  15. DEMUTH J.P. & WADE M.J. 2007: Population differentiation in the beetle Tribolium castaneum. I. Genetic architecture. Evolution 61: 494-509 Go to original source...
  16. EITAN Y. & SOLLER M. 2004: Selection induced variation - A new model to explain direct and indirect effects of sixty years of commercial selection for juvenile growth rate in broiler chickens, with implications for episodes of rapid evolutionary change. In Wasser S.P. (ed.): Evolutionary Theory and Processes: Modern Horizens Papers in Honour of Eviatar Nevo. Kluwer Academic Publ., Dordrecht, pp. 153-176
  17. FENSTER C.B. & GALLOWAY L.F. 2000: The contribution of epistasis to the evolution of natural populations: a case study of an annual plants. In Wolf J.B., Brodie E.D. & Wade M.J. (eds): Epistasis and the Evolutionary Process. Oxford University Press, New York, pp. 232-244
  18. FENSTER C.B., GALLOWAY L.F. & CHAO L. 1997: Epistasis and its consequences for the evolution of natural populations. Trends Ecol. Evol. 12: 282-286 Go to original source...
  19. FINCH C.E. & TANZI R.E. 1997: Genetics of aging. Science 278: 407-411 Go to original source...
  20. FOX C.W., CZESAK M.E. & WALLIN W.G. 2004: Complex genetic architecture of population differences in adult lifespan of a beetle: nonadditive inheritance, gender differences, body size and a large maternal effect. J. Evol. Biol. 17: 1007-1017 Go to original source...
  21. GEIGER-THORNSBERRY G.L. & MACKAY T.F.C. 2004: Quantitative trait loci affecting natural variation in Drosophila longevity. Mech. Ageing Dev. 125: 179-189 Go to original source...
  22. GILCHRIST A.S. & PARTRIDGE L.A. 1999: Comparison of the genetic basis of wing size divergence in three parallel body size clines of Drosophila melanogaster. Genetics 153: 1775-1787
  23. GLIKSMAN I. & TUCIC N. 1991: Effects of selection for early and late reproduction in low and high larval density populations of the bean weevil (Acanthoscelides obtectus). Genet. Sel. Evol. 23: 119-132 Go to original source...
  24. HAMILTON W.D. 1966: The moulding of senescence by natural selection. J. Theor. Biol. 12: 12-45 Go to original source...
  25. HARSHMAN L.G. 2002: Life span extension of Drosophila melanogaster: genetic and population studies. Pop. Dev. Rev. 29: S99-S126
  26. LEIPS J. & MACKAY T.F.C. 2000: Quantitative trait loci for life span in Drosophila melanogaster: Interactions with genetic background and larval density. Genetics 155: 1773-1788
  27. LEIPS J. & MACKAY T.F.C. 2002: The complex genetic architecture of Drosophila life span. Exp. Aging Res. 28: 361-390 Go to original source...
  28. LYNCH M. & WALSH B. 1998: Genetics and Analysis of Quantitative Traits. Sinauer Associates, Sunderland, 980 pp
  29. MACKAY T.F.C. 2001: The genetic architecture of quantitative traits. Annu. Rev. Genet. 35: 303-339 Go to original source...
  30. MATHER K. 1967: Complementary and duplicate gene interaction in biometrical genetics. Heredity 22: 97-103 Go to original source...
  31. MATHER K. & JINKS J.L. 1982: Biometrical Genetics: The Study of Continuous Variation. Chapman & Hall, London, 396 pp
  32. MEDAWAR P.B. 1952: An Unsolved Problem in Biology. H.K. Lewis, London
  33. 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 Go to original source...
  34. REYNOLDS R.M., TEMIYASATHIT S., REEDY M.M., RUEDI E.A., DRNEVICH J.M., LEIPS J. & HUGHES 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 Go to original source...
  35. ROSE M.R. 1984: Laboratory evolution of postponed senescence in Drosophila melanogaster. Evolution 38: 1004-1010 Go to original source...
  36. SPENCER C.C., HOWELL C.E., WRIGHT A.R. & PROMISLOW D.E. 2003: Testing an "aging gene" in long-lived Drosophila strains: Increased longevity depends on sex and genetic background. Aging Cell 2: 123-130 Go to original source...
  37. 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 Go to original source...
  38. TOIVONEN J.M., WALKER G.A., MARTINEZ-DIAZ P., BJEDOV I., DRIEGE Y., JACOBS H.T., GEMS D. & PARTRIDGE L. 2007: No influence of Indy on lifespan in Drosophila after correction for genetic and cytoplasmic background effects. PloS Genet. 3: e95, doi: 10.1371/journal.pgen.0030095 Go to original source...
  39. TUCIC N., STOJKOVIC O., GLIKSMAN I., MILANOVIC D. & SESLIJA D. 1997: Laboratory evolution of life-history traits in the bean weevil (Acanthoscelides obtectus): the effects of densitydependent and age-specific selection. Evolution 51: 1896-1909 Go to original source...
  40. VERMEULEN C.J. & BIJLSMA R. 2006: Changes in genetic archtecture during relaxation in Drosophila melanogaster selected on divergent virgin life span. J. Evol. Biol. 19: 216-227 Go to original source...
  41. VIEIRA C., PASYUKOVA E.G., ZENG Z.B., HACKETT J.B., LYMAN R.F. & MACKAY T.F.C. 2000: Genotype-environment interaction for quantitative trait loci affecting life span in Drosophila melanogaster. Genetics 154: 213-227
  42. WILLIAMS G.C. 1957: Pleiotropy, natural selection, and the evolution of senescence. Evolution 11: 398-411 Go to original source...
  43. WILSON R.H., MORGAN T.J. & MACKAY T.F.C. 2006: Highresolution mapping of quantitative trait loci affect life span in Drosophila melanogaster. Genetics 173: 1455-1463 Go to original source...
  44. ZWAAN B., BIJLSMA R. & HOEKSTRA R.F. 1995: Direct selection on life-span in Drosophila melanogaster. Evolution 49: 649-659 Go to original source...