Eur. J. Entomol. 105 (4): 553-560, 2008
The genetic architecture of extended life span in the seed beetle Acanthoscelides obtectus (Coleoptera: Bruchidae)
- 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; Revised: June 28, 2008; Accepted: June 28, 2008; Published: October 24, 2008 Show citation
References
- ALLISON P.D. 1995: Survival Analysis using the SAS System: A Practical Guide, SAS. Institute Inc, Cary, NC
- 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... - 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... - 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... - BISBY F.A., BUCKINGHAM J. & HARBORNE J.B. 1994: Phytochemical Dictionary of the Leguminosae. Chapman & Hall, London, vii + 1051 pp
- 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... - BLOWS M.W. & SOKOLOWSKI M.B. 1995: The expression of additive and nonadditive genetic variation under stress. Genetics 140: 1149-1159
Go to original source... - 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
- 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... - 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... - 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... - CHARLESWORTH B. 1994: Evolution in Age-structured Populations. Cambridge University Press, London, xiii + 306 pp
Go to original source... - COCKERHAM C.C. 1980: Random and fixed effects in plant genetics. Theor. Appl. Genet. 56: 119-131
Go to original source... - 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... - 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... - 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
Go to original source... - 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
- 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... - FINCH C.E. & TANZI R.E. 1997: Genetics of aging. Science 278: 407-411
Go to original source... - 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... - 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... - 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
Go to original source... - 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... - HAMILTON W.D. 1966: The moulding of senescence by natural selection. J. Theor. Biol. 12: 12-45
Go to original source... - HARSHMAN L.G. 2002: Life span extension of Drosophila melanogaster: genetic and population studies. Pop. Dev. Rev. 29: S99-S126
- 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
Go to original source... - 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... - LYNCH M. & WALSH B. 1998: Genetics and Analysis of Quantitative Traits. Sinauer Associates, Sunderland, 980 pp
- MACKAY T.F.C. 2001: The genetic architecture of quantitative traits. Annu. Rev. Genet. 35: 303-339
Go to original source... - MATHER K. 1967: Complementary and duplicate gene interaction in biometrical genetics. Heredity 22: 97-103
Go to original source... - MATHER K. & JINKS J.L. 1982: Biometrical Genetics: The Study of Continuous Variation. Chapman & Hall, London, 396 pp
Go to original source... - MEDAWAR P.B. 1952: An Unsolved Problem in Biology. H.K. Lewis, London
- 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... - 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... - ROSE M.R. 1984: Laboratory evolution of postponed senescence in Drosophila melanogaster. Evolution 38: 1004-1010
Go to original source... - 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... - 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... - 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... - 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... - 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... - 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
Go to original source... - WILLIAMS G.C. 1957: Pleiotropy, natural selection, and the evolution of senescence. Evolution 11: 398-411
Go to original source... - 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... - ZWAAN B., BIJLSMA R. & HOEKSTRA R.F. 1995: Direct selection on life-span in Drosophila melanogaster. Evolution 49: 649-659
Go to original source...
This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.




