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Associations between environmental stress, selection history, and quantitative genetic variation in Drosophila melanogaster

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Abstract

Stressful environments may increase quantitative genetic variation in populations by promoting the expression of genetic variation that has not previously been eliminated or canalized by natural selection. This “selection history” hypothesis predicts that novel stressors will increase quantitative genetic variation, and that the magnitude of this effect will decrease following continued stress exposure. We tested these predictions using Drosophila melanogaster and sternopleural bristle number as a model system. In particular, we examined the effect of high temperature stress (31°C) on quantitative genetic variation before and after our study population had been reared at 31°C for 15 generations. High temperature stress was found to increase both additive genetic variance and heritability, but contrary to the selection history hypothesis prediction, the magnitude of this effect significantly increased after the study population had been reared for 15 generations under high temperature stress. These results demonstrate that high temperature stress increases quantitative genetic variation for bristle number, but do not support the selection history hypothesis as an explanation for this effect.

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References

  • M.I. Antipin A.G. Imasheva (2001) ArticleTitleGenetic variability and fluctuating asymmetry of morphological traits in Drosophila melanogaster reared on a pesticide-containing medium Russ. J. Genet. 3 247–252 Occurrence Handle10.1023/A:1009000925144

    Article  Google Scholar 

  • M. Ashburner (1989) Drosophila: A Laboratory Handbook Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY

    Google Scholar 

  • J. Aspi A. Hoikkala (1993) ArticleTitleLaboratory and natural heritabilities of male courtship song characters in Drosophila montana and D. littoralis Heredity 70 400–406 Occurrence Handle8496069

    PubMed  Google Scholar 

  • C.C. Bennington J.B. McGraw (1996) ArticleTitleEnvironment-dependence of quantitative genetic parameters in Impatiens pallida Evolution 50 1083–1097 Occurrence Handle10.2307/2410649

    Article  Google Scholar 

  • A. Blum (1988) Plant Breeding for Stress Environments CRC Press Boca Raton, FL

    Google Scholar 

  • Z. Bochdanovits G. Jong ParticleDe (2003) ArticleTitleTemperature dependent larval resource allocation shaping adult body size in Drosophila melanogaster J. Evol. Biol. 16 1159–1167 Occurrence Handle14640407 Occurrence Handle1:STN:280:DC%2BD3srlvF2nsw%3D%3D Occurrence Handle10.1046/j.1420-9101.2003.00621.x

    Article  PubMed  CAS  Google Scholar 

  • O.A. Bubliy V. Loeschcke (2000) ArticleTitleHigh stressful temperature and genetic variation of five quantitative traits in Drosophila melanogaster Genetica 110 79–85 Occurrence Handle11519878 Occurrence Handle1:STN:280:DC%2BD3Mvns1Kksg%3D%3D Occurrence Handle10.1023/A:1017990814142

    Article  PubMed  CAS  Google Scholar 

  • O.A. Bubliy V. Loeschcke (2002) ArticleTitleEffect of low stressful temperature on genetic variation of five quantitative traits in Drosophila melanogaster Heredity 89 70–75 Occurrence Handle12080372 Occurrence Handle1:CAS:528:DC%2BD38XkslKnurk%3D Occurrence Handle10.1038/sj.hdy.6800104

    Article  PubMed  CAS  Google Scholar 

  • O.A. Bubliy V. Loeschcke (2005) ArticleTitleCorrelated responses to selection for stress resistance and longevity in a laboratory population of Drosophila melanogaster J. Evol. Biol. 18 789–803 Occurrence Handle16033550 Occurrence Handle1:STN:280:DC%2BD2Mzns1Onsw%3D%3D Occurrence Handle10.1111/j.1420-9101.2005.00928.x

    Article  PubMed  CAS  Google Scholar 

  • O.A. Bubliy V. Loeschcke A.G. Imasheva (2000) ArticleTitleEffect of stressful and nonstressful growth temperatures on variation of sternopleural bristle number in Drosophila melanogaster Evolution 54 1444–1449 Occurrence Handle11005311 Occurrence Handle1:STN:280:DC%2BD3cvltVehtQ%3D%3D Occurrence Handle10.1554/0014-3820(2000)054[1444:EOSANG]2.0.CO;2

    Article  PubMed  CAS  Google Scholar 

  • R. Bürger R. Lande (1994) ArticleTitleOn the distribution of the mean and variance of a quantitative trait under mutation-selection-drift balance Genetics 138 901–912 Occurrence Handle7851784

    PubMed  Google Scholar 

  • R. Bürger M. Lynch (1995) ArticleTitleEvolution and extinction in a changing environment – a quantitative-genetic analysis Evolution 49 151–163 Occurrence Handle10.2307/2410301

    Article  Google Scholar 

  • J.K. Conner R. Franks C. Stewart (2003) ArticleTitleExpression of additive genetic variances and covariances for wild radish floral traits: comparison between field and greenhouse environments Evolution 57 487–495 Occurrence Handle12703938 Occurrence Handle10.1554/0014-3820(2003)057[0487:EOAGVA]2.0.CO;2

    Article  PubMed  Google Scholar 

  • J.R. David B. Moreteau J.R. Gautier A. Stockel A.G. Imasheva (1994) ArticleTitleReaction norms of size characters in relation to growth temperature in Drosophila melanogaster: an isofemale line analysis Genet. Sel. Evol. 26 229–251

    Google Scholar 

  • V. Debat P. Alibert P. David E. Paradis J. Auffray (2000) ArticleTitleIndependence between developmental stability and canalization in the skull of the house mouse Proc. R. Soc. Lond. B Biol. Sci. 267 423–430 Occurrence Handle1:STN:280:DC%2BD3c7pvFKmug%3D%3D Occurrence Handle10.1098/rspb.2000.1017

    Article  CAS  Google Scholar 

  • J.A. Endler (1986) Natural Selection in the Wild Princeton University Press Princeton

    Google Scholar 

  • D.S. Falconer T.F.C. Mackay (1996) Introduction to Quantitative Genetics 4Longman Harlow UK

    Google Scholar 

  • R.A. Fisher (1930) The Genetical Theory of Natural Selection Clarendon Press Oxford

    Google Scholar 

  • I.R. Franklin R. Frankham (1998) ArticleTitleHow large must populations be to retain evolutionary potential? Anim. Conserv. 1 69–71 Occurrence Handle10.1111/j.1469-1795.1998.tb00228.x

    Article  Google Scholar 

  • A. Garcia-Dorado J.A. Gonzalez (1996) ArticleTitleStabilizing selection detected for bristle number in Drosophila melanogaster Evolution 50 1573–1578 Occurrence Handle10.2307/2410893

    Article  Google Scholar 

  • J. Guntrip R.M. Sibly G.J. Holloway (1997) ArticleTitleThe effect of novel environment and sex on the additive genetic variation and covariation in and between emergence body weight and development period in the cowpea weevil, Callosobruchus maculates (Coleoptera, Bruchidae) Heredity 78 158–165 Occurrence Handle10.1038/sj.hdy.6881430

    Article  Google Scholar 

  • W.G. Hill (2000) ArticleTitleMaintenance of quantitative genetic variation in animal breeding programmes Livest. Prod. Sci. 63 99–109 Occurrence Handle10.1016/S0301-6226(99)00115-3

    Article  Google Scholar 

  • A.A. Hoffmann & P.A. Parsons. 1991. Evolutionary Genetics and Environmental Stress Oxford University Press

  • A.A. Hoffmann P.A. Parsons (1997) Extreme Environmental Change and Evolution Cambridge Univ Press Cambridge, U.K

    Google Scholar 

  • A.A. Hoffmann M. Schiffer (1998) ArticleTitleChanges in the heritability of five morphological traits under combined environmental stresses in Drosophila melanogaster Evolution 54 1207–1212 Occurrence Handle10.2307/2411250

    Article  Google Scholar 

  • A.A. Hoffmann J. Merilä (1999) ArticleTitleHeritable variation and evolution under favorable and unfavorable conditions Trends Ecol. Evol. 14 96–101 Occurrence Handle10322508 Occurrence Handle10.1016/S0169-5347(99)01595-5

    Article  PubMed  Google Scholar 

  • G.J. Holloway S.R. Povey R.M. Sibly (1990) ArticleTitleThe effect of new environment on adapted genetic architecture Heredity 64 323–330

    Google Scholar 

  • R.D. Holt M.S. Gaines (1992) ArticleTitleAnalysis of adaptation in heterogeneous landscapes: implications for the evolution of fundamental niches Evol. Ecol. 6 433–447 Occurrence Handle10.1007/BF02270702

    Article  Google Scholar 

  • D. Houle (1992) ArticleTitleComparing evolvability and variability of quantitative traits Genetics 130 195–204 Occurrence Handle1732160 Occurrence Handle1:STN:280:DyaK387itVGitQ%3D%3D

    PubMed  CAS  Google Scholar 

  • A.G. Imasheva V. Loeschcke L.A. Zhivotovsky O.E. Lazebny (1997) ArticleTitleEffects of extreme temperatures on phenotypic variation and developmental stability in Drosophila melanogaster and D. Buzzattii Biol. J. Linn. Soc. 61 117–126 Occurrence Handle10.1006/bijl.1996.0125

    Article  Google Scholar 

  • A.G. Imasheva V. Loeschcke L.A. Zhivotovsky O.E. Lazebny (1998) ArticleTitleStress temperatures and quantitative variation in Drosophila melanogaster Heredity 81 246–253 Occurrence Handle9800368 Occurrence Handle10.1046/j.1365-2540.1998.00384.x

    Article  PubMed  Google Scholar 

  • T.J. Kawecki (1995) ArticleTitleExpression of genetic and environmental variation for life history characters on the usual and novel hosts in Callosobruchus maculatus (Coleoptera: Bruchidae) Heredity 75 70–76

    Google Scholar 

  • H. Kräublich (2000) ArticleTitleExploitable genetic variation can be changed under environmental and genetic stress. Consequences for livestock breeding – a review J. Anim. Breed. Genet. 117 275–280 Occurrence Handle10.1046/j.1439-0388.2000.00254.x

    Article  Google Scholar 

  • R. Lande (1995) Breeding plans for small populations based on the dynamics of quantitative genetic variance J.D. Ballou M. Gilpin T.J. Foose (Eds) in Population Management for Survival and Recovery: Analytical Methods and Strategies in Small Population Conservation Columbia University Press New York 318–340

    Google Scholar 

  • R. Lande G.F. Barrowclough (1987) Effective population size, genetic variation, and their use in population management M. E. Soulé (Eds) in Viable Populations for Conservation Cambridge University Press Cambridge, UK 87–123

    Google Scholar 

  • R. Linney B.W. Barnes M.J. Kearsey (1971) ArticleTitleVariation for metrical characters in Drosophila populations. III. The nature of selection Heredity 27 163–174 Occurrence Handle5290164 Occurrence Handle1:STN:280:DyaE387gtVKrsg%3D%3D

    PubMed  CAS  Google Scholar 

  • V. Loeschcke J. Bundgaard J.S.F. Barker (1999) ArticleTitleReaction norms across and genetic parameters at different temperatures for thorax and wing size traits in Drosophila aldrichi and D. buzzatii J. Evol. Biol. 12 605–623 Occurrence Handle10.1046/j.1420-9101.1999.00060.x

    Article  Google Scholar 

  • C. Lopez-Fanjul J. Guerra A. Garcia (1989) ArticleTitleChanges in the distribution of the genetic variance of a quantitative trait in small populations of Drosophila melanogaster Genet. Sel. Evol. 21 159–168

    Google Scholar 

  • M. Lynch W.G. Hill (1986) ArticleTitlePhenotypic evolution by neutral mutation Evolution 40 915–935 Occurrence Handle10.2307/2408753

    Article  Google Scholar 

  • K. Mather (1943) ArticleTitlePolygenic inheritance and natural selection Biol. Rev. 18 32–64

    Google Scholar 

  • J.A. McKenzie G.M. Game (1987) ArticleTitleDiazinon resistance in Lucilia cuprina: mapping of a fitness modifier Heredity 59 371–381

    Google Scholar 

  • B. Moreteau P. Gibert J. Delpuech G. Petavy J.R. David (2003) ArticleTitlePhenotypic plasticity of sternopleural bristle number in temperate and tropical populations of Drosophila melanogaster Genet. Res. 81 25–32 Occurrence Handle12693680 Occurrence Handle10.1017/S0016672302005967

    Article  PubMed  Google Scholar 

  • J. Merilä (1997) ArticleTitleExpression of genetic variation in body size of the collard flycatcher under different environmental conditions Evolution 51 526–536 Occurrence Handle10.2307/2411125

    Article  Google Scholar 

  • S.V. Nuzhidin J.D. Fry T.F.C. Mackay (1995) ArticleTitlePolygenic mutation in Drosophila melanogaster – the causal relationship of bristle number to fitness Genetics 139 861–872

    Google Scholar 

  • A.R. Palmer (1994) Fluctuating asymmetry analyses: a primer T. A. Markow (Eds) Developmental instability: its origins and evolutionary implications Kluwer Academic Publications Netherlands 355–364

    Google Scholar 

  • A. Perez C. Garcia (2002) ArticleTitleEvolutionary responses of Drosophila melanogaster to selection at different larval densities: changes in genetic variation, specialization, and phenotypic plasticity J. Evol. Biol. 15 524–536 Occurrence Handle10.1046/j.1420-9101.2002.00427.x

    Article  Google Scholar 

  • C. Pál (1998) ArticleTitlePlasticity, memory and the adaptive landscape of the genotype Proc. R. Soc. London Ser. B 265 1319–1323 Occurrence Handle10.1098/rspb.1998.0436

    Article  Google Scholar 

  • M. Pigliucci C.D. Schlichting J. Whitton (1995) ArticleTitleReaction norms of Arabadopsis. 2. Response to stress and unordered environmental variation Funct. Ecol. 9 537–547 Occurrence Handle10.2307/2390020

    Article  Google Scholar 

  • M. Polak (2003) Developmental Instability: Causes and Consequences Oxford University Press New York

    Google Scholar 

  • A. Robertson (1955) ArticleTitleSelection in animals: synthesis Cold Spring Harbor Symp. Quant. Biol. 20 225–229 Occurrence Handle13433565 Occurrence Handle1:STN:280:DyaG2s%2FotVaisQ%3D%3D

    PubMed  CAS  Google Scholar 

  • C.M. Sgro A.A. Hoffmann (1998) ArticleTitleHeritable variation for fecundity in field-collected Drosophila and their offspring reared under different environmental temperatures Evolution 52 134–143 Occurrence Handle10.2307/2410928

    Article  Google Scholar 

  • R.R. Sokal F.J. Rohlf (1995) Biometry W. H. Freeman New York

    Google Scholar 

  • M.E. Soulé (1987) Introduction M.E. Soulé (Eds) Viable Populations for Conservation Cambridge University Press Cambridge, UK 1–10

    Google Scholar 

  • A.O. Tantawy G.S. Mallah (1961) ArticleTitleStudies on natural populations of Drosophila. I. Heat resistance and geographical variation in Drosophila melanogaster and Drosophila simulans Evolution 15 1–14 Occurrence Handle10.2307/2405839

    Article  Google Scholar 

  • J.M. Thoday (1958) ArticleTitleHomeostasis in a selection experiment Heredity 12 401–415

    Google Scholar 

  • C.H. Waddington (1960) ArticleTitleExperiments on canalizing selection Genet. Res. 1 140–150 Occurrence Handle10.1017/S0016672300000136

    Article  Google Scholar 

  • I. Weigensberg D.A. Roff (1996) ArticleTitleNatural heritabilities: can they be reliably estimated in the laboratory? Evolution 50 2149–2157 Occurrence Handle10.2307/2410686

    Article  Google Scholar 

  • R.E. Woods C.M. Sgro M.J. Hercus A.A. Hoffmann (1999) ArticleTitleThe association between fluctuating asymmetry, trait variability, trait heritability, and stress: a multiply replicated experiment on combined stresses in Drosophila melanogaster Evolution 53 493–505 Occurrence Handle10.2307/2640785

    Article  Google Scholar 

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  1. Department of Biological Sciences, Bowling Green State University, Bowling Green, OH, 43403-0212, USA

    William R. Swindell & Juan L. Bouzat

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  1. William R. Swindell
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  2. Juan L. Bouzat
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Correspondence to William R. Swindell.

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Swindell, W.R., Bouzat, J.L. Associations between environmental stress, selection history, and quantitative genetic variation in Drosophila melanogaster . Genetica 127, 311–320 (2006). https://doi.org/10.1007/s10709-005-5240-8

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