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PLOS ONE  2013 

Phenotypic and Genetic Effects of Contrasting Ethanol Environments on Physiological and Developmental Traits in Drosophila melanogaster

DOI: 10.1371/journal.pone.0058920

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A central problem in evolutionary physiology is to understand the relationship between energy metabolism and fitness-related traits. Most attempts to do so have been based on phenotypic correlations that are not informative for the evolutionary potential of natural populations. Here, we explored the effect of contrasting ethanol environments on physiological and developmental traits, their genetic (co)variances and genetic architecture in Drosophila melanogaster. Phenotypic and genetic parameters were estimated in two populations (San Fernando and Valdivia, Chile), using a half-sib family design where broods were split into ethanol-free and ethanol-supplemented conditions. Our findings show that metabolic rate, body mass and development times were sensitive (i.e., phenotypic plasticity) to ethanol conditions and dependent on population origin. Significant heritabilities were found for all traits, while significant genetic correlations were only found between larval and total development time and between development time and metabolic rate for flies of the San Fernando population developed in ethanol-free conditions. Posterior analyses indicated that the G matrices differed between ethanol conditions for the San Fernando population (mainly explained by differences in genetic (co)variances of developmental traits), whereas the Valdivia population exhibited similar G matrices between ethanol conditions. Our findings suggest that ethanol-free environment increases the energy available to reduce development time. Therefore, our results indicate that environmental ethanol could modify the process of energy allocation, which could have consequences on the evolutionary response of natural populations of D. melanogaster.


[1]  Arnold SJ (1983) Morphology, performance, and fitness. Am Zool 23: 347–361.
[2]  Roff DA (1997) Evolutionary quantitative genetics. New York: Chapman & Hall. 493 p.
[3]  Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sunderland: Sinauer Associates. 980 p.
[4]  Arnold SJ, Burger R, Hohenlohe PA, Ajie BC, Jones AG (2008) Understanding the evolution and stability of the G-matrix. Evolution 62: 2451–2461.
[5]  Lande R (1979) Quantitative genetics analysis of multivariate evolution applied to brain: body size allometry. Evolution 33: 402–416.
[6]  Revell LJ (2007) The G matrix under fluctuating correlational mutation and selection. Evolution 61: 1857–1872.
[7]  Lande R (1976) Natural selection and random genetic drift in phenotypic evolution. Evolution 30: 314–334.
[8]  Hereford J, Hensen TF, Houle D (2004) Comparing strengths of directional selection: how strong is strong? Evolution 58: 2133–2143.
[9]  Hoekstra HE, Hoekstra JM, Berrigan D, Vignieri SM, Hoang A, et al. (2001) Strength and tempo of directional selection in the wild. Proc Natl Acad Sci USA 98: 9157–9160.
[10]  Kingsolver JG, Hoekstra HE, Hoekstra JM, Berrigan D, Vignieri SN, et al. (2001) The strength of phenotypic selection in natural populations. Am Nat 157: 245–261.
[11]  Hoffmann AA, Meril? J (1999) Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol Evol14: 96–101.
[12]  Sgrò CM, Hoffmann AA (2004) Genetic correlations, tradeoffs and environmental variation. Heredity 93: 241–248.
[13]  Bégin M, Roff DA, Debat V (2004) The effect of temperature and wing morphology on quantitative genetic variation in the cricket Gryllus firmus, with an appendix examining the statistical properties of the Jackknife-MANOVA method of matrix comparison. J Evol Biol 17: 1255–1267.
[14]  Doruszuk A, Wojewodzic MW, Gort G, Kammenga JE ( 2008) Rapid divergence of genetic variance-covariance matrix within a natural population. Am Nat 171: 291–304.
[15]  Kraft PG, Wilson RS, Franklin CE, Blows MW (2006) Substantial changes in the genetic basis of tadpoles morphology of Rana lessonae in the presence of predators. J Evol Biol 19: 1813–1818.
[16]  Messina FJ, Fry JD (2003) Environment-dependent reversal of a life history trade-off in the seed beetle Callosobruchus maculates. J Evol Biol 16: 501–509.
[17]  Parsons PA, Stanley SM, Spence GE (1979) Environmental ethanol at low concentrations: longevity and development in the sibling species Drosophila melanogaster and D. simulans. Aust J Zool 27: 747–754.
[18]  Stanley SM, Parsons PA (1981) The response of the cosmopolitan species, Drosophila melanogaster, to ecological gradients. Proc Ecol Soc Australia 11: 121–130.
[19]  Ziolo LK, Parsons PA (19820 Ethanol tolerance, alcohol-dehydrogenase activity and Adh allozymes in Drosophila melanogaster. Genetica 57: 231–237.
[20]  David JR, Mer?ot H, Capy P, McEvey SF, van Herrewege J (1986) Alcohol tolerance and Adh gene frequencies in European and African populations of Drosophila melanogaster. Gen Sel Evol 18: 405–416.
[21]  Fry JD, Donlon K, Saweikis M (2008) A worldwide polymorphism in aldehyde dehydrogenase in Drosophila melanogaster: evidence for selection mediated by dietary ethanol. Evolution 62: 66–75.
[22]  Pecsenye K, Komlési I, Saura A (2004) Heritabilities and additive genetic variance of the activities of some enzymes in Drosophila melanogaster populations living in different habitats. Heredity 93: 215–221.
[23]  Malherbe Y, Kamping A, van Delden W, van De Zande L (2004) ADH enzyme activity and Adh gene expression in Drosophila melanogaster lines differentially selected for increased alcohol tolerance. J Evol Biol 18: 811–819.
[24]  Fry JD (2001) Direct and correlated responses to selection for larval ethanol tolerance in Drosophila melanogaster. J Evol Biol 14: 296–309.
[25]  Cody ML (1966) A general theory of clutch size. Evolution 20: 174–184.
[26]  Stearns SC (1992) The evolution of life histories. Oxford: Oxford University Press. 264 p.
[27]  Roff DA (2001) Life history evolution. Sunderland: Sinauer Associates. 537 p.
[28]  Cotter SC, Kruuk LEB, Wilson W (2004) Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. J Evol Biol 17: 421–429.
[29]  Schwarzenbach GA, Ward PI (2006) Responses to selection on phenoloxidase activity in yellow dung flies. Evolution 60: 1612–1621.
[30]  McKechnie SW, Geer BW (1984) Regulation of alcohol dehydrogenase in Drosophila melanogaster by dietary alcohol and carbohydrate. Insect Biochem 14: 231–242.
[31]  Etges WJ, Klassen CS (1989) Influences of atmospheric ethanol on adult Drosophila mojavensis: altered metabolic rates and increases in fitness among population. Physiol Zool 62: 170–193.
[32]  Hayes JP, Garland T, Dohm MR (1992) Individual variation in metabolism and reproduction of Mus: are energetics and life history linked? Funct Ecol 6: 5–14.
[33]  Nespolo RF, Bustamante DM, Bacigalupe LD, Bozinovic F (2005) Quantitative genetics of bioenergetics and growth-related traits in the wild mammal, Phyllotis darwini. Evolution 59: 1829–1837.
[34]  Artacho P, Nespolo RF (2009) Natural selection reduces energy metabolism in the garden snail, Helix Aspersa (Cornu Aspersum). Evolution 63: 1044–1050.
[35]  Folguera G, Mensch J, Mu?oz JL, Ceballos SG, Hasson E, et al. (2010) Ontogenic stage-dependent effect of temperature on developmental and metabolic rates in a homometabolous insect. J Insect Physiol 56: 1679–1684.
[36]  Miller C (2000) Drosophila melanogaster. Animal Diversity Web. Available: Accessed: 2012 Oct 15.
[37]  Santos M, Fernández-Iriarte P, Céspedes W, Balanyà J, Fontdevilla A, et al. (2004) Swift laboratory thermal evolution of wing shape (but not size) in Drosophila subobscura and its relationship with chromosomal inversion polymorphism. J Evol Biol 17: 841–855.
[38]  Lighton JRB (2008) Measuring metabolic rates. New York: Oxford University Press.
[39]  Statsoft Inc. (2004) STATISTICA. Version 6.1. Tulsa: Statsoft Inc.
[40]  Wilson AJ, Réale D, Clements MN, Morrissey MM, Postma E, et al. (2010) An ecologist's guide to the animal model. J Anim Ecol 79: 13–26.
[41]  Hadfield JD (2010) MCMC methods for multi-response generalized linear models: the MCMCglmm R package. J Stat Softw 33: 2.
[42]  R Development Core Team (2011) R: a language and environment for statistical computing (version 2.13.2). Available: Accessed: 2011 Oct 3.
[43]  Serbezov D, Bernatchez, Olsen EM, V?llestad LA (2010) Quantitative genetic parameters for wild stream-living brown trout: heritability and parental effects. J Evol Biol 23: 1631–1641.
[44]  Roff DA (2002) Comparing G matrices: a MANOVA approach. Evolution 56: 1286–1291.
[45]  Oakeshott JG, Cohan FM, Gibson JB (1985) Ethanol tolerances of Drosophila melanogaster populations selected on different concentrations of ethanol supplemented media. Theor Appl Genet 69: 5–6.
[46]  Roff DA, Mousseau TA (1987) Quantitative genetics and fitness: lessons from Drosophila. Heredity 58: 103–118.
[47]  Rantala MJ, Roff DA (2006) Analysis of the importance of genotypic variation, metabolic rate, morphology, sex and development time on immune function in the cricket, Gryllus firmus. J Evol Biol 19: 834–843.
[48]  Nespolo RF, Casta?eda LE, Roff DA (2007) Quantitative genetic variation of metabolism in the nymphs of the sand cricket, Gryllus firmus, inferred from an analysis of inbred-lines. Biol Res 40: 5–12.
[49]  Blanckenhorn WU, Heyland A (2004) The quantitative genetics of two life history trade-offs in the yellow dung fly in abundant and limited food environments. Evol Ecol 18: 385–402.
[50]  Tejedo M, Reques R (1994) Does larval growth history determines timing of metamorphosis in anurans? A field experiment. Herpetologica 50: 113–118.
[51]  Shafiei M, Moczek AP, Nijhout HF (2001) Food availability controls the onset of metamorphosis in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae). Physiol Entomol 26: 173–180.
[52]  Gebhardt MD, Stearns SC (1988) Phenotypic plasticity for life history traits in Drosophila melanogaster. I. Effects on phenotypic and environmental correlations. J Evol Biol 6: 1–16.
[53]  Kause A, Saloniemi I, Morin JP, Haukioja E, Hanhim?ki S, et al. (2001) Seasonally varying diet quality and the quantitative genetics of development time and body size in birch feeding insects. Evolution 55: 1992–2001.
[54]  Jumbo-Lucioni P, Ayroles JF, Chambers MM, Jordan KW, Leips J, et al. (2010) Systems genetics analysis of body weight and energy metabolisms traits in Drosophila melanogaster. BMC Genomics 11: 297.


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