Genetic basis of fitness differences in natural populations

Genetic basis of fitness differences in natural populations


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ABSTRACT Genomics profoundly influences current biology. One of many exciting consequences of this revolution is the potential for identifying and studying the genetic basis of those traits


affecting fitness that are key to natural selection. Recent studies using a multitude of genomic approaches have established such genotype–phenotype relationships in natural populations,


giving new insight into the genetic architecture of quantitative variation. In parallel, an emerging understanding of the quantitative genetics of fitness variation in the wild means that we


are poised to see a synthesis of ecological and molecular approaches in evolutionary biology. Access through your institution Buy or subscribe This is a preview of subscription content,


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EVOLUTIONARY TRAJECTORIES Article 07 September 2020 REFERENCES * Mitchell-Olds, T. & Schmitt, J. Genetic mechanisms and evolutionary significance of natural variation in _Arabidopsis_.


_Nature_ 441, 947–952 (2006) Article  CAS  ADS  Google Scholar  * Rice, W. R. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. _Nature_ 381,


232–234 (1996) Article  CAS  ADS  Google Scholar  * Chippindale, A. K., Gibson, J. R. & Rice, W. R. Negative genetic correlation for adult fitness between sexes reveals ontogenetic


conflict in _Drosophila_. _Proc. Natl Acad. Sci. USA_ 98, 1671–1675 (2001) Article  CAS  ADS  Google Scholar  * Fedorka, K. M. & Mousseau, T. A. Female mating bias results in conflicting


sex-specific offspring fitness. _Nature_ 429, 65–67 (2004) Article  CAS  ADS  Google Scholar  * Foerster, K. et al. Sexually antagonistic genetic variation for fitness in red deer. _Nature_


447, 1107–1110 (2007) Article  CAS  ADS  Google Scholar  * Wilson, A. J. et al. Environmental coupling of selection and heritability limits evolution. _PLoS Biol._ 4, e216 (2006) Article 


CAS  Google Scholar  * Kruuk, L. E. B. et al. Antler size in red deer: heritability and selection but no evolution. _Evol. Int. J. Org. Evol._ 56, 1683–1695 (2002) Article  CAS  Google


Scholar  * Grant, P. R. & Grant, B. R. Unpredictable evolution in a 30-year study of Darwin's finches. _Science_ 296, 707–711 (2002) Article  CAS  ADS  Google Scholar  * Garant, D.,


Kruuk, L. E. B., McCleery, R. H. & Sheldon, B. C. Evolution in a changing environment: a case study with great tit fledging mass. _Am. Nat._ 164, 115–129 (2004) Article  Google Scholar


  * Knapczyk, F. N. & Conner, J. K. Estimates of the average strength of selection are not inflated by sampling error or publication bias. _Am. Nat._ 170, 501–508 (2007) Article  Google


Scholar  * Kruuk, L. E. B. Estimating genetic parameters in natural populations using the “animal model”. _Phil. Trans. R. Soc. Lond. B_ 359, 873–890 (2004) Article  Google Scholar  * Kruuk,


L. E. B. et al. Heritability of fitness in a wild mammal population. _Proc. Natl Acad. Sci. USA_ 97, 698–703 (2000) Article  CAS  ADS  Google Scholar  * Pelletier, F., Clutton-Brock, T. H.,


Pemberton, J. M., Tuljapurkar, S. & Coulson, T. The evolutionary demography of ecological change: linking trait variation and population growth. _Science_ 315, 1571–1574 (2007) Article


  CAS  ADS  Google Scholar  * Charmantier, A., Perrins, C., McCleery, R. H. & Sheldon, B. C. Quantitative genetics of age at reproduction in wild swans: support for antagonistic


pleiotropy models of senescence. _Proc. Natl Acad. Sci. USA_ 103, 6587–6592 (2006) Article  CAS  ADS  Google Scholar  * Conover, D. O. & Schultz, E. T. Phenotypic similarity and the


evolutionary significance of counter-gradient variation. _Trends Ecol. Evol._ 10, 248–252 (1995) Article  CAS  Google Scholar  * Laugen, A. T. et al. Latitudinal countergradient variation in


the common frog (_Rana temporaria_) development rates—evidence for local adaptation. _J. Evol. Biol._ 16, 996–1005 (2003) Article  CAS  Google Scholar  * Merila, J., Kruuk, L. E. B. &


Sheldon, B. C. Cryptic evolution in a wild bird population. _Nature_ 412, 76–79 (2001) Article  CAS  ADS  Google Scholar  * Garant, D., Kruuk, L. E. B., Wilkin, T. A., McCleery, R. H. &


Sheldon, B. C. Evolution driven by differential dispersal within a wild bird population. _Nature_ 433, 60–65 (2005) Article  CAS  ADS  Google Scholar  * Wilson, A. J. et al. Quantitative


genetics of growth and cryptic evolution of body size in an island population. _Evol. Ecol._ 21, 337–356 (2007) Article  Google Scholar  * Hoekstra, H. E. & Coyne, J. A. The locus of


evolution: evo devo and the genetics of adaptation. _Evol. Int. J. Org. Evol._ 61, 995–1016 (2007) Article  Google Scholar  * King, M. C. & Wilson, A. C. Evolution at two levels in


humans and chimpanzees. _Science_ 188, 107–116 (1975) Article  CAS  ADS  Google Scholar  * Carroll, S. B. _Endless Forms Most Beautiful: the New Science of Evo-Devo_ (W. W. Norton & Co.,


New York, 2005) Google Scholar  * Prud'homme, B. et al. Repeated morphological evolution through _cis_-regulatory changes in a pleiotropic gene. _Nature_ 440, 1050–1053 (2006) Article


  CAS  ADS  Google Scholar  * Borneman, A. R. et al. Divergence of transcription factor binding sites across related yeast species. _Science_ 317, 815–819 (2007) Article  CAS  ADS  Google


Scholar  * McGregor, A. P. et al. Morphological evolution through multiple _cis_-regulatory mutations at a single gene. _Nature_ 448, 587–590 (2007) Article  CAS  ADS  Google Scholar  *


ffrench-Constant, R. H., Rocheleau, T. A., Steichen, J. C. & Chalmers, A. E. A point mutation in a _Drosophila_ GABA receptor confers insecticide resistance. _Nature_ 363, 448–451 (1993)


Article  ADS  Google Scholar  * Bustamante, C. D. et al. Natural selection on protein-coding genes in the human genome. _Nature_ 437, 1153–1157 (2005) Article  CAS  ADS  Google Scholar  *


Vera, J. C. et al. Rapid transcriptome characterization for a nonmodel organism using 454 pyrosequencing. _Mol. Ecol._ advance online publication, doi: 10.1111/j.1365-294x.2008.03666.x (5


February 2008) * Mitchell-Olds, T., Willis, J. H. & Goldstein, D. B. Which evolutionary processes influence natural genetic variation for phenotypic traits? _Nature Rev. Genet._ 8,


845–856 (2007) Article  CAS  Google Scholar  * Williams, J. T. & Blangero, J. Power of variance component linkage analysis to detect quantitative trait loci. _Ann. Hum. Genet._ 63,


545–563 (1999) Article  CAS  Google Scholar  * Barton, N. H. & Keightly, P. D. Understanding quantitative genetic variation. _Nature Rev. Genet._ 3, 11–21 (2002) Article  CAS  Google


Scholar  * Lynch, M. & Walsh, B. _Genetics and Analysis of Quantitative Traits_ (Sinauer Associates, Sunderland, Massachusetts, 1998) Google Scholar  * Slate, J. et al. A genome scan for


quantitative trait loci in a wild populations of red deer (_Cervus elaphus_). _Genetics_ 162, 1863–1873 (2002) CAS  PubMed  PubMed Central  Google Scholar  * Beraldi, D. et al. Mapping


quantitative trait loci underlying fitness-related traits in a free-living sheep population. _Evol. Int. J. Org. Evol._ 61, 1403–1416 (2007) Article  Google Scholar  * Colosimo, P. F. et al.


The genetic architecture of parallel armor plate reduction in threespine sticklebacks. _PLoS Biol._ 2, e109 (2004) Article  Google Scholar  * Colosimo, P. F. et al. Widespread parallel


evolution in sticklebacks by repeated fixation of ectodysplasin alleles. _Science_ 307, 1928–1933 (2005) Article  CAS  ADS  Google Scholar  * Backström, N., Qvarnstrom, A., Gustafsson, L.


& Ellegren, H. Levels of linkage disequilibrium in a wild bird population. _Biol. Lett._ 2, 435–438 (2006) Article  Google Scholar  * Slate, J. & Pemberton, J. M. Admixture and


patterns of linkage disequilibrium in a free-living vertebrate population. _J. Evol. Biol._ 20, 1415–1427 (2007) Article  CAS  Google Scholar  * Yu, J. et al. A unified mixed-model method


for association mapping that accounts for multiple levels of relatedness. _Nature Genet._ 38, 203–208 (2006) Article  CAS  Google Scholar  * Williamson, S. et al. Localizing recent adaptive


evolution in the human genome. _PloS Genet._ 3, e90 (2007) Article  Google Scholar  * Pennings, P. S. & Hermisson, J. Soft sweeps. III: The signature of positive selection from recurrent


mutation. _PloS Genet._ 2, e186 (2006) Article  Google Scholar  * Teshima, K. M., Coop, G. & Preworski, M. How reliable are empirical genomic scans for selective sweeps? _Genome Res._


16, 702–712 (2006) Article  CAS  Google Scholar  * Beaumont, M. A. Adaptation and speciation: what can _F_ _ST_ tell us? _Trends Ecol. Evol._ 20, 435–440 (2005) Article  Google Scholar  *


Storz, J. F. Using genome scans of DNA polymorphism to infer adaptive population divergence. _Mol. Ecol._ 14, 671–688 (2005) Article  CAS  Google Scholar  * Luikart, G., England, P. R.,


Tallman, D., Jordan, S. & Taberlet, P. The power and promise of population genomics: from genotyping to genome typing. _Nature Rev. Genet._ 4, 981–993 (2003) Article  CAS  Google Scholar


  * Campbell, D. & Bernatchez, L. Generic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. _Mol. Biol.


Evol._ 21, 945–956 (2004) Article  CAS  Google Scholar  * Bonin, A. Explorative genome scan to detect candidate loci for adaptation along a gradient of altitude in the common frog (_Rana


temporaria_). _Mol. Ecol._ 23, 773–783 (2006) CAS  Google Scholar  * Rogers, S. M. & Bernatchez, L. Integrating QTL mapping and genome scans towards the characterization of candidate


loci under parallel selection in the lake whitefish (_Coregonus clupeaformis_). _Mol. Ecol._ 14, 351–361 (2005) Article  CAS  Google Scholar  * Lin, J. Y. & Fisher, D. E. Melanocyte


biology and skin pigmentation. _Nature_ 445, 843–850 (2007) Article  CAS  ADS  Google Scholar  * Hoekstra, H. E., Hirschmann, R. J., Bundey, R. A., Insel, P. A. & Crossland, J. P. A


single amino acid mutation contributes to adaptive beach mouse color pattern. _Science_ 313, 101–104 (2006) Article  CAS  ADS  Google Scholar  * Rosenblum, E. B., Hoekstra, H. E. &


Nachman, M. W. Adaptive reptile color variation and the evolution of the _MC1R_ gene. _Evolution Int. J. Org. Evolution_ 58, 1794–1808 (2004) CAS  Google Scholar  * Mundy, N. I. et al.


Conserved genetics basis of a quantitative plumage trait involved in mate choice. _Science_ 303, 1870–1873 (2004) Article  CAS  ADS  Google Scholar  * Steiner, C. C., Weber, J. N. &


Hoekstra, H. E. Adaptive variation in beach mice produced by two interacting pigmentation genes. _PLoS Biol._ 5, e239 (2007) Article  Google Scholar  * Miller, C. T. et al. _cis_-regulatory


changes in Kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. _Cell_ 131, 1179–1189 (2007) Article  CAS  Google Scholar  * Protas, M. E. et al. Genetic


analysis of cavefish reveals molecular convergence in the evolution of albinism. _Nature Genet._ 38, 107–111 (2006) Article  CAS  Google Scholar  * Dahlhoff, E. P. & Rank, N. E.


Functional and physiological consequences of genetic variation at phosphoglucose isomerase: Heat shock protein expression is related to enzyme genotype in a montane beetle. _Proc. Natl Acad.


Sci. USA_ 97, 10056–10061 (2000) Article  CAS  ADS  Google Scholar  * Haag, C. R., Saastamoinen, M., Marden, J. H. & Hanski, I. A candidate locus for variation in dispersal rate in a


butterfly metapopulation. _Proc. Biol. Sci._ 272, 2449–2456 (2005) Article  Google Scholar  * Whitehead, A. & Crawford, D. L. Variation within and among species in gene expression: raw


material for evolution. _Mol. Ecol._ 15, 1197–1211 (2006) Article  CAS  Google Scholar  * Derome, N. & Bernatchez, L. The transcriptomics of ecological convergence between two limnetic


coregonine fishes (Salmonidae). _Mol. Biol. Evol._ 23, 2370–2378 (2006) Article  CAS  Google Scholar  * Gilad, Y., Oshlack, A. & Rifkin, S. A. Natural selection on gene expression.


_Trends Genet._ 22, 456–461 (2006) Article  CAS  Google Scholar  * Gibson, G. & Weir, B. The quantitative genetics of transcription. _Trends Genet._ 21, 616–623 (2005) Article  CAS 


Google Scholar  * Ellegren, H. & Parsch, J. The evolution of sex-biased genes and sex-biased gene expression. _Nature Rev. Genet._ 8, 689–698 (2007) Article  CAS  Google Scholar  *


Nussey, D. H., Postma, E., Gienapp, P. & Visser, M. E. Selection on heritable phenotypic plasticity in a wild bird population. _Science_ 310, 304–306 (2005) Article  CAS  ADS  Google


Scholar  * Charmantier, A. & Sheldon, B. C. Testing genetic models of mate choice evolution in the wild. _Trends Ecol. Evol._ 21, 417–419 (2006) Article  Google Scholar  * Frank, S. A.


George Price's contributions to evolutionary genetics. _J. Theor. Biol._ 175, 373–388 (1995) Article  CAS  Google Scholar  * Lande, R. A quantitative genetic theory of life history


evolution. _Ecology_ 63, 607–615 (1982) Article  Google Scholar  * Lande, R. & Arnold, S. J. The measurement of selection on correlated characters. _Evolution Int. J. Org. Evolution_ 37,


1210–1226 (1983) Article  Google Scholar  * Metcalf, C. J. E. & Pavard, S. Why evolutionary biologists should be demographers. _Trends Ecol. Evol._ 22, 205–212 (2007) Article  Google


Scholar  * Coulson, T. et al. Estimating individual contributions to population growth: evolutionary fitness in ecological time. _Proc. R. Soc. Lond. Ser. B_ 273, 547–555 (2006) Article  CAS


  Google Scholar  * Fisher, R. A. _The Genetical Theory of Natural Selection_ (Clarendon Press, Oxford, 1930) Book  Google Scholar  * Price, G. R. Fisher's ‘fundamental theorem’ made


clear. _Ann. Hum. Genet._ 36, 129–140 (1972) Article  CAS  MathSciNet  Google Scholar  * Schneider, R. A. & Helms, J. A. The cellular and molecular origins of beak morphology. _Science_


299, 565–568 (2003) Article  CAS  ADS  Google Scholar  * Abzhanov, A. et al. _Bmp4_ and morphological variation of beaks in Darwin's finches. _Science_ 305, 1462–1465 (2004) Article 


CAS  ADS  Google Scholar  * Abzhanov, A. et al. The calmodulin pathway and evolution of elongated beak morphology in Darwin's finches. _Nature_ 442, 563–567 (2006) Article  CAS  ADS 


Google Scholar  Download references ACKNOWLEDGEMENTS This work was supported by grants from the Swedish Research Council (H.E.) and by a Royal Society University Research Fellowship and an


Erskine Fellowship (B.C.S). AUTHOR CONTRIBUTIONS H.E. and B.C.S. wrote the paper together. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Department of Evolutionary Biology, Evolutionary


Biology Centre, Uppsala University, Norbyvägen 18D, SE-752 36 Uppsala, Sweden, Hans Ellegren * Department of Zoology, Edward Grey Institute, University of Oxford, South Parks Road, Oxford


OX1 3PS, UK, Ben C. Sheldon Authors * Hans Ellegren View author publications You can also search for this author inPubMed Google Scholar * Ben C. Sheldon View author publications You can


also search for this author inPubMed Google Scholar CORRESPONDING AUTHORS Correspondence to Hans Ellegren or Ben C. Sheldon. RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS


ARTICLE CITE THIS ARTICLE Ellegren, H., Sheldon, B. Genetic basis of fitness differences in natural populations. _Nature_ 452, 169–175 (2008). https://doi.org/10.1038/nature06737 Download


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