Uncovering cryptic genetic variation
Abstract
Cryptic genetic variation is the dark matter of biology: it is variation that is not normally seen, but that might be an essential source of physiological and evolutionary potential. It is uncovered by environmental or genetic perturbations, and is thought to modify the penetrance of common diseases, the response of livestock and crops to artificial selection and the capacity of populations to respond to the emergence of a potentially advantageous macro-mutation. We argue in this review that cryptic genetic variation is pervasive but under-appreciated, we highlight recent progress in determining the nature and identity of genes that underlie cryptic genetic effects and we outline future research directions.
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This is true of threshold-dependent characters and cryptic variation as well as continuous variation.
“This is as true of threshold-dependent characters and cryptic variation93 as it is of continuous variation.”
From Rare and common variants: twenty arguments (2012) · cites this paper as [93]
Cites
Introduction to Quantitative Genetics.
Edwards, A. W. F., & Falconer, D. S. (1982) · Biometrics · doi:10.2307/2529912 · Cited by 21,447 · see citing works
The genetical theory of natural selection
Fisher, R. A. (1930) · doi:10.5962/bhl.title.27468 · Cited by 17,617 · see citing works
Genetics and Analysis of Quantitative Traits
(2002) · Journal of Animal Breeding and Genetics · doi:10.1046/j.1439-0388.2002.00356.x · Cited by 6,172 · see citing works
Introduction to Quantitative Genetics
J.-M., G., & Falconer, D. S. (1962) · Population · doi:10.2307/1525780 · Cited by 3,773 · see citing works
Hsp90 as a capacitor for morphological evolution
Rutherford, S. L., & Lindquist, S. (1998) · Nature · doi:10.1038/24550 · Cited by 2,270 · see citing works
Systematic Genetic Analysis with Ordered Arrays of Yeast Deletion Mutants
Tong, A. H. Y., Evangelista, M., Parsons, A. B., Xu, H., Bader, G. D., Pagé, N., Robinson, M., Raghibizadeh, S., Hogue, C. W. V., Bussey, H., et al. (2001) · Science · doi:10.1126/science.1065810 · Cited by 2,138 · see citing works
Genetics and analysis of quantitative traits
Ewens, W. J. (1999) · American Journal of Human Biology · doi:10.1002/(sici)1520-6300(199911/12)11:6 · Cited by 2,084 · see citing works
A vision for the future of genomics research
Collins, F. S., Green, E. D., Guttmacher, A. E., Guyer, M. S., & on behalf of the US National Human Genome Research Institute (2003) · Nature · doi:10.1038/nature01626 · Cited by 1,752 · see citing works
McAlpine, J. F., Peterson, B. V., Shewell, G. E., Teskey, H. J., Vockeroth, J. R., & Wood, D. M. (1981) · Research Branch, Agriculture Canada, eBooks · Cited by 1,611 · see citing works
Genetics of gene expression surveyed in maize, mouse and man
Schadt, E., Monks, S. A., Drake, T., Lusis, A., Che, N., Colinayo, V. V., Ruff, T., Milligan, S. B., Lamb, J., Cavet, G., et al. (2003) · Nature · doi:10.1038/nature01434 · Cited by 1,594 · see citing works
Targeted Disruption of Mouse EGF receptor: Effect of Genetic Background on Mutant Phenotype
Threadgill, D. W., Dlugosz, A. A., Hansen, L. A., Tennenbaum, T., Lichti, U. F., Yee, D., LaMantia, C., Mourton, T., Herrup, K., Harris, R. C., et al. (1995) · Science · doi:10.1126/science.7618084 · Cited by 1,460 · see citing works
Hsp90 as a capacitor of phenotypic variation
Queitsch, C., Sangster, T. A., & Lindquist, S. (2002) · Nature · doi:10.1038/nature749 · Cited by 1,372 · see citing works
The causes of molecular evolution
Gillespie, J. H. (1992) · Choice Reviews Online · doi:10.5860/choice.30-2064 · Cited by 1,244 · see citing works
GENETIC ASSIMILATION OF AN ACQUIRED CHARACTER
Waddington, C. H. (1953) · Evolution · doi:10.1111/j.1558-5646.1953.tb00070.x · Cited by 1,187 · see citing works
The Genetic Architecture of Quantitative Traits
Mackay, T. F. C. (2001) · Annual Review of Genetics · doi:10.1146/annurev.genet.35.102401.090633 · Cited by 1,106 · see citing works
Canalization of Development and Genetic Assimilation of Acquired Characters
Waddington, C. H. (1959) · Nature · doi:10.1038/1831654a0 · Cited by 1,100 · see citing works
Epistasis: too often neglected in complex trait studies?
Carlborg, Ö., & Haley, C. (2004) · Nature Reviews Genetics · doi:10.1038/nrg1407 · Cited by 926 · see citing works
THE POPULATION GENETICS OF ADAPTATION: THE DISTRIBUTION OF FACTORS FIXED DURING ADAPTIVE EVOLUTION
Orr, H. A. (1998) · Evolution · doi:10.1111/j.1558-5646.1998.tb01823.x · Cited by 895 · see citing works
Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks
Shapiro, M. D., Marks, M. E., Peichel, C. L., Blackman, B. K., Nereng, K. S., Jónsson, B., Schluter, D., & Kingsley, D. M. (2004) · Nature · doi:10.1038/nature02415 · Cited by 843 · see citing works
The triple helix: gene, organism, and environment
(2000) · Choice Reviews Online · doi:10.5860/choice.38-0277 · Cited by 831 · see citing works
Principles for the buffering of genetic variation
Hartman, J. L., Garvik, B., & Hartwell, L. (2001) · Science · doi:10.1126/science.1056072 · Cited by 808 · see citing works
Principles for the Buffering of Genetic Variation
Hartman IV, J. L. (2001) · Science · doi:10.1126/science.291.5506.1001 · Cited by 808 · see citing works
PERSPECTIVE: EVOLUTION AND DETECTION OF GENETIC ROBUSTNESS
de Visser, J. A. G. M., Hermisson, J., Wagner, G. P., Ancel, L. W., Bagheri, H. C., Blanchard, J. L., Chao, L., Cheverud, J. M., Elena, S. F., Fontana, W., et al. (2003) · Evolution · doi:10.1111/j.0014-3820.2003.tb00377.x · Cited by 695 · see citing works
Self-citationEVOLUTIONARY QUANTITATIVE GENETICS: HOW LITTLE DO WE KNOW?
Barton, N. H., & Turelli, M. (1989) · Annual Review of Genetics · doi:10.1146/annurev.ge.23.120189.002005 · Cited by 686 · see citing works
The Causes of Molecular Evolution
Gillespie, J. H. (1992) · doi:10.1093/oso/9780195068832.001.0001 · Cited by 644 · see citing works
Trans-acting regulatory variation in Saccharomyces cerevisiae and the role of transcription factors
Yvert, G., Brem, R. B., Whittle, J., Akey, J. M., Foss, E. J., Smith, E. N., Mackelprang, R., & Kruglyak, L. (2003) · Nature Genetics · doi:10.1038/ng1222 · Cited by 629 · see citing works
Modifier genes in mice and humans
Nadeau, J. H. (2001) · Nature Reviews Genetics · doi:10.1038/35056009 · Cited by 574 · see citing works
The complex interplay among factors that influence allelic association
Zondervan, K. T., & Cardon, L. R. (2004) · Nature Reviews Genetics · doi:10.1038/nrg1270 · Cited by 571 · see citing works
A POPULATION GENETIC THEORY OF CANALIZATION
Wagner, G. P., Booth, G., & Bagheri, H. C. (1997) · Evolution · doi:10.1111/j.1558-5646.1997.tb02420.x · Cited by 561 · see citing works
THE EVOLUTION OF POSTZYGOTIC ISOLATION: ACCUMULATING DOBZHANSKY-MULLER INCOMPATIBILITIES
Orr, H. A., & Turelli, M. (2001) · Evolution · doi:10.1111/j.0014-3820.2001.tb00628.x · Cited by 553 · see citing works
Evolutionary capacitance as a general feature of complex gene networks
Bergman, A., & Siegal, M. L. (2003) · Nature · doi:10.1038/nature01765 · Cited by 520 · see citing works
Epistasis and its contribution to genetic variance components.
Cheverud, J. M., & Routman, E. J. (1995) · Genetics · doi:10.1093/genetics/139.3.1455 · Cited by 519 · see citing works
Driever, W., Thoma, G., & Nüsslein‐Volhard, C. (1989) · Nature · doi:10.1038/340363a0 · Cited by 432 · see citing works
Quantitative trait loci in Drosophila
Mackay, T. F. C. (2001) · Nature Reviews Genetics · doi:10.1038/35047544 · Cited by 425 · see citing works
Genetic Analysis of Inherited Hypertension in the Rat
Rapp, J. P. (2000) · Physiological Reviews · doi:10.1152/physrev.2000.80.1.135 · Cited by 424 · see citing works
TWELVE YEARS OF CONTEMPORARY ARMOR EVOLUTION IN A THREESPINE STICKLEBACK POPULATION
Bell, M. A., Aguirre, W. E., & Buck, N. J. (2004) · Evolution · doi:10.1111/j.0014-3820.2004.tb00414.x · Cited by 374 · see citing works
PERSPECTIVE:EVOLUTION AND DETECTION OF GENETIC ROBUSTNESS
de Visser, J. A. G. M., Hermisson, J., Wagner, G. P., et al. (2003) · Evolution · doi:10.1554/02-750r · Cited by 364 · see citing works
GENETIC ASSIMILATION OF THEBITHORAXPHENOTYPE
Waddington, C. H. (1956) · Evolution · doi:10.1111/j.1558-5646.1956.tb02824.x · Cited by 340 · see citing works
Pattern of polymorphism after strong artificial selection in a domestication event
Innan, H., & Kim, Y. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401720101 · Cited by 332 · see citing works
Developmental instability: Causes and consequences
Lalumière, M. L. (2004) · American Journal of Human Biology · doi:10.1002/ajhb.20050 · Cited by 320 · see citing works
The Distribution of Fitness Effects Among Beneficial Mutations
Orr, H. A. (2003) · Genetics · doi:10.1093/genetics/163.4.1519 · Cited by 298 · see citing works
Between genotype and phenotype: protein chaperones and evolvability
Rutherford, S. L. (2003) · Nature Reviews Genetics · doi:10.1038/nrg1041 · Cited by 292 · see citing works
The role of CCR5 and CCR2 polymorphisms in HIV-1 transmission and disease progression
Michael, N. L., Louie, L. G., Rohrbaugh, A. L., Schultz, K., Dayhoff, D. E., Wang, C. E., & Sheppard, H. W. (1997) · Nature Medicine · doi:10.1038/nm1097-1160 · Cited by 251 · see citing works
Meiklejohn, C. D., & Hartl, D. L. (2002) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(02)02596-x · Cited by 251 · see citing works
Turelli, M., & Barton, N. (2004) · Genetics · doi:10.1534/genetics.166.2.1053 · Cited by 244 · see citing works
The Ras signaling pathway in Drosophila
Wassarman, D. A., Therrien, M., & Rubin, G. M. (1995) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(95)90052-7 · Cited by 233 · see citing works
Canalization: Genetic And Developmental Aspects
Scharloo, W. (1991) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.es.22.110191.000433 · Cited by 230 · see citing works
A Microsatellite-Based Multilocus Screen for the Identification of Local Selective Sweeps
Schlötterer, C. (2002) · Genetics · doi:10.1093/genetics/160.2.753 · Cited by 229 · see citing works
Kondrashov, A. S., & Houle, D. (1994) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1994.0166 · Cited by 225 · see citing works
Leips, J., & Mackay, T. F. C. (2000) · Genetics · doi:10.1093/genetics/155.4.1773 · Cited by 221 · see citing works
Detecting Bottlenecks and Selective Sweeps From DNA Sequence Polymorphism
Galtier, N., Depaulis, F., & Barton, N. (2000) · Genetics · doi:10.1093/genetics/155.2.981 · Cited by 201 · see citing works
Transposon-Based Strategies for Microbial Functional Genomics and Proteomics
Hayes, F. (2003) · Annual Review of Genetics · doi:10.1146/annurev.genet.37.110801.142807 · Cited by 198 · see citing works
Dopa decarboxylase (Ddc) affects variation in Drosophila longevity
Luca, M. D., Roschina, N. V., Geiger-Thornsberry, G. L., Lyman, R. F., PASYUKOVA, E. G., & Mackay, T. F. C. (2003) · Nature Genetics · doi:10.1038/ng1218 · Cited by 193 · see citing works
Population, Evolutionary and Genomic Consequences of Interference Selection
Comeron, J. M., & Kreitman, M. (2002) · Genetics · doi:10.1093/genetics/161.1.389 · Cited by 184 · see citing works
Selection for large and small size in mice
Falconer, D. S. (1953) · Journal of Genetics · doi:10.1007/bf02982939 · Cited by 180 · see citing works
Neutral additive genetic variance in a metapopulation
WHITLOCK, M. C. (1999) · Genetical Research · doi:10.1017/s0016672399004127 · Cited by 180 · see citing works
SELECTIVE NEUTRALITY OF 6PGD ALLOZYMES IN E. COLI AND THE EFFECTS OF GENETIC BACKGROUND
Dykhuizen, D. E., & Hartl, D. L. (1980) · Genetics · doi:10.1093/genetics/96.4.801 · Cited by 179 · see citing works
Effect of Polymorphism in the Drosophila Regulatory Gene Ultrabithorax on Homeotic Stability
Gibson, G. C., & Hogness, D. S. (1996) · Science · doi:10.1126/science.271.5246.200 · Cited by 176 · see citing works
Self-citationTo be or not to be active: the stochastic nature of enhancer action
Fiering, S., Whitelaw, E., & Martin, D. I. K. (2000) · BioEssays · doi:10.1002/(sici)1521-1878(200004)22:4 · Cited by 159 · see citing works
Self-citationPositive Selection on a Human-Specific Transcription Factor Binding Site Regulating IL4 Expression
Rockman, M. V., Hahn, M. W., Soranzo, N., Goldstein, D. B., & Wray, G. A. (2003) · Current Biology · doi:10.1016/j.cub.2003.11.025 · Cited by 131 · see citing works
How responses get more switch-like as you move down a protein kinase cascade
Ferrell, J. E. (1997) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(97)82217-7 · Cited by 127 · see citing works
Lauter, N., & Doebley, J. (2002) · Genetics · doi:10.1093/genetics/160.1.333 · Cited by 116 · see citing works
CANALIZATION OF THE SCUTE PHENOTYPE OF DROSOPHILA
RENDEL, J. M. (1959) · Evolution · doi:10.1111/j.1558-5646.1959.tb03033.x · Cited by 110 · see citing works
Canalization, Genetic Assimilation and Preadaptation: A Quantitative Genetic Model
Eshel, I., & Matessi, C. (1998) · Genetics · doi:10.1093/genetics/149.4.2119 · Cited by 99 · see citing works
Dworkin, I. M., Pálsson, A., Birdsall, K., & Gibson, G. C. (2003) · Current Biology · doi:10.1016/j.cub.2003.10.001 · Cited by 98 · see citing works
Self-citationEVOLUTION AND DETECTION OF GENETIC ROBUSTNESS
de Visser, J. A. G. M., Hermisson, J., Ancel, L. W., Bagheri, H. C., Blanchard, J. L., Chao, L., Cheverud, J. M., Elena, S. F., Gibson, G. C., Hansen, T. F., et al. (2003) · Cited by 98 · see citing works
Self-citationThe Genetic Architecture of Drosophila Sensory Bristle Number
Dilda, C. L., & Mackay, T. F. C. (2002) · Genetics · doi:10.1093/genetics/162.4.1655 · Cited by 95 · see citing works
Selection for an Invariant Character—‘Vibrissa Number’—in the House Mouse
Dun, R., & Fraser, A. (1958) · Nature · doi:10.1038/1811018a0 · Cited by 94 · see citing works
Modifier genes in cystic fibrosis lung disease
Merlo, C. A., & Boyle, M. (2003) · Journal of Laboratory and Clinical Medicine · doi:10.1067/mlc.2003.29 · Cited by 76 · see citing works
The genetic assimilation of four venation phenocopies
Bateman, K. G. (1959) · Journal of Genetics · doi:10.1007/bf02984796 · Cited by 75 · see citing works
Naturally occurring genetic variation affects Drosophila photoreceptor determination
Polaczyk, P., Gasperini, R., & Gibson, G. C. (1998) · Development Genes and Evolution · doi:10.1007/s004270050137 · Cited by 67 · see citing works
Self-citationHuether, C. A. (1968) · Genetics · doi:10.1093/genetics/60.1.123 · Cited by 59 · see citing works
Association Between Nucleotide Variation in Egfr and Wing Shape in Drosophila melanogaster
Pálsson, A., & Gibson, G. C. (2004) · Genetics · doi:10.1534/genetics.103.021766 · Cited by 58 · see citing works
Self-citationHaag, E. S., & True, J. (2001) · Evolution · doi:10.1111/j.0014-3820.2001.tb00627.x · Cited by 57 · see citing works
Gibson, G. C., Wemple, M., & van Helden, S. (1999) · Genetics · doi:10.1093/genetics/151.3.1081 · Cited by 54 · see citing works
Self-citationIs Hsp90 a regulator of evolvability?
Wagner, G. P., Chiu, C.-H., & Hansen, T. F. (1999) · Journal of Experimental Zoology · doi:10.1002/(sici)1097-010x(19990815)285:2 · Cited by 53 · see citing works
Is Function of the Drosophila Homeotic Gene Ultrabithorax Canalized?
Gibson, G. C., & van Helden, S. (1997) · Genetics · doi:10.1093/genetics/147.3.1155 · Cited by 51 · see citing works
Self-citationGENETIC ARCHITECTURE, GENETIC BEHAVIOR, AND CHARACTER EVOLUTION
Moreno, G. H. (1994) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.es.25.110194.000335 · Cited by 50 · see citing works
Pélabon, C., Carlson, M. L., Hansen, T. F., Yoccoz, N. G., & Armbruster, W. S. (2004) · Journal of Evolutionary Biology · doi:10.1046/j.1420-9101.2003.00663.x · Cited by 43 · see citing works
Bubliy, O. A., Loeschcke, V., & Imasheva, A. G. (2000) · Evolution · doi:10.1554/0014-3820(2000)054[1444:eosang]2.0.co;2 · Cited by 37 · see citing works
Complex genetics of Type 2 diabetes: thrifty genes and previously neutral polymorphisms
Turner, R. C., Levy, J. C., & Clark, A. (1993) · QJM · doi:10.1093/oxfordjournals.qjmed.a068835 · Cited by 34 · see citing works
A mechanistic study of evolvability using the mitogen‐activated protein kinase cascade
Nijhout, H. F., Berg, A., & Gibson, W. T. (2003) · Evolution & Development · doi:10.1046/j.1525-142x.2003.03035.x · Cited by 31 · see citing works
On models of quantitative genetic variability: a stabilizing selection-balance model.
Анатольевич, Ж. Л., & Feldman, M. W. (1992) · Genetics · doi:10.1093/genetics/130.4.947 · Cited by 26 · see citing works
Sheldon, B. L., & Milton, M. K. (1972) · Genetics · doi:10.1093/genetics/71.4.567 · Cited by 25 · see citing works
Evolution: Hox genes and the cellared wine principle
Gibson, G. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00531-5 · Cited by 24 · see citing works
Self-citationA GENETIC ANALYSIS OF THE KILLER-PRUNE (K-pn) LOCUS OF DROSOPHILA MELANOGASTER
Lifschytz, E., & Falk, R. (1969) · Genetics · doi:10.1093/genetics/62.2.353 · Cited by 23 · see citing works
Phinchongsakuldit, J. (2003) · Molecular Biology and Evolution · doi:10.1093/molbev/msh025 · Cited by 18 · see citing works
Milkman, R. (1960) · Genetics · doi:10.1093/genetics/45.4.377 · Cited by 17 · see citing works
Milkman, R. (1965) · Genetics · doi:10.1093/genetics/51.1.87 · Cited by 13 · see citing works
PRELIMINARY GENETIC ANALYSIS OF CROSSVEINLESS-LIKE STRAINS OF DROSOPHILA MELANOGASTER
Mohler, J. D. (1965) · Genetics · doi:10.1093/genetics/51.4.641 · Cited by 11 · see citing works
Mohler, J. D. (1965) · Genetics · doi:10.1093/genetics/51.3.329 · Cited by 10 · see citing works
Flagged first, then by citations
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Adaptation from standing genetic variation
BARRETT, R., & SCHLUTER, D. (2008) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2007.09.008 · Cited by 2,091 · see citing works
Sporns, O., & Betzel, R. F. (2016) · Annual Review of Psychology · doi:10.1146/annurev-psych-122414-033634 · Cited by 1,334 · see citing works
“In genetics, such external fluctuations could relate to the effects of cryptic genetic variation, which uncovers novel phenotypes under conditions of environmental change (Gibson & Dworkin 2004), thus potentially promoting increased robustness.”
BackgroundRare and common variants: twenty arguments
Gibson, G. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3118 · Cited by 1,278 · see citing works
“This is as true of threshold-dependent characters and cryptic variation”
BackgroundSelf-citationEarly Developmental Conditioning of Later Health and Disease: Physiology or Pathophysiology?
Hanson, M. A., & Gluckman, P. D. (2014) · Physiological Reviews · doi:10.1152/physrev.00029.2013 · Cited by 1,188 · see citing works
Phenotypic plasticity's impacts on diversification and speciation
Pfennig, D. W., Wund, M. A., Snell-Rood, E. C., Cruickshank, T., Schlichting, C. D., & Moczek, A. P. (2010) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2010.05.006 · Cited by 1,170 · see citing works
Evolution, the Extended Synthesis
Pigliucci, M., & Müller, G. (2010) · The MIT Press eBooks · doi:10.7551/mitpress/9780262513678.001.0001 · Cited by 966 · see citing works
The evolutionary origins of pesticide resistance
Hawkins, N. J., Bass, C., Dixon, A. L., & Neve, P. (2018) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12440 · Cited by 847 · see citing works
Epistasis and quantitative traits: using model organisms to study gene–gene interactions
Mackay, T. F. C. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3627 · Cited by 824 · see citing works
Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity
Murren, C. J., Auld, J. R., Callahan, H., Ghalambor, C. K., Handelsman, C. A., Heskel, M., Kingsolver, J. G., MacLean, H. J., Joanna Masel, A., Maughan, H., et al. (2015) · Heredity · doi:10.1038/hdy.2015.8 · Cited by 691 · see citing works
THE QTN PROGRAM AND THE ALLELES THAT MATTER FOR EVOLUTION: ALL THAT'S GOLD DOES NOT GLITTER
Rockman, M. V. (2011) · Evolution · doi:10.1111/j.1558-5646.2011.01486.x · Cited by 661 · see citing works
Past and Future Use of Wild Relatives in Crop Breeding
Dempewolf, H., Baute, G. J., Anderson, J., Kilian, B., Smith, C., & Guarino, L. (2017) · Crop Science · doi:10.2135/cropsci2016.10.0885 · Cited by 626 · see citing works
“This “hidden” or “cryptic” variation can sometimes be revealed during the crossing process in transgressive segregation (deVicente and Tanksley, 1993; Xu et al., 1998; Gibson and Dworkin, 2004).”
BackgroundThe role of developmental plasticity in evolutionary innovation
Moczek, A. P., Sultan, S. E., Foster, S. A., Ledón‐Rettig, C. C., Dworkin, I. M., Nijhout, H. F., Abouheif, E., & Pfennig, D. W. (2011) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2011.0971 · Cited by 589 · see citing works
Self-citationCanalization of development by microRNAs
Hornstein, E., & Shomron, N. (2006) · Nature Genetics · doi:10.1038/ng1803 · Cited by 511 · see citing works
Cryptic genetic variation: evolution's hidden substrate
Paaby, A. B., & Rockman, M. V. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3688 · Cited by 500 · see citing works
Crispo, E. (2007) · Evolution · doi:10.1111/j.1558-5646.2007.00203.x · Cited by 513 · see citing works
“Genetic assimilation could also allow for the accumulation of cryptic genetic variation, which could later become expressed after removal of the canalizing factor, or “de-canalization,” thus promoting evolvability (Rutherford and Lindquist 1998, Gibson and Dworkin 2004; Flatt 2005).”
BackgroundThe Origins of Plant Cultivation and Domestication in the New World Tropics
Piperno, D. R. (2011) · Current Anthropology · doi:10.1086/659998 · Cited by 481 · see citing works
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BackgroundThe Evolutionary Genetics of Canalization
Flatt, T. (2005) · The Quarterly Review of Biology · doi:10.1086/432265 · Cited by 459 · see citing works
“Why are some traits phenotypically invariant despite apparent genetic and environmental changes? Why are some traits less phenotypically variable in some taxa, but not in others? One of the most intriguing observations in evolutionary genetics is that wild-type populations often harbor vast amounts of hidden genetic v…”
BackgroundMethodInfluentialStress-induced variation in evolution: from behavioural plasticity to genetic assimilation
Badyaev, A. V. (2005) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2004.3045 · Cited by 442 · see citing works
“However, it is not clear how genetic and developmental systems can accumulate and store phenotypically neutral genetic variation while not expressing it (Wagner & Mezey 2000; Hermisson et al. 2003; Masel & Bergman 2003; Gibson & Dworkin 2004).”
BackgroundThe Evolution of Genetic Architecture
Hansen, T. F. (2006) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev.ecolsys.37.091305.110224 · Cited by 420 · see citing works
“…through epistatic interactions with an evolving genetic background (Wagner et al. 1997), and is currently the focus of considerable theoretical and empirical interest (de Visser et al. 2003, Dworkin 2005a, Flatt 2005, Gibson & Dworkin 2004, Gibson & Wagner 2000, Rutherford 2000, Wagner 2005).”
BackgroundEvolution of a Polyphenism by Genetic Accommodation
Suzuki, Y., & Nijhout, H. F. (2006) · Science · doi:10.1126/science.1118888 · Cited by 411 · see citing works
The theory of facilitated variation
Gerhart, J. C., & Kirschner, M. W. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701035104 · Cited by 404 · see citing works
The quantitative genetics of transcription
Gibson, G. C., & Weir, B. S. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.08.010 · Cited by 350 · see citing works
Self-citationPervasive robustness in biological systems
Félix, M., & Barkoulas, M. (2015) · Nature Reviews Genetics · doi:10.1038/nrg3949 · Cited by 319 · see citing works
The gene balance hypothesis: implications for gene regulation, quantitative traits and evolution
Birchler, J. A., & Veitia, R. A. (2009) · New Phytologist · doi:10.1111/j.1469-8137.2009.03087.x · Cited by 317 · see citing works
“The basis of why these selection experiments seem to respond so well is still a matter of debate as to whether they do so from standing variation, new mutations, epigenetic changes (Gibson & Dworkin, 2004; Johannes et al., 2008) or a combination of the above.”
BackgroundDecanalization and the origin of complex disease
Gibson, G. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2502 · Cited by 285 · see citing works
“Susceptibility variants will often be recently exposed cryptic factor”
BackgroundSelf-citationMasel, J., & Trotter, M. V. (2010) · Trends in Genetics · doi:10.1016/j.tig.2010.06.002 · Cited by 287 · see citing works
“The other focuses on gene networks and morphological traits in multicellular organisms, and uses the Waddingtonian metaphors of canalization, cryptic genetic variation, and genetic assimilation [8,17,18,20,21,23–25, 28, 32–34, 41–44, 74].”
BackgroundDistributed robustness versus redundancy as causes of mutational robustness
Wagner, A. (2005) · BioEssays · doi:10.1002/bies.20170 · Cited by 290 · see citing works
“Such cryptic genetic variation is ubiquituous and it can affect phenomena as different as variation in genetic disease phenotypes and reproductive isolation.((5)) It is thus not surprising that biologists have a long-standing interest in robustness, going back to Fisher’s work on dominance,((6)) as well as to Waddingt…”
BackgroundPHENOTYPIC PLASTICITY AND EPIGENETIC MARKING: AN ASSESSMENT OF EVIDENCE FOR GENETIC ACCOMMODATION
Schlichting, C. D., & Wund, M. A. (2014) · Evolution · doi:10.1111/evo.12348 · Cited by 284 · see citing works
“Exposing such cryptic genetic variation may have significant effects on the evolutionary trajectories of populations (Gibson and Dworkin 2004; Dworkin 2005a; Flatt 2005; Moczek 2007; Le Rouzic and Carlborg 2008; Schlichting 2008; McGuigan and Sgrò 2009; Masel and Trotter 2010; Draghi and Whitlock…”
BackgroundEpistasis and balanced polymorphism influencing complex trait variation
Kroymann, J., & Mitchell‐Olds, T. (2005) · Nature · doi:10.1038/nature03480 · Cited by 274 · see citing works
Snell‐Rood, E. C., Dyken, J. D. V., Cruickshank, T. E., Wade, M. J., & Moczek, A. P. (2009) · BioEssays · doi:10.1002/bies.200900132 · Cited by 272 · see citing works
“The release of cryptic genetic variation during shifts into novel or stressful environments has long been hypothesized to facilitate evolutionary change;((79,80)) relaxed selection on environment-specific genes may provide a general mechanism by which this variability accumulates.”
BackgroundEvolutionary origins of invasive populations
Lee, C. E., & Gelembiuk, G. W. (2008) · Evolutionary Applications · doi:10.1111/j.1752-4571.2008.00039.x · Cited by 261 · see citing works
Hidden Reaction Norms, Cryptic Genetic Variation, and Evolvability
Schlichting, C. D. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1438.010 · Cited by 261 · see citing works
““Adaptive walks are shaped by CGV” (Gibson & Dworkin 2004).”
BackgroundCryptic genetic variation promotes rapid evolutionary adaptation in an RNA enzyme
Hayden, E. J., Ferrada, E., & Wagner, A. (2011) · Nature · doi:10.1038/nature10083 · Cited by 221 · see citing works
Genetic assimilation: a review of its potential proximate causes and evolutionary consequences
Ehrenreich, I. M., & Pfennig, D. W. (2015) · Annals of Botany · doi:10.1093/aob/mcv130 · Cited by 212 · see citing works
Robustness and evolution: concepts, insights and challenges from a developmental model system
Félix, M.-A., & Wagner, A. (2008) · Heredity · doi:10.1038/sj.hdy.6800915 · Cited by 210 · see citing works
“Gibson and Hogness 1996), or mutations (Rutherford 2000; Gibson and Dworkin 2004).”
BackgroundInfluentialMolecular analysis of flies selected for aggressive behavior
Dierick, H. A., & Greenspan, R. J. (2006) · Nature Genetics · doi:10.1038/ng1864 · Cited by 209 · see citing works
“Such cryptic genetic variation is pervasive but generally underestimate”
BackgroundGenetical Genomics: Spotlight on QTL Hotspots
Rainer Breitling, A., Li, Y., Tesson, B. M., Fu, J., Wu, C., Wiltshire, T., Gerrits, A., Bystrykh, L. V., de Haan, G., Su, A. I., et al. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000232 · Cited by 191 · see citing works
“For example, it might well be that biological systems are so robust against subtle genetic perturbations that the majority of heritable gene expression variation is effectively ‘‘buffered’’ and does not lead to downstream effects on other genes, protein, metabolites, or phenotypes [14–17].”
BackgroundBiological Robustness: Paradigms, Mechanisms, and Systems Principles
Whitacre, J. M. (2012) · Frontiers in Genetics · doi:10.3389/fgene.2012.00067 · Cited by 182 · see citing works
“However, exposing the population to new environments can reveal phenotypic differences and a lower degree of observed mutational robustness; a phenomenon known as CGV (Gibson and Dworkin, 2004).”
BackgroundGenetics of schizophrenia: new findings and challenges
Gejman, P. V., Sanders, A. R., & Kendler, K. S. (2011) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-082410-101459 · Cited by 183 · see citing works
Evolutionary potential of hidden genetic variation
Rouzic, A. L., & Carlborg, Ö. (2008) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2007.09.014 · Cited by 183 · see citing works
The choice of model organisms in evo–devo
Jenner, R. A., & Wills, M. A. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2062 · Cited by 183 · see citing works
Lenormand, T., Roze, D., & Rousset, F. (2009) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2008.09.014 · Cited by 177 · see citing works
Chandler, C. H., Chari, S., & Dworkin, I. M. (2013) · Trends in Genetics · doi:10.1016/j.tig.2013.01.009 · Cited by 174 · see citing works
Self-citationEco-Evo-Devo: The Time Has Come
Abouheif, E., Favé, M.-J., Ibarraran-Viniegra, A. S., Lesoway, M. P., Rafiqi, A. M., & Rajakumar, R. (2013) · Advances in experimental medicine and biology · doi:10.1007/978-94-007-7347-9_6 · Cited by 170 · see citing works
“vironmental stress is too great and robustness is compromised, “cryptic variation” is released (Gibson and Dworkin 2004).”
BackgroundThe origins of cancer robustness and evolvability
Tian, T., Olson, S., Whitacre, J. M., & Harding, A. S. (2010) · Integrative Biology · doi:10.1039/c0ib00046a · Cited by 168 · see citing works
Review of Quantitative Trait Loci Identified in the Chicken
Abasht, B., Dekkers, J. C. M., & Lamont, S. J. (2006) · Poultry Science · doi:10.1093/ps/85.12.2079 · Cited by 161 · see citing works
“In these cases, the transgressive effect is caused by epistasis in synergetic or antagonistic ways (Gibson and Dworkin, 2004; Carlborg et al., 2006).”
BackgroundAssessing the Impacts of Phenotypic Plasticity on Evolution
Wund, M. A. (2012) · Integrative and Comparative Biology · doi:10.1093/icb/ics050 · Cited by 159 · see citing works
“Alternatively, a new environment can release cryptic genetic variation, rapidly altering heritable phenotypic variance and potentially shifting phenotypic means within a single generation (Gibson and Dworkin 2004; Le Rouzic and Carlborg 2008; Schlichting 2008), which, in turn, impacts the rate and nature of responses…”
BackgroundHsp90 Selectively Modulates Phenotype in Vertebrate Development
Yeyati, P. L., Bancewicz, R. M., Maule, J., & van Heyningen, V. (2005) · PLoS Genetics · doi:10.1371/journal.pgen.0030043 · Cited by 159 · see citing works
“cryptic genetic variation in good health and disease [72].”
BackgroundEvolutionary consequences of cryptic genetic variation
McGuigan, K., & Sgrò, C. M. (2009) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2009.02.001 · Cited by 157 · see citing works
Higher-order genetic interactions and their contribution to complex traits
Taylor, M. B., & Ehrenreich, I. M. (2014) · Trends in Genetics · doi:10.1016/j.tig.2014.09.001 · Cited by 151 · see citing works
Studying phenotypic evolution using multivariate quantitative genetics
McGuigan, K. (2006) · Molecular Ecology · doi:10.1111/j.1365-294x.2006.02809.x · Cited by 150 · see citing works
“2003, 2004; Barton & Turelli 2004; Gibson & Dworkin 2004) highlights the lack of basic data on the prevalence of nonadditive variance.”
BackgroundGenomics of Developmental Plasticity in Animals
Lafuente, E., & Beldade, P. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00720 · Cited by 147 · see citing works
“Such genetic variation can then fuel evolutionary change (Gibson and Dworkin, 2004; Ledón-Rettig et al., 2010; Paaby and Rockman, 2014; Schneider and Meyer, 2017).”
BackgroundSkúlason, S., Parsons, K. J., Svanbäck, R., Räsänen, K., Ferguson, M. M., Adams, C. E., Amundsen, P., Bartels, P., Bean, C. W., BOUGHMAN, J. W., et al. (2019) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12534 · Cited by 145 · see citing works
“One emerging theme is that development itself is a progenitor of phenotypic variation as it responds to environmental cues (in the present and past), thereby determining what heritable phenotypic variation is exposed to selection (West-Eberhard, 2003; Gibson & Dworkin, 2004).”
BackgroundA Single Basis for Developmental Buffering of Drosophila Wing Shape
Breuker, C. J., Patterson, J., & Klingenberg, C. P. (2006) · PLoS ONE · doi:10.1371/journal.pone.0000007 · Cited by 139 · see citing works
“Developmental buffering is an important factor in evolutionary processes, because it can maintain adaptive phenotypic traits in the presence of genetic and environmental variation and it can conceal genetic variation from selection [1–3].”
BackgroundForsberg, S. K. G., Bloom, J. S., Sadhu, M. J., Kruglyak, L., & Carlborg, Ö. (2017) · Nature Genetics · doi:10.1038/ng.3800 · Cited by 134 · see citing works
Drury, C., Manzello, D. P., & Lirman, D. (2017) · PLoS ONE · doi:10.1371/journal.pone.0174000 · Cited by 138 · see citing works
Debat, V., Debelle, A., & Dworkin, I. M. (2009) · Evolution · doi:10.1111/j.1558-5646.2009.00774.x · Cited by 138 · see citing works
“…has concerned its genetic component (e.g., Visser et al. 2003), because it theoretically allows for the build up—and thus the occasional release—of cryptic genetic variation, potentially altering the pace of morphological evolution (Rutherford and Lindquist 1998; Gibson and Dworkin 2004).”
BackgroundSelf-citationPlasticity and Errors of a Robust Developmental System in Different Environments
Braendle, C., & Félix, M. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.09.011 · Cited by 136 · see citing works
“In turn, such mutational robustness would result in genetic divergence of underlying developmental mechanisms without generating changes in the final phenotype (Gibson and Dworkin, 2004; Wagner, 2005).”
BackgroundFlood, P. J., Kruijer, W., Schnabel, S., van der Schoor, R., Jalink, H., Snel, J. F. H., Harbinson, J., & Aarts, M. G. M. (2016) · Plant Methods · doi:10.1186/s13007-016-0113-y · Cited by 135 · see citing works
“Such variation in the growth environment can be used to uncover hidden genetic variation not expressed under control conditions and identify genes important for adaptation to environmental fluctuations [19].”
BackgroundNoble, D. W. A., Radersma, R., & Uller, T. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1821066116 · Cited by 133 · see citing works
“Exposure to a novel or stressful environment may also be associated with a general increase in additive genetic variation (23).”
BackgroundCryptic genetic variation accelerates evolution by opening access to diverse adaptive peaks
Zheng, J., Payne, J. L., & Wagner, A. (2019) · Science · doi:10.1126/science.aax1837 · Cited by 124 · see citing works
Cryptic Genetic Variation Is Enriched for Potential Adaptations
Masel, J. (2005) · Genetics · doi:10.1534/genetics.105.051649 · Cited by 123 · see citing works
“THERE has recently been much interest in the abil-ity of evolutionary capacitors to tap into cryptic or hidden genetic variation and reveal a range of phenotypes (Rutherford and Lindquist 1998; True and Lindquist 2000; Queitsch et al. 2002; Bergman and Siegal 2003; Gibson and Dworkin 2004).”
BackgroundRole of Pleiotropy in the Evolution of a Cryptic Developmental Variation in Caenorhabditis elegans
Duveau, F., & Félix, M. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001230 · Cited by 116 · see citing works
“Many developmental systems produce outputs that are insensitive to a wide range of environmental or genetic perturbations. In these robust systems, buffering may allow for the accumulation of “cryptic” genetic variation affecting the system without changing its end product”
BackgroundMunshi‐South, J., Zolnik, C. P., & Harris, S. E. (2016) · Evolutionary Applications · doi:10.1111/eva.12357 · Cited by 123 · see citing works
“2010), artificial selection in crops (Gibson and Dworkin 2004), viral pathogens (Pennings 2012), and invasive species (Prentis et al.”
BackgroundStudies of threespine stickleback developmental evolution: progress and promise
Cresko, W. A., McGuigan, K., Phillips, P. C., & Postlethwait, J. H. (2006) · Genetica · doi:10.1007/s10709-006-0036-z · Cited by 119 · see citing works
“tions of alleles, both of which may expose genetic variation for phenotypes (Gibson and Dworkin 2004).”
BackgroundHoekstra, L. A., Siddiq, M. A., & Montooth, K. L. (2013) · Genetics · doi:10.1534/genetics.113.154914 · Cited by 117 · see citing works
“While many mutations in core metabolic processes will disrupt energy metabolism such that the phenotypic effects are manifest under all conditions, those mutations segregating in natural populations are more likely to cause inefficiencies in metabolism that are only revealed when temperature accelerates biological rat…”
BackgroundPleiotropy, epistasis and the genetic architecture of quantitative traits
Mackay, T. F. C., & Anholt, R. R. H. (2024) · Nature Reviews Genetics · doi:10.1038/s41576-024-00711-3 · Cited by 118 · see citing works
“With epistasis, alleles have different effects in different genetic backgrounds, which causes variable allelic effects among individuals and populations 14 and affects the magnitude of expressed quantitative genetic variation 15 .”
InfluentialCRYPTIC GENETIC VARIATION AND BODY SIZE EVOLUTION IN THREESPINE STICKLEBACK
McGuigan, K., Nishimura, N., Currey, M. C., Hurwit, D., & Cresko, W. A. (2010) · Evolution · doi:10.1111/j.1558-5646.2010.01195.x · Cited by 118 · see citing works
“…thus on evolvability, has been suggested to contribute to patterns of evolutionary stasis in stable environments and rapid evolution in novel environments (Waddington 1957; Rutherford and Lindquist 1998; Gibson and Dworkin 2004; Badyaev 2005; Wagner 2005; Schlichting 2008; Masel and Siegal 2009).”
BackgroundGenome-wide patterns of divergence during speciation: the lake whitefish case study
Renaut, S., Maillet, N., Normandeau, É., Sauvage, C., Derôme, N., Rogers, S. M., & Bernatchez, L. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0197 · Cited by 114 · see citing works
Gómez-Mestre, I., & Jovani, R. (2013) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.1869 · Cited by 111 · see citing works
“Moreover, the accumulated genetic variation can be rapidly released and manifested in the face of further environmental or mutational changes, enabling rapid adaptive divergences [6,17,51,52].”
BackgroundPhenotypic plasticity, global change, and the speed of adaptive evolution
Gibert, P., Debat, V., & Ghalambor, C. K. (2019) · Current Opinion in Insect Science · doi:10.1016/j.cois.2019.06.007 · Cited by 110 · see citing works
Haerty, W., & Singh, R. S. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msl033 · Cited by 104 · see citing works
Spurious transcription factor binding: Non‐functional or genetically redundant?
Spivakov, M. (2014) · BioEssays · doi:10.1002/bies.201400036 · Cited by 96 · see citing works
“The phenomenon of ‘cryptic variability’ that is only uncovered by genetic or environmental perturbations has been described in other systems and is thought to be an important modifier of phenotypic response [114].”
BackgroundLedón‐Rettig, C. C., Pfennig, D. W., & Crespi, E. J. (2010) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2010.0877 · Cited by 101 · see citing works
“Here, we explore the proximate mechanisms that facilitate the evolution of resource-use traits by considering the role of ‘cryptic’ genetic variation (sensu Gibson & Dworkin 2004; Schlichting 2008) in fuelling evolutionary shifts in resource use.”
BackgroundKent, C. F., Daskalchuk, T. E., Cook, L., Sokolowski, M. B., & Greenspan, R. J. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000609 · Cited by 104 · see citing works
“Epistasis is identified as a two-way statistical interaction between the variant (rover or sitter) and test genotype (mutant or control) [26] (see below).”
BackgroundIt’s not magic – Hsp90 and its effects on genetic and epigenetic variation
Zabinsky, R. A., Mason, G. A., Queitsch, C., & Jarosz, D. F. (2018) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2018.05.015 · Cited by 104 · see citing works
Flexibility in a Gene Network Affecting a Simple Behavior in Drosophila melanogaster
van Swinderen, B., & Greenspan, R. J. (2005) · Genetics · doi:10.1534/genetics.104.032631 · Cited by 101 · see citing works
“Each of these partners, in turn, is likely to interact with a number of other proteins, analysis of sex-specific gene expression in two inbred strains (Gibson and Dworkin 2004) and also in individ-all of which are subject to regulation of their own.”
BackgroundMechanisms of mutational robustness in transcriptional regulation
Payne, J. L., & Wagner, A. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00322 · Cited by 95 · see citing works
“This was most likely facilitated by a protein-protein interaction with Mcm1, which is conserved among S. cerevisiae and C. albicans, and may have helped stabilize Matα1 while its interaction with DNA slowly changed.”
BackgroundThe Genetic Architecture of Skeletal Convergence and Sex Determination in Ninespine Sticklebacks
Shapiro, M. D., Summers, B. R., Balabhadra, S., Aldenhoven, J., Miller, A. L., Cunningham, C. B., Bell, M. A., & Kingsley, D. M. (2009) · Current Biology · doi:10.1016/j.cub.2009.05.029 · Cited by 96 · see citing works
“CGV is thought to be an important and pervasive, yet underappreciated, factor in the response of organisms to mutation, selection, and disease [34].”
BackgroundmiR-9a Minimizes the Phenotypic Impact of Genomic Diversity by Buffering a Transcription Factor
Cassidy, J. J., Jha, A. R., Posadas, D. M., Giri, R., Venken, K. J. T., Ji, J., Jiang, H., Bellen, H. J., White, K. P., & Carthew, R. W. (2013) · Cell · doi:10.1016/j.cell.2013.10.057 · Cited by 94 · see citing works
Mate choice for genetic quality when environments vary: suggestions for empirical progress
Bussière, L. F., Hunt, J., Stölting, K. N., Jennions, M. D., & Brooks, R. C. (2007) · Genetica · doi:10.1007/s10709-007-9220-z · Cited by 96 · see citing works
“Moreover, environmental heterogeneity may sustain even more genetic variation than our best empirical studies suggest if much of the genetic variation arising from GEI is cryptic, and only observable once specific environmental perturbations arise (Gibson and Dworkin 2004).”
BackgroundDayan, D. I., Crawford, D. L., & Oleksiak, M. F. (2015) · Molecular Ecology · doi:10.1111/mec.13188 · Cited by 96 · see citing works
“Subsequent release of this CGV in an altered genetic or environmental background results in further phenotypic diversification (Gibson & Dworkin 2004) (Le Rouzic & Carlborg 2008) and may enhance reproductive isolation among populations (Pfennig et al. 2010; Fitzpatrick 2012).”
BackgroundDevelopmental capacitance, genetic accommodation, and adaptive evolution
Moczek, A. P. (2007) · Evolution & Development · doi:10.1111/j.1525-142x.2007.00162.x · Cited by 92 · see citing works
“thus altering their ability to contribute to a given population’s response to selection (Gibson and Dworkin 2004).”
BackgroundHsp90 and the quantitative variation of wing shape in Drosophila melanogaster.
Debat, V., Milton, C. C., Rutherford, S., Klingenberg, C. P., & Hoffmann, A. A. (2006) · PubMed · Cited by 95 · see citing works
Beyond Royalactin and a master inducer explanation of phenotypic plasticity in honey bees
Maleszka, R. (2018) · Communications Biology · doi:10.1038/s42003-017-0004-4 · Cited by 94 · see citing works
The Synthesis and Evolution of a Supermodel
Gibson, G. C. (2005) · Science · doi:10.1126/science.1109835 · Cited by 94 · see citing works
Self-citationGenotype-by-Diet Interactions Drive Metabolic Phenotype Variation inDrosophila melanogaster
Reed, L. K., Williams, S., Springston, M., Brown, J., Freeman, K., DESROCHES, C. E., Sokolowski, M. B., & Gibson, G. C. (2010) · Genetics · doi:10.1534/genetics.109.113571 · Cited by 94 · see citing works
“This indicates that the high fat environment exposes cryptic genetic variation for these traits (Gibson and Dworkin 2004; Gibson 2009).”
BackgroundSelf-citationA role for genetic accommodation in evolution?
Braendle, C., & Flatt, T. (2006) · BioEssays · doi:10.1002/bies.20456 · Cited by 90 · see citing works
A history of phenotypic plasticity accelerates adaptation to a new environment
Fierst, J. L. (2011) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2011.02333.x · Cited by 92 · see citing works
“Long-term fluctuations may produce phenotypic and developmental canalization (Meyers et al., 2005), but these populations could also accumulate cryptic genetic variation (Gibson & Dworkin, 2004).”
BackgroundParsons, K. J., Concannon, M. R., Navon, D., Wang, J., Ea, I., Groveas, K., Campbell, C. S., & Albertson, R. C. (2016) · Molecular Ecology · doi:10.1111/mec.13801 · Cited by 92 · see citing works
Milloz, J., Duveau, F., Nuez, I., & Félix, M. (2008) · Genes & Development · doi:10.1101/gad.495308 · Cited by 93 · see citing works
“Microevolutionary studies of cryptic genetic variation have so far been limited by the complexity of the trait used or by the lack of detailed molecular knowledge of the system (Gibson and van Helden 1997; Gibson et al. 1999; Gibson and Dworkin 2004; Zauner and Sommer 2007).”
BackgroundThe unforeseen challenge: from genotype-to-phenotype in cell populations
Braun, E. (2015) · Reports on Progress in Physics · doi:10.1088/0034-4885/78/3/036602 · Cited by 88 · see citing works
Zhan, J., Stefanato, F. L., & McDonald, B. A. (2006) · Molecular Plant Pathology · doi:10.1111/j.1364-3703.2006.00336.x · Cited by 91 · see citing works
“Gibson and Dworkin, 2004 ) in the fungal populations and the magnitude of selection acting on them.”
BackgroundLevis, N. A., & Pfennig, D. W. (2018) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2018.01.012 · Cited by 90 · see citing works
Evolution of Morphological Integration: Developmental Accommodation of Stress-Induced Variation
Badyaev, A. V., Foresman, K. R., & Young, R. L. (2005) · The American Naturalist · doi:10.1086/432559 · Cited by 90 · see citing works
“…(Wagner and Altenberg 1996; Hadany and Beker 2003) or effects of a stressor on organism-wide homeostasis (Bradshaw and Hardwick 1989; Eshel and Matessi 1998; Schlichting and Pigliucci 1998; Gibson and Wagner 2000; Newman and Muller 2000; Nanjundiah 2003; Rutherford 2003; Gibson and Dworkin 2004).”
BackgroundHeterogeneity of Genetic Modifiers Ensures Normal Cardiac Development
Winston, J. B., Erlich, J. M., Green, C. A., Aluko, A., Kaiser, K. A., Takematsu, M., Barlow, R. S., Sureka, A. O., LaPage, M. J., Janss, L., et al. (2010) · Circulation · doi:10.1161/circulationaha.109.887687 · Cited by 86 · see citing works
Soyk, S., Lemmon, Z. H., Sedlazeck, F. J., Jiménez‐Gómez, J. M., Alonge, M., Hutton, S. F., Eck, J. M. V., Schatz, M. C., & Lippman, Z. B. (2019) · Nature Plants · doi:10.1038/s41477-019-0422-z · Cited by 86 · see citing works
Rutherford, S., Hirate, Y., & Swalla, B. J. (2007) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409230701597782 · Cited by 86 · see citing works
“A renewed interest in the importance of cryptic variation in evolution and human health highlights the importance of understanding canalization at the molecular level (Rutherford, 2000; Gibson & Dworkin, 2004).”
BackgroundJohnson, W., Penke, L., & Spinath, F. M. (2011) · European Journal of Personality · doi:10.1002/per.836 · Cited by 86 · see citing works
- Authors
- Gibson, G., & Dworkin, I.
- Affiliations
- North Carolina State University (US)
- Corresponding author
- Gibson, Greg
- Venue
- Nature Reviews Genetics
- Published
- 2004-09
- Volume
- 5
- Issue
- 9
- Pages
- 681-690
- ISSN
- 1471-0056 (ISSN-L)
- 1471-0064
- OpenAlex
- W2079319076
- Cited by
- 546
- References
- 90
- Citations by year
- 2026: 21 · 2025: 15 · 2024: 22 · 2023: 19 · 2022: 14 · 2021: 24 · 2020: 32 · 2019: 30 · 2018: 28 · 2017: 18 · 2016: 40 · 2015: 38 · 2014: 28 · 2013: 36 · 2012: 34
- FWCI
- 2.36
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Genetics (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and phenotypic traits in livestock
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Keywords
- cryptic genetic variation, susceptibility genes, gene perturbation, selective breeding, disease penetrance, adaptive potential
- MeSH terms
- Animals, Drosophila melanogaster, Selection, Genetic, Genetic Variation, Linkage Disequilibrium, Quantitative Trait, Heritable
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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