Data and theory point to mainly additive genetic variance for complex traits.
paper
Cited
Public
- Authors
- Hill, William G; Goddard, Michael E; Visscher, Peter M
- Year
- 2008
- Journal
- PLoS genetics
- PMID
- 18454194
- DOI
- 10.1371/journal.pgen.1000008
- PMCID
- PMC2265475
The relative proportion of additive and non-additive variation for complex traits is important in evolutionary biology, medicine, and agriculture. We address a long-standing controversy and paradox about the contribution of non-additive genetic variation, namely that knowledge about biological pathways and gene networks imply that epistasis is important. Yet empirical data across a range of traits and species imply that most genetic variance is additive. We evaluate the evidence from empirical studies of genetic variance components and find that additive variance typically accounts for over half, and often close to 100%, of the total genetic variance. We present new theoretical results, based upon the distribution of allele frequencies under neutral and other population genetic models, that show why this is the case even if there are non-additive effects at the level of gene action. We conclude that interactions at the level of genes are not likely to generate much interaction at the level of variance.
Distribution of r MZβ2r DZ for all traits on human twins.Data are from published papers by N.G. Martin and colleagues of the Queensland Institute of Medical Research, Brisbane (www.genepi.edu.au). Across a wide variety of traits the mean difference between the monozygotic twin correlation and twice the dizygotic twin correlation is close to zero, which is consistent with predominantly additive genetic variance and the absence of a large component of variance due to common environmental effects.
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| 20 | Model β Gene Frequency Distributions | Thus , where KβΌln(2N). |
| 21 | Model β Gene Frequency Distributions | Genetic variance components are obtained by integration of expressions for the variance as aβ¦ |
| 22 | Model β Genotypic Values β Single Locus with Arbitrary Dominance | Consider a single biallelic locus with genotypic values for CC, Cc and cc of +a, d and βa,β¦ |
| 23 | Model β Genotypic Values β Single Locus with Arbitrary Dominance | For the uniform distribution of p |
| 24 | Model β Genotypic Values β Single Locus with Arbitrary Dominance | Hence E(V A) = a 2/3 +d 2/15 and E(V D) = 2d 2/15, giving E(VA)/E(VG) = 1β2d 2/(5a 2+3d 2). |
| 25 | Model β Genotypic Values β Single Locus with Arbitrary Dominance | For the βUβ-distribution, assuming N is large, and ignoring terms of O(1/N), the integralsβ¦ |
| 26 | Model β Genotypic Values β Additive Γ Additive Model without Dominance or Interactions Including Dominance | A simple additive Γ additive epistatic model has these genotypic values: |
| 27 | Model β Genotypic Values β Additive Γ Additive Model without Dominance or Interactions Including Dominance | Assuming the frequency of B is p and of C is q, with linkage equilibrium: |
| 28 | Model β Genotypic Values β Additive Γ Additive Model without Dominance or Interactions Including Dominance | Mean = M = 2a[pq+(1βp)(1βq)] |
| 29 | Model β Genotypic Values β Additive Γ Additive Model without Dominance or Interactions Including Dominance | The average effect of substitution of allele B is given by [37] and hence |
| 30 | Model β Genotypic Values β Additive Γ Additive Model without Dominance or Interactions Including Dominance | V A = 2a 2[p(1βp)(1β2q)2+q(1βq)(1β2p)2] = a 2(Hp+Hqβ4HpHq), where H is heterozygosity |
| 31 | Model β Genotypic Values β Additive Γ Additive Model without Dominance or Interactions Including Dominance | The AA epistatic effect is given by (Ξ±Ξ±)BC = ΒΌ d2 M/dpdq = a. |
| 32 | Model β Genotypic Values β Additive Γ Additive Model without Dominance or Interactions Including Dominance | Hence V AA = 4a 2 p(1βp)q(1βq)a 2 = a 2 HpHq and VG = a 2(Hp+Hqβ3HpHq), |
| 33 | Model β Genotypic Values β Additive Γ Additive Model without Dominance or Interactions Including Dominance | Uniform: simple integration gives E(V A) = 2a 2/9, E(V AA) = a 2/9, E(V G) = a 2/3 |
| 34 | Model β Genotypic Values β Additive Γ Additive Model without Dominance or Interactions Including Dominance | βUβ: |
| 35 | Model β Genotypic Values β Additive Γ Additive Model without Dominance or Interactions Including Dominance | Similarly E(V AA) = a 2/(4K). Hence E(V A)/E(V G) = (2β4/K)/(2β3/K) = 1β1/(2Kβ3), which ββ¦ |
| 36 | Model β Genotypic Values β Duplicate Factor Model | A simple epistatic model involving all epistatic components for two loci is the following: |
| 37 | Model β Genotypic Values β Duplicate Factor Model | For an arbitrary number (L) of loci (i), the genotypic value is a except for the multipleβ¦ |
| 38 | Model β Genotypic Values β Duplicate Factor Model | For pi = 0.5 at all loci: V G = a 2[(Β½)2Lβ(ΒΌ)2L], V A = a 2 L(Β½)4Lβ1 and V A/V G =β¦ |
| 39 | Model β Genotypic Values β Duplicate Factor Model | Uniform: |
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| Extensions of BLUP Models for Genomic Prediction in Heterogeneous Populations: Application in a Diverse Switchgrass Sample. | Ramstein GP et al. | β | 2019 | β |
| From R.A. Fisher's 1918 Paper to GWAS a Century Later. | Visscher PM et al. | β | 2019 | β |
| Genetic contribution to waist-to-hip ratio in Mexican children and adolescents based on 12 loci validated in European adults. | Turcotte M et al. | β | 2019 | β |
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| Prediction of Subgenome Additive and Interaction Effects in Allohexaploid Wheat. | Santantonio N et al. | β | 2019 | β |
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| Thinking About the Evolution of Complex Traits in the Era of Genome-Wide Association Studies. | Sella G et al. | β | 2019 | β |
| Use of F2 Bulks in Training Sets for Genomic Prediction of Combining Ability and Hybrid Performance. | Technow F | β | 2019 | β |
| Using tree-based methods for detection of gene-gene interactions in the presence of a polygenic signal: simulation study with application to educational attainment in the Generation Scotland Cohort Study. | Meijsen JJ et al. | β | 2019 | β |
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| Detecting the genomic signal of polygenic adaptation and the role of epistasis in evolution. | CsillΓ©ry K et al. | β | 2018 | β |
| Dominance and epistatic genetic variances for litter size in pigs using genomic models. | Vitezica ZG et al. | β | 2018 | β |
| Eco-evolutionary Feedbacks from Non-target Species Influence Harvest Yield and Sustainability. | Wood ZT et al. | β | 2018 | β |
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| Evaluation of nonadditive effects in yearling weight of tropical beef cattle. | Raidan FSS et al. | β | 2018 | β |
| Gene Co-expression Analysis Indicates Potential Pathways and Regulators of Beef Tenderness in Nellore Cattle. | GonΓ§alves TM et al. | β | 2018 | β |
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| Genome-Based Prediction of Time to Curd Induction in Cauliflower. | Rosen A et al. | β | 2018 | β |
| Genome-wide association scan for heterotic quantitative trait loci in multi-breed and crossbred beef cattle. | Akanno EC et al. | β | 2018 | β |
| Genome-wide scan for commons SNPs affecting bovine leukemia virus infection level in dairy cattle. | Carignano HA et al. | β | 2018 | β |
| Genomic heritability estimates in sweet cherry reveal non-additive genetic variance is relevant for industry-prioritized traits. | Piaskowski J et al. | β | 2018 | β |
| Genomic Model with Correlation Between Additive and Dominance Effects. | Xiang T et al. | β | 2018 | β |
| Genomic relationships reveal significant dominance effects for growth in hybrid Eucalyptus. | Tan B et al. | β | 2018 | β |
| Genomic selection models for directional dominance: an example for litter size in pigs. | Varona L et al. | β | 2018 | β |
| Heritability of body size in the polar bears of Western Hudson Bay. | Malenfant RM et al. | β | 2018 | β |
| How does parental environment influence the potential for adaptation to global change? | Chirgwin E et al. | β | 2018 | β |
| Identifying loci affecting trait variability and detecting interactions in genome-wide association studies. | Young AI et al. | β | 2018 | β |
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| Influence of a growth hormone transgene on the genetic architecture of growth-related traits: A comparative analysis between transgenic and wild-type coho salmon. | Kodama M et al. | β | 2018 | β |
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| Polygenic Risk Scores in Clinical Psychology: Bridging Genomic Risk to Individual Differences. | Bogdan R et al. | β | 2018 | β |
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| Selection on Expected Maximum Haploid Breeding Values Can Increase Genetic Gain in Recurrent Genomic Selection. | MΓΌller D et al. | β | 2018 | β |
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| Signatures of negative selection in the genetic architecture of human complex traits. | Zeng J et al. | β | 2018 | β |
| The genetic architecture of socially-affected traits: a GWAS for direct and indirect genetic effects on survival time in laying hens showing cannibalism. | Brinker T et al. | β | 2018 | β |
| Using structural equation modelling to jointly estimate maternal and fetal effects on birthweight in the UK Biobank. | Warrington NM et al. | β | 2018 | β |
| Weak Epistasis May Drive Adaptation in Recombining Bacteria. | Arnold BJ et al. | β | 2018 | β |
| Whole-genome scan reveals significant non-additive effects for sire conception rate in Holstein cattle. | Nicolini P et al. | β | 2018 | β |
| Accounting for genetic interactions improves modeling of individual quantitative trait phenotypes in yeast. | Forsberg SK et al. | β | 2017 | β |
| A Model of Compound Heterozygous, Loss-of-Function Alleles Is Broadly Consistent with Observations from Complex-Disease GWAS Datasets. | Sanjak JS et al. | β | 2017 | β |
| Combinatorial Methods for Epistasis and Dominance. | Sverdlov S et al. | β | 2017 | β |
| Commentary: Fisher's infinitesimal model: A story for the ages. | Turelli M | β | 2017 | β |
| Concepts, estimation and interpretation of SNP-based heritability. | Yang J et al. | β | 2017 | β |
| "Conversion" of epistatic into additive genetic variance in finite populations and possible impact on long-term selection response. | Hill WG | β | 2017 | β |
| Detecting epistasis with the marginal epistasis test in genetic mapping studies of quantitative traits. | Crawford L et al. | β | 2017 | β |
| Dissection of additive, dominance, and imprinting effects for production and reproduction traits in Holstein cattle. | Jiang J et al. | β | 2017 | β |
| Epistasis Γ environment interactions among Arabidopsis thaliana glucosinolate genes impact complex traits and fitness in the field. | Kerwin RE et al. | β | 2017 | β |
| Epistasis in Neuropsychiatric Disorders. | Webber C | β | 2017 | β |
| Epistasis: Searching for Interacting Genetic Variants Using Crosses. | Ehrenreich IM | β | 2017 | β |
| Epistasis: Searching for Interacting Genetic Variants Using Crosses. | Ehrenreich IM | β | 2017 | β |
| Epistatic interactions between mutations of TACI (<i>TNFRSF13B</i>) and <i>TCF3</i> result in a severe primary immunodeficiency disorder and systemic lupus erythematosus. | Ameratunga R et al. | β | 2017 | β |
| Epistatic Networks Jointly Influence Phenotypes Related to Metabolic Disease and Gene Expression in Diversity Outbred Mice. | Tyler AL et al. | β | 2017 | β |
| Evaluation of non-additive genetic variation in feed-related traits of broiler chickens. | Li Y et al. | β | 2017 | β |
| Exhaustive search for epistatic effects on the human methylome. | Egli T et al. | β | 2017 | β |
| Familial Analysis of Epistatic and Sex-Dependent Association of Genes of the Renin-Angiotensin-Aldosterone System and Blood Pressure. | Scurrah KJ et al. | β | 2017 | β |
| Gene-based interaction analysis shows GABAergic genes interacting with parenting in adolescent depressive symptoms. | Van Assche E et al. | β | 2017 | β |
| Genetic and Environmental Pathways Underlying Personality Traits and Perceived Stress: Concurrent and Longitudinal Twin Studies. | Luo J et al. | β | 2017 | β |
| Genetic Mechanisms Leading to Sex Differences Across Common Diseases and Anthropometric Traits. | Traglia M et al. | β | 2017 | β |
| Genomic estimation of additive and dominance effects and impact of accounting for dominance on accuracy of genomic evaluation in sheep populations. | Moghaddar N et al. | β | 2017 | β |
| Genomics of adaptive divergence with chromosome-scale heterogeneity in crossover rate. | Berner D et al. | β | 2017 | β |
| Heritability Estimation using a Regularized Regression Approach (HERRA): Applicable to continuous, dichotomous or age-at-onset outcome. | Gorfine M et al. | β | 2017 | β |
| Heritable Micro-environmental Variance Covaries with Fitness in an Outbred Population of <i>Drosophila serrata</i>. | Sztepanacz JL et al. | β | 2017 | β |
| How does epistasis influence the response to selection? | Barton NH | β | 2017 | β |
| Imaging Genetics and Genomics in Psychiatry: A Critical Review of Progress and Potential. | Bogdan R et al. | β | 2017 | β |
| Influence of epistasis on response to genomic selection using complete sequence data. | Forneris NS et al. | β | 2017 | β |
| Interactions within the MHC contribute to the genetic architecture of celiac disease. | Goudey B et al. | β | 2017 | β |
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| Omics-based hybrid prediction in maize. | Westhues M et al. | β | 2017 | β |
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| Orthogonal Estimates of Variances for Additive, Dominance, and Epistatic Effects in Populations. | Vitezica ZG et al. | β | 2017 | β |
| Polygenicity and Epistasis Underlie Fitness-Proximal Traits in the <i>Caenorhabditis elegans</i> Multiparental Experimental Evolution (CeMEE) Panel. | Noble LM et al. | β | 2017 | β |
| Potential of gene drives with genome editing to increase genetic gain in livestock breeding programs. | Gonen S et al. | β | 2017 | β |
| Strong epistatic and additive effects of linked candidate SNPs for Drosophila pigmentation have implications for analysis of genome-wide association studies results. | Gibert JM et al. | β | 2017 | β |
| The Evolutionary Consequences of Stepwise Infection Processes. | Hall MD et al. | β | 2017 | β |
| The Genetic Architecture of Gene Expression in Peripheral Blood. | Lloyd-Jones LR et al. | β | 2017 | β |
| The impact of parental investment on lifetime reproductive success in Iceland. | Lynch RF et al. | β | 2017 | β |
| The other 96%: Can neglected sources of fitness variation offer new insights into adaptation to global change? | Chirgwin E et al. | β | 2017 | β |
| The potential of shifting recombination hotspots to increase genetic gain in livestock breeding. | Gonen S et al. | β | 2017 | β |
| The quantitative genetic basis of clinal divergence in phenotypic plasticity. | van Heerwaarden B et al. | β | 2017 | β |
| Translating natural genetic variation to gene expression in a computational model of the Drosophila gap gene regulatory network. | Gursky VV et al. | β | 2017 | β |
| Acclimatization and Adaptive Capacity of Marine Species in a Changing Ocean. | Foo SA et al. | β | 2016 | β |
| Advantages of continuous genotype values over genotype classes for GWAS in higher polyploids: a comparative study in hexaploid chrysanthemum. | Grandke F et al. | β | 2016 | β |
| Analysis of Heritability Using Genome-Wide Data. | Hall JB et al. | β | 2016 | β |
| A perspective on interaction effects in genetic association studies. | Aschard H | β | 2016 | β |
| Assessing the effects of 35 European-derived BMI-associated SNPs in Mexican children. | Abadi A et al. | β | 2016 | β |
| Capturing neutral and adaptive genetic diversity for conservation in a highly structured tree species. | RodrΓguez-QuilΓ³n I et al. | β | 2016 | β |
| Cryptic Genetic Variation in Evolutionary Developmental Genetics. | Paaby AB et al. | β | 2016 | β |
| Differential contribution of genomic regions to marked genetic variation and prediction of quantitative traits in broiler chickens. | Abdollahi-Arpanahi R et al. | β | 2016 | β |
| Environmental Correlation Analysis for Genes Associated with Protection against Malaria. | Mackinnon MJ et al. | β | 2016 | β |
| Epistasis and covariance: how gene interaction translates into genomic relationship. | Martini JW et al. | β | 2016 | β |
| Epistasis-Induced Evolutionary Plateaus in Selection Responses. | Le Rouzic A et al. | β | 2016 | β |
| Genetic Risk Scores. | Cooke Bailey JN et al. | β | 2016 | β |
| Genetics of murine craniofacial morphology: diallel analysis of the eight founders of the Collaborative Cross. | Percival CJ et al. | β | 2016 | β |
| Genomic BLUP including additive and dominant variation in purebreds and F1 crossbreds, with an application in pigs. | Vitezica ZG et al. | β | 2016 | β |
| Genomic prediction of growth in pigs based on a model including additive and dominance effects. | Lopes MS et al. | β | 2016 | β |
| Genotypic Context and Epistasis in Individuals and Populations. | Sackton TB et al. | β | 2016 | β |
| Heritability of major depressive and comorbid anxiety disorders in multi-generational families at high risk for depression. | Guffanti G et al. | β | 2016 | β |
| Impact of fitting dominance and additive effects on accuracy of genomic prediction of breeding values in layers. | Heidaritabar M et al. | β | 2016 | β |
| Implementation of the Realized Genomic Relationship Matrix to Open-Pollinated White Spruce Family Testing for Disentangling Additive from Nonadditive Genetic Effects. | Gamal El-Dien O et al. | β | 2016 | β |
| Incorporating parent-of-origin effects in whole-genome prediction of complex traits. | Hu Y et al. | β | 2016 | β |
| Marker-Based Estimates Reveal Significant Nonadditive Effects in Clonally Propagated Cassava (<i>Manihot esculenta</i>): Implications for the Prediction of Total Genetic Value and the Selection of Varieties. | Wolfe MD et al. | β | 2016 | β |
| Parents face quantity-quality trade-offs between reproduction and investment in offspring in Iceland. | Lynch RF | β | 2016 | β |
| PEPIS: A Pipeline for Estimating Epistatic Effects in Quantitative Trait Locus Mapping and Genome-Wide Association Studies. | Zhang W et al. | β | 2016 | β |
| POEM: Identifying Joint Additive Effects on Regulatory Circuits. | Botzman M et al. | β | 2016 | β |
| Reflections on the Field of Human Genetics: A Call for Increased Disease Genetics Theory. | Schrodi SJ | β | 2016 | β |
| Summaries of plenary, symposia, and oral sessions at the XXII World Congress of Psychiatric Genetics, Copenhagen, Denmark, 12-16 October 2014. | Aas M et al. | β | 2016 | β |
| Survival of the Curviest: Noise-Driven Selection for Synergistic Epistasis. | Wilkins JF et al. | β | 2016 | β |
| The effect of gene interactions on the long-term response to selection. | PaixΓ£o T et al. | β | 2016 | β |
| The Genetic Architecture of Quantitative Traits Cannot Be Inferred from Variance Component Analysis. | Huang W et al. | β | 2016 | β |
| Uncovering the Genetic Architectures of Quantitative Traits. | Lee JJ et al. | β | 2016 | β |
| What is the biological reality of gene-environment interaction estimates? An assessment of bias in developmental models. | Moore SR et al. | β | 2016 | β |
| Within- and across-breed genomic prediction using whole-genome sequence and single nucleotide polymorphism panels. | Iheshiulor OO et al. | β | 2016 | β |
| Accounting for genetic architecture improves sequence based genomic prediction for a Drosophila fitness trait. | Ober U et al. | β | 2015 | β |
| A comparison of genomic selection models across time in interior spruce (Picea engelmannii Γ glauca) using unordered SNP imputation methods. | Ratcliffe B et al. | β | 2015 | β |
| A Genome-Wide Association Analysis Reveals Epistatic Cancellation of Additive Genetic Variance for Root Length in Arabidopsis thaliana. | Lachowiec J et al. | β | 2015 | β |
| A meta-analysis of heritability of cognitive aging: minding the "missing heritability" gap. | Reynolds CA et al. | β | 2015 | β |
| Contemporary Considerations for Constructing a Genetic Risk Score: An Empirical Approach. | Goldstein BA et al. | β | 2015 | β |
| Dearth of polymorphism associated with a sustained response to selection for flowering time in maize. | Durand E et al. | β | 2015 | β |
| Determination of nonlinear genetic architecture using compressed sensing. | Ho CM et al. | β | 2015 | β |
| Dominance genetic variance for traits under directional selection in Drosophila serrata. | Sztepanacz JL et al. | β | 2015 | β |
| Dominance genetic variation contributes little to the missing heritability for human complex traits. | Zhu Z et al. | β | 2015 | β |
| Epidemiology and Heritability of Major Depressive Disorder, Stratified by Age of Onset, Sex, and Illness Course in Generation Scotland: Scottish Family Health Study (GS:SFHS). | Fernandez-Pujals AM et al. | β | 2015 | β |
| Epistasis for quantitative traits in Drosophila. | Mackay TF | β | 2015 | β |
| Epistasis Is a Major Determinant of the Additive Genetic Variance in Mimulus guttatus. | Monnahan PJ et al. | β | 2015 | β |
| Estimation of Additive, Dominance, and Imprinting Genetic Variance Using Genomic Data. | Lopes MS et al. | β | 2015 | β |
| Evolutionary behavioral genetics. | Zietsch BP et al. | β | 2015 | β |
| Evolutionary genetic bases of longevity and senescence. | Govindaraju DR | β | 2015 | β |
| Expected influence of linkage disequilibrium on genetic variance caused by dominance and epistasis on quantitative traits. | Hill WG et al. | β | 2015 | β |
| Genes and quantitative genetic variation involved with senescence in cells, organs, and the whole plant. | Pujol B | β | 2015 | β |
| Genetic and environmental etiologies of the longitudinal relations between prereading skills and reading. | Christopher ME et al. | β | 2015 | β |
| Genetic architecture of natural variation in Drosophila melanogaster aggressive behavior. | Shorter J et al. | β | 2015 | β |
| Genetic basis of transcriptome diversity in Drosophila melanogaster. | Huang W et al. | β | 2015 | β |
| Genetic interactions contribute less than additive effects to quantitative trait variation in yeast. | Bloom JS et al. | β | 2015 | β |
| Genome-Enabled Estimates of Additive and Nonadditive Genetic Variances and Prediction of Apple Phenotypes Across Environments. | Kumar S et al. | β | 2015 | β |
| Genomic risk prediction of complex human disease and its clinical application. | Abraham G et al. | β | 2015 | β |
| Heritability of heterozygosity offers a new way of understanding why dominant gene action contributes to additive genetic variance. | Nietlisbach P et al. | β | 2015 | β |
| Identification of additive, dominant, and epistatic variation conferred by key genes in cellulose biosynthesis pathway in Populus tomentosaβ . | Du Q et al. | β | 2015 | β |
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