The mystery of missing heritability: Genetic interactions create phantom heritability.
paper
Cited
Public
Unavailable
- Authors
- Zuk, Or; Hechter, Eliana; Sunyaev, Shamil R; Lander, Eric S
- Year
- 2012
- Journal
- Proceedings of the National Academy of Sciences of the United States of America
- PMID
- 22223662
- DOI
- 10.1073/pnas.1119675109
- PMCID
- PMC3268279
Human genetics has been haunted by the mystery of "missing heritability" of common traits. Although studies have discovered >1,200 variants associated with common diseases and traits, these variants typically appear to explain only a minority of the heritability. The proportion of heritability explained by a set of variants is the ratio of (i) the heritability due to these variants (numerator), estimated directly from their observed effects, to (ii) the total heritability (denominator), inferred indirectly from population data. The prevailing view has been that the explanation for missing heritability lies in the numerator--that is, in as-yet undiscovered variants. While many variants surely remain to be found, we show here that a substantial portion of missing heritability could arise from overestimation of the denominator, creating "phantom heritability." Specifically, (i) estimates of total heritability implicitly assume the trait involves no genetic interactions (epistasis) among loci; (ii) this assumption is not justified, because models with interactions are also consistent with observable data; and (iii) under such models, the total heritability may be much smaller and thus the proportion of heritability explained much larger. For example, 80% of the currently missing heritability for Crohn's disease could be due to genetic interactions, if the disease involves interaction among three pathways. In short, missing heritability need not directly correspond to missing variants, because current estimates of total heritability may be significantly inflated by genetic interactions. Finally, we describe a method for estimating heritability from isolated populations that is not inflated by genetic interactions.
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| The overdue promise of short tandem repeat variation for heritability. | Press MO et al. | β | 2014 | β |
| The relationship between diastolic blood pressure and coronary artery calcification is dependent on single nucleotide polymorphisms on chromosome 9p21.3. | Kim DS et al. | β | 2014 | β |
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| An evolutionary perspective on epistasis and the missing heritability. | Hemani G et al. | β | 2013 | β |
| A novel approach to detect cumulative genetic effects and genetic interactions in Crohn's disease. | Wang MH et al. | β | 2013 | β |
| A novel permutation test for case-only analysis identifies epistatic effects on human longevity in the FOXO gene family. | Tan Q et al. | β | 2013 | β |
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| Contribution of an additive locus to genetic variance when inheritance is multi-factorial with implications on interpretation of GWAS. | Gianola D et al. | β | 2013 | β |
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| Dissecting the genetic architecture of frost tolerance in Central European winter wheat. | Zhao Y et al. | β | 2013 | β |
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| Do epistatic modules exist in the genetic control of blood pressure in Dahl rats? A critical perspective. | Rapp JP et al. | β | 2013 | β |
| Dopamine transporter DAT and receptor DRD2 variants affect risk of lethal cocaine abuse: a gene-gene-environment interaction. | Sullivan D et al. | β | 2013 | β |
| DRD4 genotype predicts longevity in mouse and human. | Grady DL et al. | β | 2013 | β |
| Effect of inter- and intragenic epistasis on the heritability of oil content in rapeseed (Brassica napus L.). | WΓΌrschum T et al. | β | 2013 | β |
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| Efficient network-guided multi-locus association mapping with graph cuts. | Azencott CA et al. | β | 2013 | β |
| Efficient two-step testing of gene-gene interactions in genome-wide association studies. | Lewinger JP et al. | β | 2013 | β |
| Epistatic effects on abdominal fat content in chickens: results from a genome-wide SNP-SNP interaction analysis. | Li F et al. | β | 2013 | β |
| eQTL Epistasis - Challenges and Computational Approaches. | Huang Y et al. | β | 2013 | β |
| Estimation and partition of heritability in human populations using whole-genome analysis methods. | Vinkhuyzen AA et al. | β | 2013 | β |
| Evaluating empirical bounds on complex disease genetic architecture. | Agarwala V et al. | β | 2013 | β |
| Evaluation of 41 candidate gene variants for obesity in the EPIC-Potsdam cohort by multi-locus stepwise regression. | KnΓΌppel S et al. | β | 2013 | β |
| Exome sequencing identifies novel rheumatoid arthritis-susceptible variants in the BTNL2. | Mitsunaga S et al. | β | 2013 | β |
| Exploring the genetic architecture of circulating 25-hydroxyvitamin D. | Hiraki LT et al. | β | 2013 | β |
| Finding the sources of missing heritability in a yeast cross. | Bloom JS et al. | β | 2013 | β |
| Fine mapping of 11q13.5 identifies regions associated with prostate cancer and prostate cancer death. | Nurminen R et al. | β | 2013 | β |
| From genetics of inflammatory bowel disease towards mechanistic insights. | Graham DB et al. | β | 2013 | β |
| From systems to structure: bridging networks and mechanism. | Fraser JS et al. | β | 2013 | β |
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| Gene-environment interactions in genome-wide association studies: current approaches and new directions. | Winham SJ et al. | β | 2013 | β |
| Gene-gene-environment interactions between drugs, transporters, receptors, and metabolizing enzymes: Statins, SLCO1B1, and CYP3A4 as an example. | Sadee W | β | 2013 | β |
| Gene-gene interaction between RBMS3 and ZNF516 influences bone mineral density. | Yang TL et al. | β | 2013 | β |
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| Gene-smoking interactions in multiple Rho-GTPase pathway genes in an early-onset coronary artery disease cohort. | Ward-Caviness C et al. | β | 2013 | β |
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| Genetic association studies between SNPs and suicidal behavior: a meta-analytical field synopsis. | Schild AH et al. | β | 2013 | β |
| Genetic control of obesity and gut microbiota composition in response to high-fat, high-sucrose diet in mice. | Parks BW et al. | β | 2013 | β |
| Genetic determinants of mortality. Can findings from genome-wide association studies explain variation in human mortality? | Ganna A et al. | β | 2013 | β |
| Genetic incompatibilities are widespread within species. | Corbett-Detig RB et al. | β | 2013 | β |
| Genetic insights in Alzheimer's disease. | Bettens K et al. | β | 2013 | β |
| Genetic interaction networks: toward an understanding of heritability. | Baryshnikova A et al. | β | 2013 | β |
| Genetic linkage analysis identifies Pas1 as the common locus modulating lung tumorigenesis and acute inflammatory response in mice. | Galvan A et al. | β | 2013 | β |
| Genetic profiling and individualized assessment of fracture risk. | Nguyen TV et al. | β | 2013 | β |
| Genetic risk prediction: individualized variability in susceptibility to toxicants. | Nebert DW et al. | β | 2013 | β |
| Genetics of attention-deficit/hyperactivity disorder: current findings and future directions. | Akutagava-Martins GC et al. | β | 2013 | β |
| Genetic variants and their interactions in disease risk prediction - machine learning and network perspectives. | Okser S et al. | β | 2013 | β |
| Genome-wide association study of chronic periodontitis in a general German population. | Teumer A et al. | β | 2013 | β |
| Genome-wide meta-analysis identifies 11 new loci for anthropometric traits and provides insights into genetic architecture. | Berndt SI et al. | β | 2013 | β |
| Genome-wide SNP and CNV analysis identifies common and low-frequency variants associated with severe early-onset obesity. | Wheeler E et al. | β | 2013 | β |
| Genomic risk models improve prediction of longitudinal lipid levels in children and young adults. | Wineinger NE et al. | β | 2013 | β |
| Genomics in cardiovascular disease. | Roberts R et al. | β | 2013 | β |
| Genotype to phenotype: lessons from model organisms for human genetics. | Lehner B | β | 2013 | β |
| Genotype to phenotype via network analysis. | Carter H et al. | β | 2013 | β |
| Global increases in both common and rare copy number load associated with autism. | Girirajan S et al. | β | 2013 | β |
| Gradient Boosting as a SNP Filter: an Evaluation Using Simulated and Hair Morphology Data. | Lubke G et al. | β | 2013 | β |
| GWIS--model-free, fast and exhaustive search for epistatic interactions in case-control GWAS. | Goudey B et al. | β | 2013 | β |
| H2DB: a heritability database across multiple species by annotating trait-associated genomic loci. | Kaminuma E et al. | β | 2013 | β |
| Height matters-from monogenic disorders to normal variation. | Durand C et al. | β | 2013 | β |
| Highlights of the 2012 Research Workshop: Using nutrigenomics and metabolomics in clinical nutrition research. | Zeisel SH et al. | β | 2013 | β |
| High trans-ethnic replicability of GWAS results implies common causal variants. | Marigorta UM et al. | β | 2013 | β |
| How genome-wide SNP-SNP interactions relate to nasopharyngeal carcinoma susceptibility. | Su WH et al. | β | 2013 | β |
| How meaningful are heritability estimates of liability? | Benchek PH et al. | β | 2013 | β |
| Hunting human disease genes: lessons from the past, challenges for the future. | Brunham LR et al. | β | 2013 | β |
| Identifying multiple causative genes at a single GWAS locus. | Flister MJ et al. | β | 2013 | β |
| Identity-by-descent-based heritability analysis in the Northern Finland Birth Cohort. | Browning SR et al. | β | 2013 | β |
| Identity by descent: variation in meiosis, across genomes, and in populations. | Thompson EA | β | 2013 | β |
| Immune-mediated disease genetics: the shared basis of pathogenesis. | Cotsapas C et al. | β | 2013 | β |
| Improving the accuracy and efficiency of identity-by-descent detection in population data. | Browning BL et al. | β | 2013 | β |
| Improving the accuracy and efficiency of partitioning heritability into the contributions of genomic regions. | Kostem E et al. | β | 2013 | β |
| Individualized genomics and the future of translational medicine. | Muenke M | β | 2013 | β |
| Inference of the genetic architecture underlying BMI and height with the use of 20,240 sibling pairs. | Hemani G et al. | β | 2013 | β |
| Influence of SNPs in nutrient-sensitive candidate genes and gene-diet interactions on blood lipids: the DiOGenes study. | Brahe LK et al. | β | 2013 | β |
| Interaction between retinoid acid receptor-related orphan receptor alpha (RORA) and neuropeptide S receptor 1 (NPSR1) in asthma. | Acevedo N et al. | β | 2013 | β |
| Interpersonal and genetic origins of adult attachment styles: a longitudinal study from infancy to early adulthood. | Fraley RC et al. | β | 2013 | β |
| Introduction to the special section on genomics. | Grigorenko EL et al. | β | 2013 | β |
| Invited commentary: Off-roading with social epidemiology--exploration, causation, translation. | Glymour MM et al. | β | 2013 | β |
| Isolation and high-throughput sequencing of two closely linked epistatic hypertension susceptibility loci with a panel of bicongenic strains. | Pillai R et al. | β | 2013 | β |
| Mapping of immune-mediated disease genes. | RicaΓ±o-Ponce I et al. | β | 2013 | β |
| Molecular genetic aspects of weight regulation. | Hebebrand J et al. | β | 2013 | β |
| Molecular genetic gene-environment studies using candidate genes in schizophrenia: a systematic review. | Modinos G et al. | β | 2013 | β |
| Molecular genetics and subjective well-being. | Rietveld CA et al. | β | 2013 | β |
| Multi-site genetic analysis of diffusion images and voxelwise heritability analysis: a pilot project of the ENIGMA-DTI working group. | Jahanshad N et al. | β | 2013 | β |
| Network analysis of GWAS data. | Leiserson MD et al. | β | 2013 | β |
| Non-heritable genetics of human disease: spotlight on post-zygotic genetic variation acquired during lifetime. | Forsberg LA et al. | β | 2013 | β |
| Novel gene-by-environment interactions: APOB and NPC1L1 variants affect the relationship between dietary and total plasma cholesterol. | Kim DS et al. | β | 2013 | β |
| OGA: an ontological tool of human phenotypes with genetic associations. | Herrera-Galeano JE et al. | β | 2013 | β |
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| Partitioning the heritability of Tourette syndrome and obsessive compulsive disorder reveals differences in genetic architecture. | Davis LK et al. | β | 2013 | β |
| Pathways to neurodegeneration: mechanistic insights from GWAS in Alzheimer's disease, Parkinson's disease, and related disorders. | Ramanan VK et al. | β | 2013 | β |
| Patterns of methylation heritability in a genome-wide analysis of four brain regions. | Quon G et al. | β | 2013 | β |
| Phenotypic impact of genomic structural variation: insights from and for human disease. | Weischenfeldt J et al. | β | 2013 | β |
| Precision phenotyping of biomass accumulation in triticale reveals temporal genetic patterns of regulation. | Busemeyer L et al. | β | 2013 | β |
| Projecting the performance of risk prediction based on polygenic analyses of genome-wide association studies. | Chatterjee N et al. | β | 2013 | β |
| Properties of local interactions and their potential value in complementing genome-wide association studies. | Wei W et al. | β | 2013 | β |
| Protein set analyses: how could this impact the clinic? | Sauer S | β | 2013 | β |
| Republished: Non-heritable genetics of human disease: spotlight on post-zygotic genetic variation acquired during lifetime. | Forsberg LA et al. | β | 2013 | β |
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| Serotonin transporter and receptor genes significantly impact nicotine dependence through genetic interactions in both European American and African American smokers. | Yang Z et al. | β | 2013 | β |
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| The benefits of selecting phenotype-specific variants for applications of mixed models in genomics. | Lippert C et al. | β | 2013 | β |
| The Contribution of the Framingham Heart Study to Gene Identification for Cardiovascular Risk Factors and Coronary Heart Disease. | Ehret GB | β | 2013 | β |
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