Representation in genetic studies affects inference about genetic architecture

遗传学研究中的代表性会影响对遗传结构的推断。

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Abstract

Knowledge of a trait's "genetic architecture," namely the joint distribution of allele frequencies of causal variants and the direction and magnitude of their effects, is essential to understanding its evolution and underlying biology. Inferences about genetic architecture are based on data collected in heterogeneous ways in cohorts recruited through heterogeneous mechanisms. As a result, cohorts differ in genotype, environment, and trait distributions. For example, the UK Biobank (UKB) was designed for broad population representation, whereas FinnGen drew extensively from clinical registries enriched for diagnosed health conditions. Here, we asked whether representation in genetic studies influences inferences about genetic architectures. Using GWAS data from the UKB, FinnGen, and All of Us (AoU), we find that some summaries of a trait's genetic architecture, such as effective polygenicity, vary little across biobanks. Others, like SNP heritability, are on average lower in one biobank (AoU) than in another (UKB), even when matching samples such that they have similar genetic ancestry compositions. This result aligns with other recent evidence that biobanks enriched for diagnosed health conditions, also sometime characterized by less-standardized phenotyping, have lower heritability than population-based biobanks. We highlight a third case, where a summary of genetic architecture varies considerably but not systematically across traits and biobanks. Such is the case for the mean direction of allelic effects ("sign bias"). For example, 72% of rare minor alleles affecting type 2 diabetes risk are inferred to be risk-increasing based on AoU data, while nearly all (>99%) are inferred to be risk-increasing based on UKB data. We hypothesize that the inferred sign bias is heavily influenced by the skewness of the trait distribution in the study and otherwise largely independent of other study or trait characteristics, including whether the trait is binary or quantitative. We provide strong support for this hypothesis through simulations and data from the three biobanks: the variation in inferred sign bias for rare minor alleles across traits and biobanks is explained remarkably well (82% and 97% of variance explained for trait-associated and for a random set of SNPs, respectively) solely by the trait's skewness in the biobank, with residual biobank-specificity explaining little. Our findings suggest that inferences about the map between genetic and trait variation can depend on study design and participation in genetic studies in surprising ways.

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