Since ancient times, natural pearls have captivated mankind for their rarity, value and beauty. Today, commercial pearl culture is based on implanting a seed nucleus along with mantle tissue from a donor oyster into the gonad of a recipient or host oyster. Due to the complexity of the biological system involved (e.g. pearls are the potential product of two genomes from both donor and host oysters), the genetic determinants underlying pearl quality traits remain poorly understood. Our study is the first to combine experimental grafting with genome-wide SNP genotyping to investigate how genetic and environmental factors influence pearl quality in donor and host black-lipped pearl oysters (Pinctada margaritifera). Pearl quality traits such as quality score, lustre, size, nacre thickness, weight and roundness were evaluated on 1821 pearls originating from 214 hatchery-produced donors and 1033 unrelated host oysters, reared at two distinct pearl farms. Using a custom 65 K SNP array, we successfully assigned the 214 donor oysters to 15 half and full-sib families and estimated genetic parameters. In donor oysters, the heritability for quality score and roundness was low, while lustre and nacre deposition traits were moderately heritable (h2 > 0.20); gene-environment interactions significantly influenced lustre (σGxE = 0.194) but had a negligible impact on other traits. Genome-wide association study on the donor and host genomes revealed six candidate genes associated with pearl quality traits, characterized by patterns of pleiotropy and unique trait-specific variants. Although no interaction between donor and host oysters (σGxH < 0.001) was detected, chitin synthase, a candidate gene known to be involved in nacre formation in mollusks, contains SNPs in association with multiple pearl quality traits in both donor and host oysters. Prediction accuracy was improved using an in silico analysis involving the top-ranked 1 K SNPs based on GWAS rather than using all SNPs for the most heritable trait (lustre), uncovering that a lower density SNP panel can be used for genomic selection. Overall, these findings advance our understanding of the heritability and genetic architecture of pearl quality traits in Pinctada margaritifera, providing valuable insights that can inform and guide future breeding programs.
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