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Tetraploid oysters hold a significant position in the global oyster industry, particularly as core germplasm resources for the production of triploids. Triploids exhibit desirable characteristics such as reduced gonadal development, larger adult size, and superior flesh quality compared with diploids. However, tetraploids often face challenges of slow growth and chromosomal instability during the breeding process, and the mechanisms underlying the formation of these polyploid characteristics remain unclear. This study aimed to elucidate these mechanisms by constructing a polyploid oyster system and comparing the differences in growth-related phenotypes and gene expression among diploids, triploids, and tetraploids. We identified 1404 differentially expressed genes (DEGs) between diploids and triploids, 1814 DEGs between triploids and tetraploids, and 933 DEGs between diploids and tetraploids. Furthermore, we observed distinct gene expression patterns related to innate immunity response and biomineralization between different ploidy levels. Through trend analysis, we clustered genes with similar expression level changes across different ploidy levels and conducted gene ontology (GO) enrichment analysis on genes with different expression profiles. The results indicated that genes associated with the innate immunity response exhibited significantly upregulated expression with increasing ploidy, while genes related to biomineralization showed higher or lower expression levels in triploid oysters. As biomineralization is closely linked to oyster shell growth, this highlights the crucial role of genes associated with biomineralization in regulating the rapid shell growth observed in triploid oysters. Confronted with environmental challenges, tetraploid oysters may display a stronger innate immune response than diploids and triploids. Our study provides valuable resources for investigating the functional aspects of genes related to polyploid phenotype differences and offers new insights into the molecular mechanisms of existing issues in tetraploid oyster breeding. • Triploid oysters show enhanced calcium transport, regulation, and protein degradation. • Chromosomal duplication affects polyploid oysters' growth and adaptability. • Gene replication exhibits detrimental dosage effects following duplication. [ABSTRACT FROM AUTHOR]