Haplotype-resolved genomes provide insights into the origin and function of genome diversity in bivalves

Most bivalve genomes exhibit extensive heterozygosity and diversity, yet the origin and function of these genomic features remain unclear. As an ancient bivalve group, oysters demonstrate high ecological adaptability with diverse genomes, which serve as a good model for studies in genome diversity and evolution. Here, we report the significant contraction but highly divergent genomic landscape of Crassostrea species and highlight the association of transposable elements (TEs) activity with this genomic feature. By constructing a haplotype-resolved genome of C. sikamea, we identified the widespread presence of high divergence sequences (HDS) between the haplotype genome. Combined with population resequencing data, we underscore the role of genome divergence driven by TEs in shaping and maintaining oyster genomic diversity. By comparing haplotype genomes across C. sikamea, Pinctada fucata, Arcuatula senhousia, and Mimachlamys varia, we find that while haplotype divergence is common, its mechanisms of occurrence and maintenance differ significantly among bivalve species. Furthermore, our results show that the widespread presence of HDS not only contributes to substantial genetic variation but also influences the regulation of gene expression in oysters. The lack of conservation in allele-specific expression among individuals in oysters suggests high plasticity in haplotype polymorphism, allowing significant variation in gene regulation to supporting high phenotype plasticity and environment adaption. Overall, these findings offer novel insights into the connection between the unique genomic features and their role in adaptive evolution.