Haplotype-resolved genomes provide insights into the origins and functional significance of genome diversity in bivalves.

Bivalves are famed for exhibiting vast genetic diversity of poorly understood origins and functional significance. Through comparative genomics, we demonstrate that high genetic diversity in these invertebrates is not directly linked to genome size. Using oysters as a representative clade, we show that despite genome size reduction during evolution, these bivalves maintain remarkable genetic variability. By constructing a haplotype-resolved genome for Crassostrea sikamea, we identify widespread haplotype divergent sequences (HDSs), representing genomic regions unique to each haplotype. We show that HDSs are driven by transposable elements, playing a key role in creating and maintaining genetic diversity during oyster evolution. Comparisons of haplotype-resolved genomes across four bivalve orders uncover diverse HDS origins, highlighting a role in genetic innovation and expression regulation across broad timescales. Further analyses show that, in oysters, haplotype polymorphisms drive gene expression variation, which is likely to promote phenotypic plasticity and adaptation. These findings advance our understanding of the relationships among genome structure, diversity, and adaptability in a highly successful invertebrate group.