The origins and functional significance of bivalve genome diversity

Bivalves are famed for exhibiting vast genetic diversity of poorly understood origins and functional significance. Within bivalves, oysters are an ancient group showing remarkable genetic and phenotypic variability alongside extensive adaptability, serving as an ideal system to understand the origins and functional significance of genomic diversity. Here, we reveal the divergent genomic landscape of Crassostrea oysters, characterized by a history of genome size reduction associated with transposable elements (TEs). By constructing a haplotype-resolved genome for Kumamoto oyster C. sikamea, we demonstrate the widespread presence of haplotype divergent sequences (HDS); genomic regions present in just one haplotype. Combined with population resequencing, we define the role of genomic divergence driven by TEs in shaping oyster genetic diversity. Comparisons of haplotype-resolved genomes across four bivalve orders reveal that while extensive HDS is common, its origins may differ markedly. We show that HDS are a hotspot of genetic innovation, harboring rapidly evolving genes of various evolutionary ages, while also strongly influencing gene expression phenotypes. A widespread lack of allele-specific expression shared among oyster individuals indicates that haplotype polymorphism provides a key source of expression variation, promoting phenotypic plasticity and adaptation. These findings advance understanding on the origins of genomic diversity and its role in adaptive evolution.