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The estuarine oyster (Crassostrea ariakensis), a species native to Asia, is widespread throughout the estuarine region along the northern and southern coasts of China and has important ecological and economic values. Owing to runoff dropping and environmental threats caused by climate change and anthropogenic influences, the natural resources of C. ariakensis have persistently declined. Therefore, breeding oysters with high adaptability, which requires efficient and accurate genotyping tools, is beneficial to restore the germplasm resources and aquaculture. However, targeted genotyping tools are poorly developed for this species and even in other aquatic species. Previously, we have detected some selective regions and genes associated with temperature and salinity adaptation using selection signature analysis and found that the upstream regulatory regions of the environment-responsive genes exhibited higher differentiation. In this study, we developed a single nucleotide polymorphism (SNP) targeted genotyping tool for C. ariakensis , which includes 30 K SNPs located in previously identified target regions. The target genomic regions were enriched by hybridization capture using double-stranded DNA (dsDNA) biotin-labeled probes, and sequenced with high depth. A total of 24,541 (81.8%) high-quality SNPs were successfully genotyped in 655 samples. Compared to the genotypes obtained from previous genome-wide resequencing, 74.2% of the SNPs had a consistency rate of 1, with an average consistency rate for each sample of 97.8%. Population structure analysis showed three divergent populations (northern, southern, and middle) on the coast of China, consistent with those constructed using SNPs derived from whole-genome resequencing data. Most of the 30 K SNPs were located in the intergenic and regulatory regions, whereas 7% were located in the coding region. These high-quality SNPs were located in 953 genes, including 100 heat-response and 348 high-salinity-responsive genes. Therefore, this panel can be used to evaluate the adaptive divergence between populations, and causative SNPs related to temperature and salinity adaptation in the linkage and association analysis, providing robust support for the molecular breeding of estuarine oyster. To the best of our knowledge, this study proposes the first high-throughput SNP-targeted genotyping tool for studying the genetic basis of environmental adaptation in oyster, and providing insights into the development of targeted SNP genotyping tools for the adaptation study in other aquatic species under climate changes. • We developed a 30 K targeted genotyping tool for Crassostrea. Ariakensis. • 24,541 high-quality SNPs were successfully genotyped in 655 samples. • These high-quality SNPs were located in environment-responsive genes. • 74.2% of the SNPs had a consistency rate of 1 with resequencing. Population structure analysis showed three divergent populations on the coast of China • This study could be used to dissect the genetic basis of environmental adaptation. [ABSTRACT FROM AUTHOR]

Understanding the roles of genetic divergence and phenotypic plasticity in adaptation is central to evolutionary biology and important for assessing adaptive potential of species under climate change. Analysis of a chromosome-level assembly and resequencing of individuals across wide latitude distribution in the estuarine oyster (Crassostrea ariakensis) revealed unexpectedly low genomic diversity and population structures shaped by historical glaciation, geological events and oceanographic forces. Strong selection signals were detected in genes responding to temperature and salinity stress, especially of the expanded solute carrier families, highlighting the importance of gene expansion in environmental adaptation. Genes exhibiting high plasticity showed strong selection in upstream regulatory regions that modulate transcription, indicating selection favoring plasticity. Our findings suggest that genomic variation and population structure in marine bivalves are heavily influenced by climate history and physical forces, and gene expansion and selection may enhance phenotypic plasticity that is critical for the adaptation to rapidly changing environments. Ao Li, He Dai, and Ximing Guo et al. present a high-quality genome from the estuarine oyster, Crassostrea ariakensis. They highlight the climate impact on population divergence, a suite of genes likely important for adaptation to environments of different temperatures and salinities, and provide further insight into the evolution of this species. [ABSTRACT FROM AUTHOR]