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Regulatory variants in gene expression serve as bridges linking genetic variation and phenotypic plasticity. Environmental conditions typically influence the effects of regulatory variants on phenotypic plasticity; however, such genotype-by-environment interactions (G × E) are poorly understood. This study aimed to investigate the genetic basis of G × E in estuarine oyster (Crassostrea ariakensis), which is an important model animal for studying environmental adaption owing to its high plasticity and large intraspecific divergence. Genome-wide mapping of expression quantitative trait loci (eQTLs) for 23 environmental adaptive genes was performed for 256 estuarine oysters. We identified 1194 eQTL single nucleotide polymorphisms (eSNPs), including 433 cis -eSNPs in four genes and 722 trans -eSNPs in eight genes. The expression variation explanation of cis -eSNPs (9.95%) was significantly higher than that of trans -eSNPs (9.15%). We specifically showed cis- and trans-eSNPs with high linkage disequilibrium (LD) for Traf7 , Slc6a5 , Ggt , and Dap3. For example, we identified a cis -regulatory LD block containing 68 cis -eSNP and a trans -regulatory LD block, including 20 trans -eSNPs in Traf7. A high proportion (85%) of 40 vital eSNPs exhibited significant G × E effects. We identified crossing and nonparallel interactions of G × E, with the tag cis -eSNPs of Baat and Slc6a5 as representatives. Our results indicated that cis -eQTLs are highly conserved. This study provides insights into the understanding of adaptive evolutionary mechanisms and phenotypic response prediction to variable environments, as well as the genetic improvement for superior adaptive traits for genetic resource conservation and aquaculture. • We identified trans and cis regulatory variants and built potential regulatory networks. • Cis -eSNPs had larger contributions to gene expression plasticity and are conserved in different environments. • Trans -eSNPs are more abundant than cis -eSNPs and usually environment-specific. • A large proportion of eSNPs exhibited significant G × E effects. • Crossing and nonparallel G × E patterns were identified. [ABSTRACT FROM AUTHOR]

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]

Oysters are a keystone species in estuaries and intertidal zones and have important economic and ecological significance; however, worldwide, the dominant aquaculture oyster species suffers from mass mortality owing to anthropogenic impacts and rapid climate change. As a possible solution, inter/intraspecies hybridization is a feasible way to breed new germplasms with genetic improvement and high environmental adaptability. Suminoe oysters (Crassostrea ariakensis) are broadly distributed in the estuaries of China and have evolved strong genetic divergence between the northern and southern populations; therefore, they are ideal candidates to explore intraspecies heterosis and the associated molecular mechanisms. In this study, we performed reciprocal hybridization and examined fitness traits in oysters cultured in both northern and southern habitats. Reciprocal hybrids performed better than inbred populations in both environments, indicating heterosis in Suminoe oysters. Hybrids reared in maternal habitats showed faster growth, higher field survival, and greater aerobic metabolism than alternative hybrid oysters under the same conditions. The transcriptional analysis identified modules related to heterosis and maternal effect, while genes responsible for galactose metabolism, glycolysis/gluconeogenesis, and the tricarboxylic acid cycle were enriched and upregulated in hybrids, especially those in maternal environments. Our findings reveal that accelerated aerobic energy metabolism, which may result from mitonuclear coadaptation, underlies the molecular basis of heterosis and maternal effect in the hybridization of Suminoe oysters. Thus, we provide important insights for the aquaculture management of marine species, revealing that selecting appropriate environments (maternal habitats) is critical for heterosis in cross-breeding. • Hybrids from divergent oyster populations showed heterosis in growth and survival. • Hybrids in maternal habitat exhibited better performance indicating maternal effect. • Accelerated aerobic metabolism underlies heterosis and maternal effect in oyster. • Our findings propose better hybridization breeding of hybrids in maternal habitat. [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]