The interplay between divergence and phenotypic plasticity is critical to our understanding of a species’ adaptive potential under rapid climate changes. We investigated divergence and plasticity in natural populations of the Pacific oyster Crassostrea gigas with a congeneric oyster Crassostrea angulata from southern China used as an outgroup. Genome re-sequencing of 371 oysters revealed unexpected genetic divergence in a small area that coincided with phenotypic divergence in growth, physiology, heat tolerance and gene expression across environmental gradients. These findings suggest that selection and local adaptation are pervasive and, together with limited gene flow, influence population structure. Genes showing sequence differentiation between populations also diverged in transcriptional response to heat stress. Plasticity in gene expression is positively correlated with evolved divergence, indicating that plasticity is adaptive and favoured by organisms under dynamic environments. Divergence in heat tolerance—partly through acetylation-mediated energy depression—implies differentiation in adaptive potential. Trade-offs between growth and survival may play an important role in local adaptation of oysters and other marine invertebrates.
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G.Z. and L.L. are supported by the National Natural Science Foundation of China (31530079 to G.Z. and 31572620 to L.L.). G.Z. is supported by the Strategic Priority Research Program of the ‘Western Pacific Ocean System: Structure, Dynamics and Consequences’ project (XDA 11020305), Blue Life Breakthrough Program of LMBB (MS2018NO02) of Qingdao National Laboratory for Marine Science and Technology, and Modern Agro-industry Technology Research System (CARS-49). X.G. is supported by the ‘Taishan Overseas Scholar Program’ of Shandong and USDA/NJAES project 1004475/NJ32920. We thank J. Yan for suggestions on the experimental design and data analyses, Q. Li, Z. Yu, C. Ke, Z. Zeng, Y. Ning and Y. Bao for sampling collection, and B. Yin and J. Qi for information on marine currents.
The authors declare no competing interests.
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Supplementary Figures and Tables
Mapping statistics for Pacific oyster samples resequenced
SNP statistics in different genomic regions for each Pacific oyster sample
Genes from genomic regions under selection in Bohai and southern Yellow Seas and their FST values
GO enrichment analysis of genes from regions under selection in Bohai and southern Yellow Seas
Annotation of genes from regions under selection in Bohai and southern Yellow Seas
Summary statistics of transcriptome dataset
Genes exhibiting significant transcriptional response at 6 and 24 hr of heat shock in oysters from JZ and QD
Summary statistics of proteome and acetylome datasets
Numbers of proteins and acetyl sites showing differential abundance
Genes exhibiting both significantly differential expression in response to high temperature and differential plasticity at 6 and 24 hr in oysters from JZ and QD
Acetyl sites exhibiting differential plasticity in proteins of major energy metabolic pathways when oysters were exposed to high temperature for 6 and 24 hr
Expression level of proteins corresponding to acetyl sites exhibiting differential plasticity in key energy metabolic pathways
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