Abstract

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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Data availability

The whole-genome re-sequencing and transcriptome datasets were deposited in the Sequence Read Archive (SRA) database under the accession number PRJNA394055. The proteome and acetylome data are available via the ProteomeXchange Consortium with the identifier PXD008057.

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Acknowledgements

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.

Author information

Author notes

  1. These authors contributed equally: L. Li, A. Li, K. Song, J. Meng, X. Guo, S. Li.

Affiliations

  1. CAS Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China

    • Li Li
    • , Ao Li
    • , Kai Song
    • , Jie Meng
    • , Chunyan Li
    • , Huayong Que
    • , Fucun Wu
    • , Wei Wang
    • , Haigang Qi
    • , Fei Xu
    • , Rihao Cong
    • , Baoyu Huang
    • , Yingxiang Li
    • , Ting Wang
    • , Xueying Tang
    • , Sheng Liu
    • , Busu Li
    • , Ruihui Shi
    • , Youli Liu
    • , Shoudu Zhang
    • , Linlin Zhang
    •  & Guofan Zhang
  2. Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China

    • Li Li
    • , Kai Song
    • , Jie Meng
    • , Huayong Que
    • , Fucun Wu
    • , Wei Wang
    • , Haigang Qi
    • , Fei Xu
    • , Rihao Cong
    •  & Guofan Zhang
  3. University of Chinese Academy of Sciences, Beijing, China

    • Li Li
    • , Ao Li
    • , Xueying Tang
    • , Sheng Liu
    • , Busu Li
    • , Ruihui Shi
    •  & Youli Liu
  4. Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China

    • Li Li
    • , Baoyu Huang
    •  & Yingxiang Li
  5. Center for Ocean Mega-Science, Chinese Academy of Sciences, Beijing, China

    • Li Li
    • , Kai Song
    • , Jie Meng
    • , Huayong Que
    • , Fucun Wu
    • , Wei Wang
    • , Haigang Qi
    • , Fei Xu
    • , Rihao Cong
    • , Baoyu Huang
    • , Yingxiang Li
    • , Linlin Zhang
    •  & Guofan Zhang
  6. National & Local Joint Engineering Key Laboratory of Ecological Mariculture, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China

    • Li Li
    • , Kai Song
    • , Jie Meng
    • , Huayong Que
    • , Fucun Wu
    • , Wei Wang
    • , Haigang Qi
    • , Fei Xu
    • , Rihao Cong
    • , Linlin Zhang
    •  & Guofan Zhang
  7. Haskin Shellfish Research Laboratory, Department of Marine and Coastal Sciences, Rutgers University, Port Norris, NJ, USA

    • Ximing Guo
  8. BGI Genomics, BGI–Shenzhen, Shenzhen, China

    • Shiming Li
    • , Chi Zhang
    •  & Weiming He
  9. BGI Institute of Applied Agriculture, BGI–Shenzhen, Shenzhen, China

    • Shiming Li
    •  & Shancen Zhao
  10. Department of Marine Sciences, University of Gothenburg, Stromstad, Sweden

    • Pierre De Wit
  11. Jingjie PTM Biolabs, Hangzhou, China

    • Chen Bu
  12. National Marine Environmental Monitoring Center, Dalian, China

    • Hongjun Li

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Contributions

L.L. and G.Z. conceived the study and designed the major scientific objectives. X.G. participated in the final data analysis and interpretation. L.L., W.W., H. Que, F.W., H. Qi, F.X., R.C., B.H., S. Zhang and Y. Li. participated in the collection of wild oysters. L.L., W.W., H. Qi., J.M., S.Z., C.L., T.W. and A.L. participated in oyster breeding for F1 and F2 generations. A.L., X.T., S.Liu, B.L., R.S. and Y. Liu. participated in larval rearing and adult management. J.M., C.L., T.W., X.T. and A.L. conducted DNA extraction and sequencing library preparation. K.S., S.Li, C.Z. and W.H. performed the genome sequencing. K.S., S.Li, C.Z., W.H., S. Zhao and A.L. contributed to the re-sequencing data analysis. A.L. and X.T. participated in the morphological measurements and sample collection for physiological and cellular determinations. A.L. conducted the laboratory experiments for measuring physiological and cellular parameters, as well as data analysis. A.L. conducted messenger RNA extraction for transcriptome and data analysis, and protein extraction for proteome and acetylome analysis. A.L. and C.B. contributed to data analysis of the proteome and acetylome. H.L. collected data on the monthly average SST. L.L., A.L., K.S., X.G., P.D.W., J.M., L.Z. and G.Z. did most of the writing and revision, with input from all authors. All authors approved the manuscript.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Guofan Zhang.

Supplementary Information

  1. Supplementary Information

    Supplementary Figures and Tables

  2. Reporting Summary

  3. Supplementary Table 3

    Mapping statistics for Pacific oyster samples resequenced

  4. Supplementary Table 4

    SNP statistics in different genomic regions for each Pacific oyster sample

  5. Supplementary Table 8

    Genes from genomic regions under selection in Bohai and southern Yellow Seas and their FST values

  6. Supplementary Table 9

    GO enrichment analysis of genes from regions under selection in Bohai and southern Yellow Seas

  7. Supplementary Table 10

    Annotation of genes from regions under selection in Bohai and southern Yellow Seas

  8. Supplementary Table 11

    Summary statistics of transcriptome dataset

  9. Supplementary Table 12

    Genes exhibiting significant transcriptional response at 6 and 24 hr of heat shock in oysters from JZ and QD

  10. Supplementary Table 13

    Summary statistics of proteome and acetylome datasets

  11. Supplementary Table 14

    Numbers of proteins and acetyl sites showing differential abundance

  12. Supplementary Table 16

    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

  13. Supplementary Table 17

    Acetyl sites exhibiting differential plasticity in proteins of major energy metabolic pathways when oysters were exposed to high temperature for 6 and 24 hr

  14. Supplementary Table 18

    Expression level of proteins corresponding to acetyl sites exhibiting differential plasticity in key energy metabolic pathways

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DOI

https://doi.org/10.1038/s41559-018-0668-2