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Intraspecific Variation in Mitogenomes of Five Crassostrea Species Provides Insight into Oyster Diversification and Speciation

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Abstract

A large number of Crassostrea oysters are found in Asia-Pacific. While analyses of interspecific variation have helped to establish historical relationships among these species, studies on intraspecific variation are necessary to understand their recent evolutionary history and current forces driving population biology. We resequenced 18 and analyzed 31 mitogenomes of five Crassostrea species from China: Crassostrea gigas, Crassostrea angulata, Crassostrea sikamea, Crassostrea ariakensis, and Crassostrea hongkongensis. Our analysis finds abundant insertions, deletions, and single-nucleotide polymorphisms in all species. Intraspecific variation varies greatly among species with polymorphic sites ranging from 54 to 293 and nucleotide diversity ranging from 0.00106 to 0.00683. In all measurements, C. hongkongensis that has the narrowest geographic distribution exhibits the least sequence diversity; C. ariakensis that has the widest distribution shows the highest diversity, and species with intermediate distribution show intermediate levels of diversity. Low sequence diversity in C. hongkongensis may reflect recent bottlenecks that are probably exacerbated by human transplantation. High diversity in C. ariakensis is likely due to divergence of northern and southern China populations that have been separated without gene flow. The significant differences in mitogenome diversity suggest that the five sister species of Crassostrea have experienced different evolutionary forces since their divergence. The recent divergence of two C. ariakensis populations and the C. gigas/angulata species complex provides evidence for continued diversification and speciation of Crassostrea species along China’s coast, which are shaped by unknown mechanisms in a north–south divide.

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Acknowledgments

We thank the following colleagues for helping with the collection of some samples: Aimin Wang, Lumin Qian, Fei Xu, Guofan Zhang, Na Zhang, Tao Zhang, Akira Komaru, and Joana Cardoso. We also thank Feng Jiang for helping with data analysis. This work was supported by the grants from the National High Technology Research and Development Program (2012AA10A412), Shanghai Universities First-class Disciplines Project of Fisheries, the Bairen program of Chinese Academy of Sciences, the MFG Fund of Chinese Academy of Sciences, Taishan Oversea Scholar Program of Shandong and US NOAA CBO Non-native Oyster Research Program (NA04NMF4570424) and NSFC (40406032).

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Authors and Affiliations

  1. Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University, Ministry of Education, Shanghai, 201306, China

    Jianfeng Ren

  2. Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China

    Jianfeng Ren, Zhanhui Hou, Haiyan Wang, Xiao Liu & Bin Liu

  3. Haskin Shellfish Research Laboratory, Department of Marine and Coastal Sciences, Rutgers University, 6959 Miller Avenue, Port Norris, NJ, 08349, USA

    Haiyan Wang & Ximing Guo

  4. Epigenomics and Computational Biology Lab, Virginia Bioinformatics Institute, Virginia Polytechnic Institute and State University, Blacksburg, VA, 24060, USA

    Ming-an Sun

  5. Center of Systematic Genomics, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, 830011, China

    Bin Liu

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Correspondence to Xiao Liu, Bin Liu or Ximing Guo.

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Authors’ Contributions

JR conducted experiments and data analyses with assistance from MS and ZH. HW performed molecular identification of oysters. XG and XL provided the samples. XG, XL, and BL conceived the study. JR and XG did most of the writing. All authors read and approved the final manuscript.

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Table S2 (sample information), Table S3 (sequence variation) and Figure S1 (alignment) of a selected mitogenome fragment flanking a 7-bp indel that separates C. ariakensis from north and south China. (DOCX 1.07 mb)

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Ren, J., Hou, Z., Wang, H. et al. Intraspecific Variation in Mitogenomes of Five Crassostrea Species Provides Insight into Oyster Diversification and Speciation. Mar Biotechnol 18, 242–254 (2016). https://doi.org/10.1007/s10126-016-9686-8

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