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Evolution of coastal forests based on a full set of mangrove genomes

Nature Ecology & Evolution volume 6, pages 738–749 (2022)Cite this article

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Abstract

Genomic studies are now poised to explore whole communities of species. The ~70 species of woody plants that anchor the coastal ecosystems of the tropics, collectively referred to as mangroves, are particularly suited to this exploration. In this study, we de novo sequenced the whole genomes of 32 mangroves, which we combined with other sequences of 30 additional species, comprising almost all mangroves globally. These community-wide genomic data will be valuable for ecology, evolution and biodiversity research. While the data revealed 27 independent origins of mangroves, the total phylogeny shows only modest increases in species number, even in coastal areas of active speciation, suggesting that mangrove extinction is common. A possible explanation for common extinction is the frequent sea-level rises and falls (SLRs and SLFs) documented in the geological record. Indeed, near-extinctions of species with extremely small population size (N) often happened during periods of rapid SLR, as revealed by the genome-wide heterozygosity of almost all mangroves. Reduction in N has possibly been further compounded by population fragmentation and the subsequent accumulation of deleterious mutations, thus pushing mangroves even closer to extinction. Crucially, the impact of the next SLR will be exacerbated by human encroachment into these mangrove habitats, potentially altering the ecosystems of tropical coasts irreversibly.

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Fig. 1: Genome-scale phylogeny of mangroves.
Fig. 2: Independent origins of mangrove lineages.
Fig. 3: Demographic histories of four mangrove species.
Fig. 4: Model of population subdivision and inferred histories of the PSMC method using simulated samples.

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Data availability

The sequences of this study have been deposited in National Genomics Data Center (NGDC), China National Center for Bioinformation. The 48 genome assembly sequences have been deposited in the Genome Warehouse (https://ngdc.cncb.ac.cn/gwh) in NGDC, under BioProject ID PRJCA004930. Detailed accession numbers of assemblies are listed in Supplementary Table 1. RNA-seq data from multiple species have been deposited in the Genome Sequence Archive (https://ngdc.cncb.ac.cn/gsa) in NGDC, under accession number CRA004363 with BioProject ID PRJCA005451. The genomic and RNA sequences were also deposited in National Center for Biotechnology Information under BioProject ID PRJNA817364.

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Acknowledgements

We thank P. H. Raven, X. He, W. Wang, Q. Qiu, J. Lu, J. Liu, K. Zeng, T. Tang and K. Huang for insightful comments. We also thank J. W. H. Yong, L. Chen, S. Jian, Y. Zhang, W. Lun Ng, M. Tracy, Y. Chen and S. Li for sample collection and Y. Sun and J. Ruan for technical support. This project was supported by the National Natural Science Foundation of China (grant nos. 31830005 to S. Shi and 31971540 to Z.H.); the National Key Research and Development Plan (grant no. 2017FY100705 to S. Shi); the Guangdong Basic and Applied Basic Research Foundation (grant no. 2019A1515010752 to Z.H.); the Science and Technology Project of Guangzhou (grant no. 202102020483 to Z.H.); and the Innovation Group Project of Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai) (grant no. 311021006 to S. Shi).

Author information

Author notes

  1. These authors contributed equally: Ziwen He, Xiao Feng, Qipian Chen, Liangwei Li.

Authors and Affiliations

  1. State Key Laboratory of Biocontrol, Guangdong Key Lab of Plant Resources, School of Life Sciences, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen University, Guangzhou, China

    Ziwen He, Xiao Feng, Qipian Chen, Sen Li, Zixiao Guo, Jiayan Wang, Min Liu, Shaohua Xu, Shao Shao, Xiaomeng Mao, Wei Xie, Xinfeng Wang, Rufan Zhang, Guohong Li, Weihong Wu, Zheng Zheng, Chung-I Wu & Suhua Shi

  2. BGI-Qingdao, BGI-Shenzhen, Qingdao, China

    Liangwei Li, Kai Han, Chengcheng Shi, Xin Liu & Guangyi Fan

  3. College of Life Sciences, University of Chinese Academy of Sciences, Beijing, China

    Liangwei Li

  4. Hainan Academy of Forestry (Hainan Academy of Mangrove), Haikou, China

    Cairong Zhong

  5. Centre for Tropical Water and Aquatic Ecosystem Research, James Cook University, Townsville, Queensland, Australia

    Norman C. Duke

  6. Harvard University Herbaria, Cambridge, MA, USA

    David E. Boufford

  7. State Key Laboratory of Agricultural Genomics, BGI-Shenzhen, Shenzhen, China

    Guangyi Fan

  8. Department of Biology, University of Missouri–St. Louis, St. Louis, MO, USA

    Robert E. Ricklefs

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Contributions

S. Shi conceived of the study, while Z.H., C.-I.W. and S. Shi designed and conceptualized it. S. Shi, Z.H., X.F., Q.C., S.L., Z.G., M.L., S. Shao, X.M., W.X., X.W., R.Z., G.L., W.W., C.Z. and N.C.D. collected samples. X.F., S.L., M.L., S. Shao, W.W. and Z.Z. performed the experiments. Z.H., X.F., L.L., S.L., K.H., C.S., X.L. and G.F. sequenced and assembled the genomes. Z.H., X.F. and Q.C. performed the data analysis with assistance from S.L., J.W., S.X., S. Shao and W.W. Z.H., C.-I.W., R.E.R and S. Shi made the data interpretation and presentation. Z.H., C.-I.W. and S. Shi wrote the manuscript with input from X.F., Q.C. and Z.G. D.E.B and R.E.R revised the manuscript.

Corresponding author

Correspondence to Suhua Shi.

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The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks Richard Buggs, Abraham Morales-Cruz and Maheshi Dassanayake for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Phylogenetic tree of 61 species of mangroves, 23 mangrove associates, and 64 relatives of mangroves.

The types of sequences used to generate the phylogenetic tree are denoted to the right of the name of each species.

Supplementary information

Supplementary Information

Supplementary Figs. 1–7.

Reporting Summary

Peer Review File

Supplementary Tables

Supplementary Tables 1–14.

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He, Z., Feng, X., Chen, Q. et al. Evolution of coastal forests based on a full set of mangrove genomes. Nat Ecol Evol 6, 738–749 (2022). https://doi.org/10.1038/s41559-022-01744-9

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  • DOI: https://doi.org/10.1038/s41559-022-01744-9

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