Article

Constrained vertebrate evolution by pleiotropic genes

  • Nature Ecology & Evolution 117221730 (2017)
  • doi:10.1038/s41559-017-0318-0
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Abstract

Despite morphological diversification of chordates over 550 million years of evolution, their shared basic anatomical pattern (or ‘bodyplan’) remains conserved by unknown mechanisms. The developmental hourglass model attributes this to phylum-wide conserved, constrained organogenesis stages that pattern the bodyplan (the phylotype hypothesis); however, there has been no quantitative testing of this idea with a phylum-wide comparison of species. Here, based on data from early-to-late embryonic transcriptomes collected from eight chordates, we suggest that the phylotype hypothesis would be better applied to vertebrates than chordates. Furthermore, we found that vertebrates’ conserved mid-embryonic developmental programmes are intensively recruited to other developmental processes, and the degree of the recruitment positively correlates with their evolutionary conservation and essentiality for normal development. Thus, we propose that the intensively recruited genetic system during vertebrates’ organogenesis period imposed constraints on its diversification through pleiotropic constraints, which ultimately led to the common anatomical pattern observed in vertebrates.

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Acknowledgements

The EXPANDE (EXpression Profiling AloNg Development and Evolution) project and N.I. was supported in part by Grants in Aid from the Ministry of Education, Culture, Sports, Science and Technology, Japan (15H05603, 22128003, 24570243, 3902 and 17H06387) and the Platform for Dynamic Approaches to Living System from the Ministry of Education, Culture, Sports, Science and Technology, Japan. T.G.K. was supported in part by KAKENHI 16H04724. The research performed by J.-K.Y. was supported by grants from Academia Sinica and the Ministry of Science and Technology, Taiwan (AS-98-CDA-L06, 102-2311-B-001-011-MY3 and 104-2923-B-001-002-MY3). We thank K. Yamanaka for help collecting the embryos (mouse, chicken, turtle, frog and zebrafish), extracting RNAs and sample preparation using Quartz-Seq for early embryos from mice. We thank C. Tanegashima, K. Itomi, O. Nishimura and S. Kuraku for help constructing libraries, sequencing samples and quality checking some of the RNA-seq data. We thank F. Castellan for critically reading the manuscript. We thank Y. Uchida for providing high-resolution images of zebrafish embryos. We thank G. Renaud and J. Kelso for providing the robust demultiplexing method for analysing the ascidian sequencing data.

Author information

Author notes

  1. Haiyang Hu, Masahiro Uesaka and Song Guo contributed equally to this work.

Affiliations

  1. Key Laboratory of Computational Biology, Chinese Academy of Sciences–Max Planck Society Partner Institute for Computational Biology, Chinese Academy of Sciences, Shanghai, 200031, China

    • Haiyang Hu
    • , Song Guo
    •  & Philipp Khaitovich
  2. School of Life Science and Technology, China Pharmaceutical University, Nanjing, 210009, China

    • Haiyang Hu
  3. Department of Biological Sciences, University of Tokyo, Tokyo, 113-0033, Japan

    • Masahiro Uesaka
    •  & Naoki Irie
  4. Institute for Integrative Neurobiology and Department of Biology, Faculty of Science and Engineering, Konan University, Kobe, Japan

    • Kotaro Shimai
    •  & Takehiro G. Kusakabe
  5. Institute of Cellular and Organismic Biology, Academia Sinica, Taipei, 115, Taiwan

    • Tsai-Ming Lu
    •  & Jr-Kai Yu
  6. China National GeneBank, BGI-Shenzhen, Shenzhen, 518083, China

    • Fang Li
    • , Shiping Liu
    •  & Guojie Zhang
  7. Evolutionary Morphology Laboratory, RIKEN, Kobe, 650-0047, Japan

    • Satoko Fujimoto
    •  & Shigeru Kuratani
  8. Department of Bioinformatics and Systems Biology, School of Science, University of Tokyo, Tokyo, 113-0032, Japan

    • Masato Ishikawa
  9. Bioinformatics Research Unit, Advanced Center for Computing and Communication, RIKEN, Saitama, 351-0198, Japan

    • Yohei Sasagawa
  10. Centre for Social Evolution, Department of Biology, University of Copenhagen, Copenhagen, DK-2200, Denmark

    • Guojie Zhang
  11. Universal Biology Institute, University of Tokyo, Tokyo, 113-0033, Japan

    • Naoki Irie

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Consortia

  1. the EXPANDE Consortium

    Contributions

    N.I., P.K. and S.K. conceived the study. S.F., K.S., T.-M.L., J.-K.Y., T.G.K., Y.S. and N.I. collected the samples. H.H., S.G., S.F., Y.S., T.G.K. and N.I. conducted the experiments needed for RNA-seq. F.L., S.L., G.Z. and H.H. made new gene sets in X. laevis and B. floridae. H.H., S.G., M.U., P.K., M.I. and N.I. analysed the data. N.I., J.-K.Y., M.U., T.G.K. and S.K. edited the paper. N.I. and P.K. supervised the project.

    Competing interests

    The authors declare no competing financial interests.

    Corresponding author

    Correspondence to Naoki Irie.

    Electronic supplementary material

    1. Supplementary Information

      Supplementary Methods, Supplementary Notes, Supplementary Figures 1–13, Supplementary Tables 1–16

    2. Supplementary Data

      FPKM-based normalized gene expression profiles at each developmental stage for each species