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Constrained vertebrate evolution by pleiotropic genes

Nature Ecology & Evolution volume 1, pages 1722–1730 (2017)Cite this article

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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.

Over the past 550 million years, the basic anatomical features (or ‘bodyplan’) of animals at the phylum level have been conserved1,2. However, potential mechanisms underlying this conservation on the macro-evolutionary time scale remain poorly understood2,3,4,5,6. In this regard, the phylotype hypothesis7,8,9 of the developmental hourglass model7,9 provides an attractive framework for analysing this problem because it predicts that the bodyplan for each animal phylum can be defined by anatomical features observed during a mid-embryonic phase (the phylotypic period) that are conserved among species across a phylum (a process also known as phylotypic progression7,8,9,10). The model further predicts that the conservation of this phylotype arises from gene regulatory networks that are vulnerable to changes in molecular developmental signalling7,9. These ideas inspired scientists to test the hourglass model from a molecular perspective5,11,12,13,14,15,16,17,18,19,20 and these efforts have provided support for hourglass-like, mid-embryonic conservation during development not only in animals (for example, vertebrates11,12,13,15,18, Drosophila species14, molluscs20 and nematodes17), but also in plants (Arabidopsis thaliana 16) and fungi (Coprinopsis cinerea 19). A recent study showed that hourglass-like conservation was consistently not observed among ten species from different animal phyla and concluded that the phylotype hypothesis should be applied to species within the same phylum21. However, whether or not the phylotype hypothesis can be applied to animals at the phylum level still remains to be verified4,22 as no studies have made phylum-wide comparisons of species to confirm that the most transcriptomically conserved mid-embryonic period actually accounts for phylotype or bodyplan-defining stages. For the phylum Chordata, it is known that ascidians do not have developmental stages that match the phylotypic period (as there is no developmental stage that shows chordate bodyplan elements simultaneously)23,24 and the phylotype hypothesis may be applied only to the subphylum Vertebrata7. Nevertheless, the phylotypic period is still possibly a bodyplan-defining phase that once existed in a common ancestor of the phylum Chordata, and the period was modified secondarily during ascidian evolution25, but remained the most conserved mid-embryonic phase in other species. In this study, we asked whether this phylotype hypothesis stands for phylum Chordata by analysing the gene expression profiles of chordates. In addition, since no consensus has been reached regarding the potential mechanisms that caused animals to follow hourglass-like conservation3,4,6, we further sought to elucidate these by analysing the expression dataset.

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Fig. 1: Basic strategy for evaluating evolutionarily conserved developmental stages.
Fig. 2: Conserved embryonic stages identified by gene expression similarity.
Fig. 3: Regulatory quiescence and highly pleiotropic genes enriched in the mid-embryonic period.
Fig. 4: Temporally pleiotropic genes tend to be evolutionarily conserved and essential for normal development.

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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.

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Author notes

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

Authors and 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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  1. Haiyang Hu
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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.

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Correspondence to Naoki Irie.

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Supplementary Information

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

Supplementary Data

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

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Hu, H., Uesaka, M., Guo, S. et al. Constrained vertebrate evolution by pleiotropic genes. Nat Ecol Evol 1, 1722–1730 (2017). https://doi.org/10.1038/s41559-017-0318-0

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