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Hagfish and lamprey Hox genes reveal conservation of temporal colinearity in vertebrates

Nature Ecology & Evolution volume 2, pages 859–866 (2018)Cite this article

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Abstract

Hox genes exert fundamental roles for proper regional specification along the main rostro-caudal axis of animal embryos. They are generally expressed in restricted spatial domains according to their position in the cluster (spatial colinearity)—a feature that is conserved across bilaterians. In jawed vertebrates (gnathostomes), the position in the cluster also determines the onset of expression of Hox genes (a feature known as whole-cluster temporal colinearity (WTC)), while in invertebrates this phenomenon is displayed as a subcluster-level temporal colinearity. However, little is known about the expression profile of Hox genes in jawless vertebrates (cyclostomes); therefore, the evolutionary origin of WTC, as seen in gnathostomes, remains a mystery. Here, we show that Hox genes in cyclostomes are expressed according to WTC during development. We investigated the Hox repertoire and Hox gene expression profiles in three different species—a hagfish, a lamprey and a shark—encompassing the two major groups of vertebrates, and found that these are expressed following a whole-cluster, temporally staggered pattern, indicating that WTC has been conserved during the past 500 million years despite drastically different genome evolution and morphological outputs between jawless and jawed vertebrates.

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Fig. 1: Hox cluster evolution in chordates.
Fig. 2: Molecular phylogenetic tree of vertebrate Hox genes.
Fig. 3: Spatial colinearity of hagfish Hox genes in the hindbrain of E. burgeri embryos.
Fig. 4: Developmental expression profiling of Hox genes in chordates.

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Acknowledgements

We thank Y. Oisi and S. Fujimoto for providing preliminary hagfish Hox gene sequences, J. M. Martín-Durán, I. Maeso, M. Irimia and C. Böhmer for fruitful discussions, O. Kakitani for hagfish sampling, K. Shirato for shark sampling, S. Shibuya and K. Yamamoto for maintenance of aquarium tanks, S. Kuraku, K. Itomi, C. Tanegashima, K. Tatsumi and O. Nishimura at the Phyloinformatics Unit, RIKEN Center for Life Science Technologies for RNA-seq data production, J. Huddleston and E. Eichler for providing the code to mask BAC vector sequences from PacBio reads, I. Măndoiu for help using DGE-EM software, and B. Chevreaux for help with the MIRA assembler. This work was supported by the Chinese Academy of Sciences programme XDB13000000 to W.W., a Grant-in-Aid for Scientific Research (A) 15H02416 (Japan Society for the Promotion of Science), a Grant-in-Aid for Scientific Research on Innovative Areas (Research in a Proposed Research Area) 17H06384 (Ministry of Education, Culture, Sports, Science and Technology of Japan) and a Naito Grant for the Promotion of Focused Research (The Naito Foundation) to S.K. A.R.-V. holds a ‘Juan de la Cierva’ postdoctoral contract (Ministerio de Economía y Competitividad of Spain).

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Author notes

  1. Wataru Takagi

    Present address: Physiology Laboratory, Atmosphere Ocean Research Institute, The University of Tokyo, Chiba, Japan

  2. These authors contributed equally: Iori Sato and Fumiaki Sugahara.

Authors and Affiliations

  1. Evolutionary Morphology Laboratory, RIKEN, Kobe, Japan

    Juan Pascual-Anaya, Iori Sato, Fumiaki Sugahara, Shinnosuke Higuchi, Wataru Takagi & Shigeru Kuratani

  2. Evolutionary Morphology Research Team, RIKEN Center for Biosystems Dynamics Research (BDR), Kobe, Japan

    Iori Sato, Shinnosuke Higuchi & Shigeru Kuratani

  3. Division of Biology, Hyogo College of Medicine, Nishinomiya, Japan

    Fumiaki Sugahara

  4. School of Biological Sciences, University of Essex, Colchester, UK

    Jordi Paps

  5. State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China

    Yandong Ren & Wen Wang

  6. University of Chinese Academy of Sciences, Beijing, China

    Yandong Ren

  7. Centro de Investigación Médica Aplicada (CIMA), Área de Terapia Celular, Universidad de Navarra, Pamplona, Spain

    Adrián Ruiz-Villalba

  8. Instituto de Salud Pública de Navarra, IdiSNA, Pamplona, Spain

    Adrián Ruiz-Villalba

  9. Laboratory of Aquatic Zoology, Marine Research Station, Institute of Cellular and Organismic Biology, Academia Sinica, Yilan, Taiwan

    Kinya G. Ota

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Contributions

J.P.-A. conceived the project, designed the experiments and wrote the paper. J.P.-A., F.S., S.H. and W.T. obtained the hagfish embryos. J.P.-A., I.S., F.S., S.H., W.T. and A.R.-V. performed the experiments. K.G.O. built the BAC library. Y.R. and W.W. sequenced and assembled the E. burgeri draft genome. J.P. performed the phylogenetic analyses. All authors analysed and discussed the data. All authors approved the final version of the manuscript.

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Correspondence to Juan Pascual-Anaya.

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Supplementary Table 4

Accession numbers of sequences used for phylogenetic analyses

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Pascual-Anaya, J., Sato, I., Sugahara, F. et al. Hagfish and lamprey Hox genes reveal conservation of temporal colinearity in vertebrates. Nat Ecol Evol 2, 859–866 (2018). https://doi.org/10.1038/s41559-018-0526-2

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