Coelacanth genomes reveal signatures for evolutionary transition from water to land

  1. Norihiro Okada1,12,13,15
  1. 1Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama, Kanagawa 226-8501, Japan;
  2. 2National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan;
  3. 3Department of Medical Genome Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa City, Chiba 277-0882, Japan;
  4. 4Tanzania Fisheries Research Institute, Dar es Salaam, Tanzania;
  5. 5Regional Commissioner's Office Tanga, Tanga, Tanzania;
  6. 6Faculty of Fisheries and Marine Sciences, Sam Ratulangi University, Kampus Unsrat Manado 95115, North Sulawesi, Indonesia;
  7. 7Department of Medicine, Sam Ratulangi University, Kampus Unsrat Manado 95115, North Sulawesi, Indonesia;
  8. 8Department of Veterinary Medicine, College of Bioresource Sciences, Nihon University, Fujisawa Kanagawa 252-0880, Japan;
  9. 9Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido 080-8555, Japan;
  10. 10Aquamarine Fukushima, Marine Science Museum, Iwaki, Fukushima 971-8101, Japan;
  11. 11Department of Anatomy, The Jikei University of Medicine, Minato-ku, Tokyo 105-8461, Japan;
  12. 12Department of Life Sciences, National Cheng Kung University, Tainan 701, Taiwan;
  13. 13Nagahama Institute of Bio-Science and Technology, Nagahama, Shiga 526-0829, Japan
    1. 14 These authors contributed equally to this work.

    Abstract

    Coelacanths are known as “living fossils,” as they show remarkable morphological resemblance to the fossil record and belong to the most primitive lineage of living Sarcopterygii (lobe-finned fishes and tetrapods). Coelacanths may be key to elucidating the tempo and mode of evolution from fish to tetrapods. Here, we report the genome sequences of five coelacanths, including four Latimeria chalumnae individuals (three specimens from Tanzania and one from Comoros) and one L. menadoensis individual from Indonesia. These sequences cover two African breeding populations and two known extant coelacanth species. The genome is ∼2.74 Gbp and contains a high proportion (∼60%) of repetitive elements. The genetic diversity among the individuals was extremely low, suggesting a small population size and/or a slow rate of evolution. We found a substantial number of genes that encode olfactory and pheromone receptors with features characteristic of tetrapod receptors for the detection of airborne ligands. We also found that limb enhancers of bmp7 and gli3, both of which are essential for limb formation, are conserved between coelacanth and tetrapods, but not ray-finned fishes. We expect that some tetrapod-like genes may have existed early in the evolution of primitive Sarcopterygii and were later co-opted to adapt to terrestrial environments. These coelacanth genomes will provide a cornerstone for studies to elucidate how ancestral aquatic vertebrates evolved into terrestrial animals.

    Footnotes

    • 15 Corresponding authors

      E-mail nokada{at}bio.titech.ac.jp

      E-mail afujiyam{at}nig.ac.jp

      E-mail ykohara{at}nig.ac.jp

      E-mail ssugano{at}k.u-tokyo.ac.jp

      E-mail takehiko{at}bio.titech.ac.jp

    • [Supplemental material is available for this article.]

    • Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.158105.113.

      Freely available online through the Genome Research Open Access option.

    • Received March 27, 2013.
    • Accepted June 27, 2013.

    This article, published in Genome Research, is available under a Creative Commons License (Attribution-NonCommercial 3.0 Unported), as described at http://creativecommons.org/licenses/by-nc/3.0/.

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