Ultrastructure of the lamprey head mesoderm reveals evolution of the vertebrate head
Takayuki Onai,
Noritaka Adachi,
Hidetoshi Urakubo,
Fumiaki Sugahara,
Toshihiro Aramaki,
Mami Matsumoto,
Nobuhiko Ohno
Affiliations
Takayuki Onai
Department of Anatomy, University of Fukui, School of Medical Sciences, 23-3, Matsuokashimoaizuki, Eiheiji, Yoshida, Fukui, Japan; Life Science Innovation Center, University of Fukui, 23-3, Matsuokashimoaizuki, Eiheiji, Yoshida, Fukui, Japan; Corresponding author
Noritaka Adachi
Aix-Marseille Université, IBDM, CNRS UMR 7288, Campus De Luminy Case 907, 13288 Marseille Cedex 9, France
Hidetoshi Urakubo
Section of Electron Microscopy, National Institute for Physiological Sciences, 38, Nishigonaka, Myodaiji, Okazaki, Aichi, Japan
Fumiaki Sugahara
Division of Biology, Hyogo Medical University, 1-1, Mukogawa, Nishinomiya, Hyogo, Japan
Toshihiro Aramaki
Graduate School of Frontier Biosciences, Osaka University, 1-1, Yamadaoka, Suita, Osaka, Japan
Mami Matsumoto
Section of Electron Microscopy, Supportive Center for Brain Research, National Institute for Physiological Sciences, 38, Nishigonaka, Myodaiji, Okazaki, Aichi, Japan; Department of Developmental and Regenerative Biology, Nagoya City University Graduate School of Medical Sciences, 1, Kawasumi, Mizuho, Nagoya, Aichi, Japan
Nobuhiko Ohno
Department of Anatomy, Division of Histology and Cell Biology, School of Medicine, Jichi Medical University, 3311-1, Yakushiji, Shimotsuke, Tochigi, Japan; Division of Ultrastructural Research, National Institute for Physiological Sciences, 38, Nishigonaka, Myodaiji, Okazaki, Aichi, Japan
Summary: The cranial muscle is a critical component in the vertebrate head for a predatory lifestyle. However, its evolutionary origin and possible segmental nature during embryogenesis have been controversial. In jawed vertebrates, the presence of pre-otic segments similar to trunk somites has been claimed based on developmental observations. However, evaluating such arguments has been hampered by the paucity of research on jawless vertebrates. Here, we discovered different cellular arrangements in the head mesoderm in lamprey embryos (Lethenteron camtschaticum) using serial block-face scanning electron and laser scanning microscopies. These cell populations were morphologically and molecularly different from somites. Furthermore, genetic comparison among deuterostomes revealed that mesodermal gene expression domains were segregated antero-posteriorly in vertebrates, whereas such segregation was not recognized in invertebrate deuterostome embryos. These findings indicate that the vertebrate head mesoderm evolved from the anteroposterior repatterning of an ancient mesoderm and developmentally diversified before the split of jawless and jawed vertebrates.
