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Zoological Lett. 2016 Apr 14;2:10. doi: 10.1186/s40851-016-0046-3. eCollection 2016.

Comparative morphology and development of extra-ocular muscles in the lamprey and gnathostomes reveal the ancestral state and developmental patterns of the vertebrate head.

Author information

1
Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8572 Japan.
2
Laboratory for Evolutionary Morphology, RIKEN, Kobe, 650-0047 Japan ; Department of Cytology and Histology, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, 2-5-1 Shikata-cho, Okayama, 700-8558 Japan ; Sumitomo Besshi Hospital, 3-1 Oji-cho, Niihama, Ehime 792-8543 Japan.
3
Graduate School of Science and Engineering for Research, University of Toyama, 3190 Gofuku, Toyama, 930-8555 Japan.
4
Department of Cytology and Histology, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, 2-5-1 Shikata-cho, Okayama, 700-8558 Japan ; Center for Medical Science, International University of Health and Welfare, 2600-1 Kitakanemaru, Ohtawara, Tochigi 324-8501 Japan.
5
Laboratory for Evolutionary Morphology, RIKEN, Kobe, 650-0047 Japan.

Abstract

The ancestral configuration of the vertebrate head has long been an intriguing topic in comparative morphology and evolutionary biology. One peculiar component of the vertebrate head is the presence of extra-ocular muscles (EOMs), the developmental mechanism and evolution of which remain to be determined. The head mesoderm of elasmobranchs undergoes local epithelialization into three head cavities, precursors of the EOMs. In contrast, in avians, these muscles appear to develop mainly from the mesenchymal head mesoderm. Importantly, in the basal vertebrate lamprey, the head mesoderm does not show overt head cavities or signs of segmental boundaries, and the development of the EOMs is not well described. Furthermore, the disposition of the lamprey EOMs differs from those the rest of vertebrates, in which the morphological pattern of EOMs is strongly conserved. To better understand the evolution and developmental origins of the vertebrate EOMs, we explored the development of the head mesoderm and EOMs of the lamprey in detail. We found that the disposition of lamprey EOM primordia differed from that in gnathostomes, even during the earliest period of development. We also found that three components of the paraxial head mesoderm could be distinguished genetically (premandibular mesoderm: Gsc+/TbxA-; mandibular mesoderm: Gsc-/TbxA-; hyoid mesoderm: Gsc-/TbxA+), indicating that the genetic mechanisms of EOMs are conserved in all vertebrates. We conclude that the tripartite developmental origin of the EOMs is likely to have been possessed by the latest common ancestor of the vertebrates. This ancestor's EOM developmental pattern was also suggested to have resembled more that of the lamprey, and the gnathostome EOMs' disposition is likely to have been established by a secondary modification that took place in the common ancestor of crown gnathostomes.

KEYWORDS:

Evo-devo; Extra-ocular muscles; Head mesoderm; Head segmentation; Lamprey

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