Study of lamprey embryos sheds light on evolutionary origin of vertebrate heads

The origin of the vertebrate skull is the subject of much debate among evolutionary biologists. Some believe that the head of vertebrates developed as a result of modification of the segmental elements of the trunk, such as the vertebrae and somites. On the other hand, others believe that the vertebrate head evolved as a new, unsegmented body part, unrelated to other widely observed embryonic segment somites.

Interestingly, previous studies of embryos have revealed the presence of some somite remnants in the head mesoderm (e.g., head cavities and somitomeres). However, the homology between the trunk somites and these head segments has been controversial.

The failure to understand the evolutionary origins of the vertebrate head is also attributable to the lack of studies of extant species such as lampreys, which are known to share several traits with fossil jawless vertebrates and retain primitive traits related to the head mesoderm.

Although some studies have focused on the embryonic morphology of lampreys, they have often failed due to challenges such as tissue destruction and acid fixation during examination, making it difficult to observe mesoderm formation. of the head and somites of the trunk.

However, a research team led by Assistant Professor Takayuki Onai from the University of Fukui, Japan, used advanced techniques such as transmission electron microscopy and serial scanning electron microscopy (SBF-SEM) to understand the development of the head mesoderm. and somites in lamprey embryos.

Researchers also analyzed the morphology and gene expression patterns of cephalochordates and hemichordates (both invertebrates) to understand the origins of somites and head mesoderm from an evolutionary perspective.

This article is published in the journal iScienceand is co-authored by Dr. Noritaka Adachi of Aix-Marseille University, Dr. Hidetoshi Urakubo of the National Institute of Physiological Sciences (NIPS), Dr. Fumiaki Sugahara of Hyogo Medical University, Dr. Toshihiro Aramaki of Osaka University, Dr. Mami Matsumoto of NIPS and Nagoya City University, and Dr. Nobuhiko Ohno of NIPS.

To clarify the presence or absence of somites in the head mesoderm during early stages of diversification, researchers focused on rosettes, which are major somite patterns and important for later vertebrae development. Their first observations of lamprey embryos showed that the tissue closely related to the formation of facial muscles and other elements of the skull, known as head mesoderm, had clusters of cells with characteristics similar to somite rosettes.

To clarify whether these groups of cells were rosettes, they conducted ultrastructural experiments, including SBF-SEM and gene expression analysis. Examination of cell morphology and gene expression revealed that cell clusters were clearly distinct from rosettes. “The cell clusters we observed are likely lamprey-specific features, as they are not recognizable in the head mesoderm of hagfish and shark embryos,” says Dr. Onai.

Furthermore, gene expression analysis also revealed the absence of segmental expression of somitogenesis-related genes, indicating their distinctness from somites. These results indicate that the rosette pattern typically observed in somites is not necessarily the essential or most fundamental feature that defines the process of body segmentation.

Additionally, experiments provide evidence that vertebrate head mesoderm diverged during early phases of vertebrate evolution. Furthermore, a comparison of hemichordate (a basal deuterostome), amphioxus (a basal chordate), and vertebrate embryos revealed that the somites likely originated from the “endomesoderm” tissue of an ancient deuterostome ancestor.

The evolutionary origin of somites has been the central question in zoology for over 150 years, and in this study, Onai et al. revealed the riddle. Concerning the evolutionary mechanism of the emergence of head mesoderm, they discovered that head mesoderm emerged during the segregation of mesodermal genes between the front and rear parts of organisms (rostrocaudal axis).

“Our findings revealed a different evolutionary origin for vertebrate head mesoderm, suggesting that it evolved from remodeling of ancient mesoderm and diversified even before the emergence of jawed vertebrates.” , concludes Dr. Onai.

In summary, the finding that cell clusters present in head mesoderm are morphologically and molecularly distinct from somites favors a new model in which vertebrate head mesoderm diverged early in evolution. This sheds more light on the centuries-old debate over the evolution of the vertebrate head and may help us advance our understanding of our own origins.