Development of the vertebra and fin skeleton in the lamprey and its implications for the homology of vertebrate vertebrae

• Published in: Developmental dynamics 2024-03, Vol.253 (3), p.283-295
• Main Authors: Kariyayama, Hirofumi, Gogoleva, Natalia, Harada, Keishi, Yokoyama, Hiromasa, Ono, Hiroki, Suzuki, Daichi G., Yamazaki, Yuji, Wada, Hiroshi
• Format: Article
• Language: English
• Subjects: Animals; Body length; Cartilage; Cell differentiation; Elastin; evolution; fin; Homology; lamprey; Lampreys; Mesenchyme; Metamorphosis; Musculoskeletal System; Notochord; sclerotome; Skeleton; Somitogenesis; Spine; Tracing; vertebra; Vertebrae; Vertebrates
• ISSN: 1058-8388; 1097-0177
• DOI: 10.1002/dvdy.657

Background Although vertebrae are the defining character of vertebrates, they are found only in rudimentary form in extant agnathans. In addition, the vertebrae of agnathans possess several unique features, such as elastin‐like molecules as the main matrix component and late (post‐metamorphosis) differentiation of lamprey vertebrae. In this study, by tracing the developmental process of vertebrae in lamprey, we examined the homology of vertebrae between lampreys and gnathostomes. Results We found that the lamprey somite is first subdivided mediolaterally, with myotome cells differentiating medially and non‐myotome cells emerging laterally. Subsequently, collagen‐positive non‐myotome cells surround the myotome. This pattern of somitogenesis is rather similar to that in amphioxi and sheds doubt on the presence of a sclerotome, in terms of mesenchyme cells induced by a signal from the notochord, in lamprey. Further tracing of non‐myotome cell development revealed that fin cartilage develops in ammocoete larvae approximately 35 mm in body length. The development of the fin cartilage occurs much earlier than that of the vertebra whose development proceeds during metamorphosis. Conclusion We propose that the homology of vertebrae between agnathans and gnathostomes should be discussed carefully, because the developmental process of the lamprey vertebra is different from that of gnathostomes. Key Findings Lamprey somite is first subdivided medio‐laterally, and myotome emerge medially. Subsequently, collagen‐positive non‐myotome cells surround the myotome. Fin cartilage develops in ammocoete larvae well before metamorphosis. Vertebra develop in adaxial region during metamorphosis.