Development of cyclostomes and early evolution of vertebrates
by Shigeru Kuratani | RIKEN Center for Biosystems Dynamics Research
Abstract ID: 42
Event: The 3rd AsiaEvo Conference
Topic: Early evolution of vertebrates from evo-devo and paleontological perspectives
Presenter Name: Shigeru Kuratani

Modern jawless vertebrates, including lampreys and hagfish, belong to a monophyletic group called cyclostomes. This group is closely related to its sister group, gnathostomes. While we previously knew little about the embryonic development of hagfish, we can now observe their embryos using histological and gene expression techniques. One interesting aspect of cyclostome development is that the embryos of lampreys and hagfish resemble each other during the middle stages of development. This similarity allows us to compare the structures of these two animals. At a specific stage of development unique to cyclostomes, the craniofacial region of the embryo consists of anterior and posterior processes adjacent to the median nasaohypophyseal placode, as well as the mandibular arch. For example, the upper lip of the ammocoete (lamprey larva) is derived from the posterior process, like the oro-nasal septum of the hagfish, and also similar to a skeletal element called trabecula cranii in jawed vertebrates. In hagfish, the root of the posterior process undergoes degeneration, connecting the nasohypophyseal duct and the oral cavity. This trait once distinguished hagfishes from lampreys, but this difference only emerges in the later stages of development, confirming their close evolutionary relationship. Primarily, the craniofacial features of cyclostomes include having a single nasohypophyseal duct that does not directly open into the oral cavity, a trait also found in the stem group of jawed vertebrates known as ostracoderms. This suggests that cyclostomes retain an ancient craniofacial developmental program. On the other hand, possessing structures like the lingual apparatus and velum, which derive from the mandibular arch, can possibly be considered defining features of cyclostomes. Among the cyclostomes, hagfishes seem to have undergone more changes in craniofacial morphology compared to lampreys, which show a pattern more similar to the embryonic state of cyclostomes. However, lampreys also display unique traits that may have arisen during their larval stage or metamorphosis. For instance, the position of the lamprey esophagus shifts as they undergo metamorphosis, and their brain development differs from that of hagfishes and jawed vertebrates: larval lamprey brain does not differentiate a rhombic lip (at the morphological level) as in the hagfish and gnathostomes. The appearance of an exocrine organ, endostyle, in lamprey larvae is also puzzling. Although the ammocoete endostyle was regarded to recapitulate an ancestral, pre-vertebrate state of evolution, recent findings suggest that the larval stage of lampreys might have evolved relatively recently (Miyashita et al., 2021), challenging the previously accepted idea that lamprey and protochordate endostyles are homologous. Thus, embryonic development and craniofacial features of cyclostomes provide insights into mechanisms behind morpphological diversity in early evolution of vertebrates.