Organization of the body wall in lampreys informs the evolution of the vertebrate paired appendages

Abstract

Vertebrate paired appendages are one of the most important evolutionary novelties in vertebrates. During embryogenesis, the skeletal elements of paired appendages differentiate from the somatic mesoderm, which is a layer of lateral plate mesoderm. However, the presence of the somatic mesoderm in the common ancestor of vertebrates has been controversial. To address this problem, it is necessary but insufficient to understand the developmental process of lateral plate mesoderm formation in lamprey (jawless vertebrates) embryos. Here, I show the presence of the somatic mesoderm in lamprey (Lethenteron camtschaticum) embryos using plastic sectioning and transmission electron microscopy analysis. During the early pharyngeal stages, the somatic mesoderm transforms from the lateral plate mesoderm in the trunk region. Soon after, when the cardiac structures were morphologically distinct, the somatic mesoderm was recognized through the cardiac to more caudal regions. These findings indicated that the somatic mesoderm evolved before the emergence of paired appendages. I also discuss the developmental changes in the body wall organization in the common ancestor of vertebrates, which is likely related to the evolution of the paired appendages.

Paired fins in vertebrate evolution and ontogeny

“…Neither theory has yet been supported by decisive embryological, paleontological, or genetic evidence. At the same time, certain evidence can be found to support each view (Diogo, 2020; Onai, 2023; Sleight & Gillis, 2020; Tulenko et al, 2013).…”

“…In particular, this is indicated by the expression of the somatic marker Irx3 in lampreys (in contrast to gnathostomes) only in the zone of the CM (Onimaru et al, 2011). Recently, however, splitting of the LPM has also been detected in the trunk of lamprey embryos using transmission electron microscopy, although the coelom formed in this case has a very small volume (Onai, 2023). Thus, the question of LPM regionalization in cyclostomes remains controversial.…”

“…This suggests the evolutionary primacy of such a mechanism for the formation of the mesodermal basis of gnathostome paired fins (Okamoto et al, 2017). It is suggested that the appearance of migrating myogenic progenitors may be one of the key prerequisites for the emergence of paired fins (Onai, 2023).…”