Development of the head and trunk mesoderm in the dogfish, Scyliorhinus torazame: II. Comparison of gene expression between the head mesoderm and somites with reference to the origin of the vertebrate head

Abstract

The vertebrate mesoderm differs distinctly between the head and trunk, and the evolutionary origin of the head mesoderm remains enigmatic. Although the presence of somite-like segmentation in the head mesoderm of model animals is generally denied at molecular developmental levels, the appearance of head cavities in elasmobranch embryos has not been explained, and the possibility that they may represent vestigial head somites once present in an amphioxus-like ancestor has not been ruled out entirely. To examine whether the head cavities in the shark embryo exhibit any molecular signatures reminiscent of trunk somites, we isolated several developmentally key genes, including Pax1, Pax3, Pax7, Pax9, Myf5, Sonic hedgehog, and Patched2, which are involved in myogenic and chondrogenic differentiation in somites, and Pitx2, Tbx1, and Engrailed2, which are related to the patterning of the head mesoderm, from an elasmobranch species, Scyliorhinus torazame. Observation of the expression patterns of these genes revealed that most were expressed in patterns that resembled those found in amniote embryos. In addition, the head cavities did not exhibit an overt similarity to somites; that is, the similarity was no greater than that of the unsegmented head mesoderm in other vertebrates. Moreover, the shark head mesoderm showed an amniote-like somatic/visceral distinction according to the expression of Pitx2, Tbx1, and Engrailed2. We conclude that the head cavities do not represent a manifestation of ancestral head somites; rather, they are more likely to represent a derived trait obtained in the lineage of gnathostomes.

The ups and downs of amphioxus biology: a history

“…Such anterior condensations of mesoderm are clearly present in shark embryos (Gilland, 1992;Holland et al, 2008b). The most anterior one extends a ventral process into the mandibular arch that expresses engrailed (Adachi, 2012;Gilland, 1992). However, engrailed is but one gene.…”

The stepwise development of the lamprey visual system and its evolutionary implications

“…). It seems that the oculomotor, abducens and trochlear neurons also develop gradually (Pombal, Rodicio & Anadon, ; see also Fritzsch et al, ), although their differentiation is generally antecedent to that of the extra‐ocular muscles (lamprey – Suzuki et al, ; shark – Adachi et al, ; Kuratani & Horigome ; chick – Chilton & Guthrie, ; Noden & Francis‐West, ; mouse – Cordes, ; Sambasivan et al, ). The development of the extra‐ocular muscles and their nerves starts before the development of the topographic retinotectal projection, i.e.…”

Development of head and trunk mesoderm in the dogfish, Scyliorhinus torazame: I. Embryology and morphology of the head cavities and related structures

“…As the histogenetic modes of coelom formation (schizocoely vs. enterocoely) often vary, even within an array of somitic segments in one animal (e.g., amphioxus;Jefferies 1986;Holland and Holland 1998;Schubert et al 2001;Beaster-Jones et al 2008), or differ in the same region of the mesoderm among different species (mandibular mesodermal region of vertebrates), the types of coelom formation may not reflect directly the ancestral origin or the serial homology of mesodermal segments. The analysis of the segmental nature of the vertebrate head mesoderm will require additional advanced histological and experimental methods of observation, as well as examination at the molecular level, which will be addressed in the sequel to this study (Adachi et al 2012). …”