Abstract
The ancestral configuration of the vertebrate head has long been an intriguing topic in comparative morphology and evolutionary biology. One peculiar component of the vertebrate head is the presence of extra-ocular muscles (EOMs), the developmental mechanism and evolution of which remain to be determined. The head mesoderm of elasmobranchs undergoes local epithelialization into three head cavities, precursors of the EOMs. In contrast, in avians, these muscles appear to develop mainly from the mesenchymal head mesoderm. Importantly, in the basal vertebrate lamprey, the head mesoderm does not show overt head cavities or signs of segmental boundaries, and the development of the EOMs is not well described. Furthermore, the disposition of the lamprey EOMs differs from those the rest of vertebrates, in which the morphological pattern of EOMs is strongly conserved. To better understand the evolution and developmental origins of the vertebrate EOMs, we explored the development of the head mesoderm and EOMs of the lamprey in detail. We found that the disposition of lamprey EOM primordia differed from that in gnathostomes, even during the earliest period of development. We also found that three components of the paraxial head mesoderm could be distinguished genetically (premandibular mesoderm: Gsc+/TbxA–; mandibular mesoderm: Gsc–/TbxA–; hyoid mesoderm: Gsc–/TbxA+), indicating that the genetic mechanisms of EOMs are conserved in all vertebrates. We conclude that the tripartite developmental origin of the EOMs is likely to have been possessed by the latest common ancestor of the vertebrates. This ancestor’s EOM developmental pattern was also suggested to have resembled more that of the lamprey, and the gnathostome EOMs’ disposition is likely to have been established by a secondary modification that took place in the common ancestor of crown gnathostomes.Electronic supplementary materialThe online version of this article (doi:10.1186/s40851-016-0046-3) contains supplementary material, which is available to authorized users.
Highlights
The morphological nature and ancestral configuration of the vertebrate head are longstanding topics of interest in comparative morphology and evolutionary biology
We found that the developmental pattern of extraocular muscles (EOMs) was conserved in the lamprey, because the muscle originated from three domains along the anteroposterior axis in the dorsal head mesoderm
EOM disposition was different between lampreys and gnathostomes, as soon as EOMs were observed as differentiated muscles. These findings indicate that the developmental mechanisms of EOMs from the three subdivisions of the head mesoderm was already established in the common ancestor of vertebrates, and that diversification of the muscle patterns is due to changes during the later phase of development
Summary
The morphological nature and ancestral configuration of the vertebrate head are longstanding topics of interest in comparative morphology and evolutionary biology. A peculiar component of the vertebrate head is the extraocular muscles (EOMs), which control the visual field by the moving eyes These muscles are derived from the paraxial portion of the head mesoderm, and their development has attracted the attention of morphologists in the context of head mesodermal segmentation. Some researchers believe that these muscles are derived from rostral mesodermal segments of an amphioxus-like ancestor (reviewed in [1,2,3,4]) This idea partially stems from the presence of the epithelialized head mesodermal cysts (head cavities) in the shark embryo [5]; the head mesoderm in elasmobranch embryos typically forms three pairs of head cavities, from anterior to posterior, the premandibular (pc), mandibular (mc), and hyoid cavities (hc). This indicates that possession of these cavities is a shared, derived characteristic for gnathostomes, they tend to disappear in many osteichthyan taxa
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