Comparative morphology and development of extra-ocular muscles in the lamprey and gnathostomes reveal the ancestral state and developmental patterns of the vertebrate head

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.

Neural crest and the patterning of vertebrate craniofacial muscles

“…Smaller epithelial clusters have been described within pre‐otic mesoderm in sturgeon (Kuratani et al, ); chicks (Adelmann, ; Jacob et al, ), and several species of mammals (opossum: Fraser, ; Gilbert, ; cat: Gilbert ; human: Gilbert, ), although whether these are homologous with the large chondrichthian head cavities remains uncertain. While the apparent lack of a consistent correlation between the presence of these vesicles and the sites of EOM and branchial muscle development in many species is confounding, the possibility that they are vestiges of an ancient head mesoderm patterning remains under active investigation (Horder, Presley, & Slipka, ; Suzuki, Fukumoto, et al, ).…”

“…EOMs are among the most conserved of vertebrate muscle groups with respect to innervation and early molecular signatures (reviewed by: Suzuki, Fukumoto, et al, 2016) although considerable evolutionary changes in attachments to orbital skeletal elements have been described (Young, 2008). There are, of course, some specialized adaptations, such as "heater" EOMs in billfish (e.g., swordfish, marlin) that are enlarged and physiologically modified to provide a thermal warming blanket to the brain (Block, 1986;Block & Franzini-Armstrong, 1988).…”

Launch of Zoological Letters

“…In its first two years, comparative morphology and embryology in evolutionary developmental contexts have been major themes of interest (ex. Hirasawa and Kuratani, 2015;Hojo et al, 2015;Tada and Kuratani, 2015;Hayashi et al, 2015;Nakano, 2015;Onai et al, 2015a, b;Oisi et al, 2015;Shigeno et al, 2015;Kaji et al, 2016;Takeuchi et al, 2016;Suzuki et al, 2016;Hirasawa et al, 2016), a clear trend dating to the launch year, as we reported in a previous review (Fukatsu and Kuratani, 2014). Nonetheless, ZL is open to all areas of basic zoology, and many of the top cited and most frequently accessed papers have been from fields other than evo-devo (Holland, 2015;Kishida et al, 2015;Inoue et al, 2015;Mizunami et al, 2015;Hosokawa et al, 2015;Moriyama and Numata, 2015).…”

“…Shone et al (2016) evaluated fossil agnathan morphological traits to speculate about an evolutionary sequence in vertebrate gill number. Suzuki et al (2016) referred to placoderm fossil data (Young, 2008) in suggesting that vertebrate extrinsic eye muscles adhere to ancestral anatomical patterns. As a substantive move in embracing paleontological approaches, ZL has invited Robert Jenkins, a specialist in invertebrate paleontology, to join its editorial board.…”

Local retinoic acid directs emergence of the extraocular muscle functional unit

“…Among the craniofacial muscles, the morphological configuration of the extraocular muscles (EOMs) has been a longstanding challenge in comparative anatomy and evolutionary biology. Besides specialized adaptations, the basic EOM pattern is shared among all vertebrate classes (Noden and Francis-West, 2006;Suzuki et al, 2016;Young, 2008) and includes 4 recti muscles (the superior rectus, the medial rectus, the inferior rectus, and the lateral rectus) and two oblique muscles (superior oblique and inferior oblique) for movement of the eyeball. Most vertebrates have also accessory ocular muscles involved in protecting the cornea (Noden and Francis-West, 2006;Spencer and Porter, 2006): the retractor bulbi, which serves to retract the eye in several groups of vertebrates and the levator palpabrae superioris, which is not directly associated with the eyeball but controls eyelid elevation in mammalian species.…”