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Palaeospondylus as a primitive hagfish

View Article: PubMed Central - PubMed

ABSTRACT

Background: The taxonomic position of the Middle Devonian fish-like animal Palaeospondylus has remained enigmatic, due mainly to the inability to identify homologous cranial elements. This animal has been classified into nearly all of the major vertebrate taxa over a century of heuristic taxonomic research, despite the lack of conclusive morphological evidence.

Results: Here we report the first comparative morphological analysis of hagfish embryos and Palaeospondylus, and a hitherto overlooked resemblance in the chondrocranial elements of these animals; i.e., congruence in the arrangement of the nasal capsule, neurocranium and mandibular arch-derived velar bar. The large ventral skeletal complex of Palaeospondylus is identified as a cyclostome-specific lingual apparatus. Importantly, the overall morphological pattern of the Palaeospondylus cranium coincides well with the cyclostome pattern of craniofacial development, which is not shared with that of crown gnathostomes. Previously, the presence of the vertebral column in Palaeospondylus made its assignment problematic, but the recent identification of this vertebral element in hagfish is consistent with an affinity between this group and Palaeospondylus.

Conclusion: These lines of evidence support the hagfish affinity of Palaeospondylus. Moreover, based on the less specialized features in its cranial morphology, we conclude that Palaeospondylus is likely a stem hagfish.

Electronic supplementary material: The online version of this article (doi:10.1186/s40851-016-0057-0) contains supplementary material, which is available to authorized users.

No MeSH data available.


Cranial skeletons of the Eptatretus embryo. aEptatretus burgeri embryo at stage 53 in dorsal view. bE. burgeri embryo at stage 53 in ventral view. cE. burgeri embryo at stage 60 in dorsal view. dE. burgeri embryo at stage 60 in left lateral view. e Relative growth of the developing hagfish chondrocrania. From top to bottom, stage 53, stage 60, prehatching and adult hagfish crania. Note, due to the rostral growth of the snout by addition of nasal duct cartilage and extension of subnasal cartilage (green), that the position of the nasal capsule (red) shifts relatively caudal through development. The palatine bar, or the transverse commissure on the rostral tip of the dorsal longitudinal bar, is colored blue for the reference. avnb, anterior vertical nasal bar; com1, 2, commissures of dlb; cornc, cornual cartilage; dlb, dorsal longitudinal bar; dp, dental plate; hypcom, hypophyseal commissure; lp, lingual plate; nc, nasal capsule; nd, nasal duct cartilage; nt, notochord; otc, otic capsule; palb, palatine bar; pch, parachordal; pvnb, posterior vertical nasal bar; rp, rostral plate; snc, subnasal cartilage; t1-3, cartilaginous support for tentacles; trh, trabecula of hagfish; vb, velar bar
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Fig2: Cranial skeletons of the Eptatretus embryo. aEptatretus burgeri embryo at stage 53 in dorsal view. bE. burgeri embryo at stage 53 in ventral view. cE. burgeri embryo at stage 60 in dorsal view. dE. burgeri embryo at stage 60 in left lateral view. e Relative growth of the developing hagfish chondrocrania. From top to bottom, stage 53, stage 60, prehatching and adult hagfish crania. Note, due to the rostral growth of the snout by addition of nasal duct cartilage and extension of subnasal cartilage (green), that the position of the nasal capsule (red) shifts relatively caudal through development. The palatine bar, or the transverse commissure on the rostral tip of the dorsal longitudinal bar, is colored blue for the reference. avnb, anterior vertical nasal bar; com1, 2, commissures of dlb; cornc, cornual cartilage; dlb, dorsal longitudinal bar; dp, dental plate; hypcom, hypophyseal commissure; lp, lingual plate; nc, nasal capsule; nd, nasal duct cartilage; nt, notochord; otc, otic capsule; palb, palatine bar; pch, parachordal; pvnb, posterior vertical nasal bar; rp, rostral plate; snc, subnasal cartilage; t1-3, cartilaginous support for tentacles; trh, trabecula of hagfish; vb, velar bar

Mentions: In E. burgeri embryos at stages 53–60 (Fig. 2a–d), the neurocranium consists of two pairs of longitudinal bars with transverse commissures and processes, rostrally attached to the nasal capsule. Caudally, the longitudinal bars are contiguous to the otic capsule, which continues medially to the parachordal that surrounds the rostral part of the notochord (Fig. 2a, b). From the boundary between the neurocranium and otic capsule, a pair of velar bars grows ventromedially, and later, by stage 53, becoming fused at the median plane to form a V-shaped element. The dental plate of the oral apparatus is located below the neurocranium, associated with the rostral part of the lingual plate that supports the muscles of the cyclostome ‘tongue’ [22]. The topographical relationships between these cranial elements in hagfish embryos continue to change over the course of development [23]. Prior to hatching, the nasal capsule grows cartilages supporting the rostrally extended nasal duct (Fig. 2e). Simultaneously, cartilages in the oronasal septum extend rostrally, and supporting cartilages arise within tentacles, features that are specific to adult individuals in all known hagfish species. These changes result in a caudad shift in the relative position of the nasal capsule in the cranium.Fig. 2


Palaeospondylus as a primitive hagfish
Cranial skeletons of the Eptatretus embryo. aEptatretus burgeri embryo at stage 53 in dorsal view. bE. burgeri embryo at stage 53 in ventral view. cE. burgeri embryo at stage 60 in dorsal view. dE. burgeri embryo at stage 60 in left lateral view. e Relative growth of the developing hagfish chondrocrania. From top to bottom, stage 53, stage 60, prehatching and adult hagfish crania. Note, due to the rostral growth of the snout by addition of nasal duct cartilage and extension of subnasal cartilage (green), that the position of the nasal capsule (red) shifts relatively caudal through development. The palatine bar, or the transverse commissure on the rostral tip of the dorsal longitudinal bar, is colored blue for the reference. avnb, anterior vertical nasal bar; com1, 2, commissures of dlb; cornc, cornual cartilage; dlb, dorsal longitudinal bar; dp, dental plate; hypcom, hypophyseal commissure; lp, lingual plate; nc, nasal capsule; nd, nasal duct cartilage; nt, notochord; otc, otic capsule; palb, palatine bar; pch, parachordal; pvnb, posterior vertical nasal bar; rp, rostral plate; snc, subnasal cartilage; t1-3, cartilaginous support for tentacles; trh, trabecula of hagfish; vb, velar bar
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
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getmorefigures.php?uid=PMC5015246&req=5

Fig2: Cranial skeletons of the Eptatretus embryo. aEptatretus burgeri embryo at stage 53 in dorsal view. bE. burgeri embryo at stage 53 in ventral view. cE. burgeri embryo at stage 60 in dorsal view. dE. burgeri embryo at stage 60 in left lateral view. e Relative growth of the developing hagfish chondrocrania. From top to bottom, stage 53, stage 60, prehatching and adult hagfish crania. Note, due to the rostral growth of the snout by addition of nasal duct cartilage and extension of subnasal cartilage (green), that the position of the nasal capsule (red) shifts relatively caudal through development. The palatine bar, or the transverse commissure on the rostral tip of the dorsal longitudinal bar, is colored blue for the reference. avnb, anterior vertical nasal bar; com1, 2, commissures of dlb; cornc, cornual cartilage; dlb, dorsal longitudinal bar; dp, dental plate; hypcom, hypophyseal commissure; lp, lingual plate; nc, nasal capsule; nd, nasal duct cartilage; nt, notochord; otc, otic capsule; palb, palatine bar; pch, parachordal; pvnb, posterior vertical nasal bar; rp, rostral plate; snc, subnasal cartilage; t1-3, cartilaginous support for tentacles; trh, trabecula of hagfish; vb, velar bar
Mentions: In E. burgeri embryos at stages 53–60 (Fig. 2a–d), the neurocranium consists of two pairs of longitudinal bars with transverse commissures and processes, rostrally attached to the nasal capsule. Caudally, the longitudinal bars are contiguous to the otic capsule, which continues medially to the parachordal that surrounds the rostral part of the notochord (Fig. 2a, b). From the boundary between the neurocranium and otic capsule, a pair of velar bars grows ventromedially, and later, by stage 53, becoming fused at the median plane to form a V-shaped element. The dental plate of the oral apparatus is located below the neurocranium, associated with the rostral part of the lingual plate that supports the muscles of the cyclostome ‘tongue’ [22]. The topographical relationships between these cranial elements in hagfish embryos continue to change over the course of development [23]. Prior to hatching, the nasal capsule grows cartilages supporting the rostrally extended nasal duct (Fig. 2e). Simultaneously, cartilages in the oronasal septum extend rostrally, and supporting cartilages arise within tentacles, features that are specific to adult individuals in all known hagfish species. These changes result in a caudad shift in the relative position of the nasal capsule in the cranium.Fig. 2

View Article: PubMed Central - PubMed

ABSTRACT

Background: The taxonomic position of the Middle Devonian fish-like animal Palaeospondylus has remained enigmatic, due mainly to the inability to identify homologous cranial elements. This animal has been classified into nearly all of the major vertebrate taxa over a century of heuristic taxonomic research, despite the lack of conclusive morphological evidence.

Results: Here we report the first comparative morphological analysis of hagfish embryos and Palaeospondylus, and a hitherto overlooked resemblance in the chondrocranial elements of these animals; i.e., congruence in the arrangement of the nasal capsule, neurocranium and mandibular arch-derived velar bar. The large ventral skeletal complex of Palaeospondylus is identified as a cyclostome-specific lingual apparatus. Importantly, the overall morphological pattern of the Palaeospondylus cranium coincides well with the cyclostome pattern of craniofacial development, which is not shared with that of crown gnathostomes. Previously, the presence of the vertebral column in Palaeospondylus made its assignment problematic, but the recent identification of this vertebral element in hagfish is consistent with an affinity between this group and Palaeospondylus.

Conclusion: These lines of evidence support the hagfish affinity of Palaeospondylus. Moreover, based on the less specialized features in its cranial morphology, we conclude that Palaeospondylus is likely a stem hagfish.

Electronic supplementary material: The online version of this article (doi:10.1186/s40851-016-0057-0) contains supplementary material, which is available to authorized users.

No MeSH data available.