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Palaeospondylus as a primitive hagfish

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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.


Developmental origins of Palaeospondylus cranial skeleton. a,b Diagrammatic anatomy of the cranial skeleton in dorsal (a) and ventral (b) views. c Cyclostome pattern in embryonic development of lamprey, hagfish, and also of Palaeospondylus. d Hypothetical developmental configuration of Palaeospondylus derived from the cyclostome craniofacial pattern. anp, anterior nasal process and its derivatives; ma, mandibular arch; mo, mouth; ne, nasal epithelium; nhp, nasohypophyseal plate; ph, pharynx; php, post-hypophyseal process and its derivatives; vert, vertebra. For other abbreviations, see Fig. 2
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Fig3: Developmental origins of Palaeospondylus cranial skeleton. a,b Diagrammatic anatomy of the cranial skeleton in dorsal (a) and ventral (b) views. c Cyclostome pattern in embryonic development of lamprey, hagfish, and also of Palaeospondylus. d Hypothetical developmental configuration of Palaeospondylus derived from the cyclostome craniofacial pattern. anp, anterior nasal process and its derivatives; ma, mandibular arch; mo, mouth; ne, nasal epithelium; nhp, nasohypophyseal plate; ph, pharynx; php, post-hypophyseal process and its derivatives; vert, vertebra. For other abbreviations, see Fig. 2

Mentions: As in cyclostomes, the cranium of Palaeospondylus is generally believed to consist of endoskeletal elements [5, 8, 9]. In many Palaeospondylus specimens, the vertebral column is preserved, and it is generally accepted that the massive skeletal element at the level of the first vertebral element represents the otic capsule [3–9] (Figs. 1 and 3a, b, Additional file 1: Figure S1, Additional file 2: Figure S2). We use this feature as a landmark in our identification of other skeletal elements in this species. Our observations (Additional file 1: Figure S1) and a review of the literature [5, 8, 26] (Additional file 2: Figure S2) indicate that Palaeospondylus possessed a neurocranium comparable to that of the hagfish embryo, in terms of the possession of two pairs of longitudinal bars (the dorsal longitudinal bar and hagfish trabecula), the palatine bar, and other commissures connecting these bars (Figs. 2 and 3a, b). Rostrally, several (presumably six) longitudinal bars run in parallel (‘rostralia’ in the previous description [5]; Fig. 1a, Additional file 1: Figure S1, Additional file 2: Figure S2). These bars are contiguous caudally with a transverse bar and are expanded towards the rostral end to contact with adjacent elements (Fig. 1a, Additional file 1: Figure S1, Additional file 2: Figure S2), forming a cage-shaped structure [5, 9]. The shape and position of this structure, and in particular the presence of both the anterior and posterior transverse bars, show strong morphological similarities with those of the nasal capsule in the hagfish embryo (Fig. 3a). The nasal capsule of Palaeospondylus was previously identified at a lateral part of the neurocranium (‘hemidome’) [10], but in that model, the other neurocranial elements, including the trabeculae (in this case, the trabecula of crown gnathostomes), could not be identified. In contrast, the homologization between Palaeospondylus and the hagfish embryo described above succeeds in identifying each skeletal element at a comparable position.Fig. 3


Palaeospondylus as a primitive hagfish
Developmental origins of Palaeospondylus cranial skeleton. a,b Diagrammatic anatomy of the cranial skeleton in dorsal (a) and ventral (b) views. c Cyclostome pattern in embryonic development of lamprey, hagfish, and also of Palaeospondylus. d Hypothetical developmental configuration of Palaeospondylus derived from the cyclostome craniofacial pattern. anp, anterior nasal process and its derivatives; ma, mandibular arch; mo, mouth; ne, nasal epithelium; nhp, nasohypophyseal plate; ph, pharynx; php, post-hypophyseal process and its derivatives; vert, vertebra. For other abbreviations, see Fig. 2
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig3: Developmental origins of Palaeospondylus cranial skeleton. a,b Diagrammatic anatomy of the cranial skeleton in dorsal (a) and ventral (b) views. c Cyclostome pattern in embryonic development of lamprey, hagfish, and also of Palaeospondylus. d Hypothetical developmental configuration of Palaeospondylus derived from the cyclostome craniofacial pattern. anp, anterior nasal process and its derivatives; ma, mandibular arch; mo, mouth; ne, nasal epithelium; nhp, nasohypophyseal plate; ph, pharynx; php, post-hypophyseal process and its derivatives; vert, vertebra. For other abbreviations, see Fig. 2
Mentions: As in cyclostomes, the cranium of Palaeospondylus is generally believed to consist of endoskeletal elements [5, 8, 9]. In many Palaeospondylus specimens, the vertebral column is preserved, and it is generally accepted that the massive skeletal element at the level of the first vertebral element represents the otic capsule [3–9] (Figs. 1 and 3a, b, Additional file 1: Figure S1, Additional file 2: Figure S2). We use this feature as a landmark in our identification of other skeletal elements in this species. Our observations (Additional file 1: Figure S1) and a review of the literature [5, 8, 26] (Additional file 2: Figure S2) indicate that Palaeospondylus possessed a neurocranium comparable to that of the hagfish embryo, in terms of the possession of two pairs of longitudinal bars (the dorsal longitudinal bar and hagfish trabecula), the palatine bar, and other commissures connecting these bars (Figs. 2 and 3a, b). Rostrally, several (presumably six) longitudinal bars run in parallel (‘rostralia’ in the previous description [5]; Fig. 1a, Additional file 1: Figure S1, Additional file 2: Figure S2). These bars are contiguous caudally with a transverse bar and are expanded towards the rostral end to contact with adjacent elements (Fig. 1a, Additional file 1: Figure S1, Additional file 2: Figure S2), forming a cage-shaped structure [5, 9]. The shape and position of this structure, and in particular the presence of both the anterior and posterior transverse bars, show strong morphological similarities with those of the nasal capsule in the hagfish embryo (Fig. 3a). The nasal capsule of Palaeospondylus was previously identified at a lateral part of the neurocranium (‘hemidome’) [10], but in that model, the other neurocranial elements, including the trabeculae (in this case, the trabecula of crown gnathostomes), could not be identified. In contrast, the homologization between Palaeospondylus and the hagfish embryo described above succeeds in identifying each skeletal element at a comparable position.Fig. 3

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.