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Vertebral Development in Paleozoic and Mesozoic Tetrapods Revealed by Paleohistological Data - PubMed Skip to main page content
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. 2016 Apr 13;11(4):e0152586.
doi: 10.1371/journal.pone.0152586. eCollection 2016.

Vertebral Development in Paleozoic and Mesozoic Tetrapods Revealed by Paleohistological Data

Marylène Danto  1 , Florian Witzmann  1   2 , Nadia B Fröbisch  1
Affiliations

Vertebral Development in Paleozoic and Mesozoic Tetrapods Revealed by Paleohistological Data

Marylène Danto et al. PLoS One. .

Abstract

Basal tetrapods display a wide spectrum of vertebral centrum morphologies that can be used to distinguish different tetrapod groups. The vertebral types range from multipartite centra in stem-tetrapods, temnospondyls, and seymouriamorphs up to monospondylous centra in lepospondyls and have been drawn upon for reconstructing major evolutionary trends in tetrapods that are now considered textbook knowledge. Two modes of vertebral formation have been postulated: the multipartite vertebrae formed first as cartilaginous elements with subsequent ossification. The monospondylous centrum, in contrast, was formed by direct ossification without a cartilaginous precursor. This study describes centrum morphogenesis in basal tetrapods for the first time, based on bone histology. Our results show that the intercentra of the investigated stem-tetrapods consist of a small band of periosteal bone and a dense network of endochondral bone. In stereospondyl temnospondyls, high amounts of calcified cartilage are preserved in the endochondral trabeculae. Notably, the periosteal region is thickened and highly vascularized in the plagiosaurid stereospondyls. Among "microsaur" lepospondyls, the thickened periosteal region is composed of compact bone and the notochordal canal is surrounded by large cell lacunae. In nectridean lepospondyls, the periosteal region has a spongy structure with large intertrabecular spaces, whereas the endochondral region has a highly cancellous structure. Our observations indicate that regardless of whether multipartite or monospondylous, the centra of basal tetrapods display first endochondral and subsequently periosteal ossification. A high interspecific variability is observed in growth rate, organization, and initiation of periosteal ossification. Moreover, vertebral development and structure reflect different lifestyles. The bottom-dwelling Plagiosauridae increase their skeletal mass by hyperplasy of the periosteal region. In nectrideans, the skeletal mass decreases, as the microstructure is spongy and lightly built. Additionally, we observed that vertebral structure is influenced by miniaturization in some groups. The phylogenetic information that can be drawn from vertebral development, however, is limited.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Phylogenetic relationship of extinct tetrapods examined in this study.
After [4, 10, 65, 66]. The sizes of the vertebral elements are not to scale and have been redrawn from [, , , , , –73]. Grey: intercentrum; green: pleurocentrum; white: origin unresolved.
Fig 2
Fig 2. Vertebral histology of Greererpeton sp. (Stem-tetrapod, Colosteidae), Adelogyrinidae indet. (Stem-tetrapod, Adelospondyli), and Whatcheeria deltae (Stem-tetrapod, Whatcheeriidae).
(A) Transverse section (1969.4-1G) of an intercentrum of Greererpeton sp. (CMNH 1969–4). (B) Transverse section (1993–2) of a centrum of Adelogyrinidae indet. (NMS 1993.56.111). (C) Transverse section (3347–2) of an intercentrum of Whatcheeria deltae (FMNH PR 3347). (D) Close-up of (A), in polarized light; calcified cartilage covers the dorsal surface of the intercentrum. (E) Close-up of (B), in normal transmitted light; thickened, spongy periosteal region with simple vascular canals and erosion rooms. (F) Close-up of (C), in normal transmitted light; remodeled trabecula that contains a core of primary calcified cartilage. Dotted line in (A), (B), and (C) indicates the border between periosteal and endochondral bone. In all centra, dorsal is to the top. Scale bars in (A)-(C) equal 5mm, in (D)-(F) 500μm. Abbreviations: cc—calcified cartilage; eb—endochondral bone; ER—erosion room; lb—lamellar bone; N—notochordal canal; NC—neural canal; pb—periosteal bone; PVC—primary vascular canal.
Fig 3
Fig 3. Vertebral histology of Doleserpeton sp. (Temnospondyli, Dissorophoidea).
(A) Transverse section (73530–2) of a pleurocentrum of Doleserpeton sp. (OMNH 73530B). (B) Close-up of (C), in normal transmitted light; suture between pleurocentrum and neural arch with remnants of calcified cartilage. (C) Transverse section (73530–5) of a pleurocentrum of Doleserpeton sp. (OMNH 73530E). (D) Transverse section (73530–4) of a pleurocentrum of Doleserpeton sp. (OMNH 73530D). (E) Close-up of (D), in normal transmitted light; notochordal canal surrounded by large cell lacunae. (F) Longitudinal section (73530–6) of a pleurocentrum of Doleserpeton sp. (OMNH 73530F). Dotted line in (A), (C), (D), and (F) indicates the border between periosteal and endochondral bone. In all centra, dorsal is to the top. In (F), the arrowhead points anteriorly. Scale bars in (A), (C), (D), and (F) equal 1mm, in (B) and (E) 100μm. Abbreviations: cc—calcified cartilage; cl—cell lacuna; eb—endochondral bone; N—notochordal canal; NA—neural arch; NC—neural canal; pb—periosteal bone; TP—transverse process.
Fig 4
Fig 4. Vertebral histology of Eryops sp. (Temnospondyli, Eryopoidae).
(A) Transverse section (1529–1) of an intercentrum of Eryops sp. (MB.Am.1529). (B) Close-up of (A), in normal transmitted light; two-parted periosteal cortex with a compact external layer and an internal layer of spongy, parallel-fibered bone. (C) Close-up of (A), in normal transmitted light; layer of calcified cartilage on the dorsal surface of the intercentrum. Dotted line in (A) indicates the border between periosteal and endochondral bone. In the centrum, dorsal is to the top. Scale bar in (A) equals 5mm, in (B) and (C) 500μm. Abbreviations: cc- calcified cartilage; eb—endochondral bone; ec—external cortex; ic—internal cortex; lb—lamellar bone; pb—periosteal bone; SO—secondary osteon.
Fig 5
Fig 5. Vertebral histology of Metoposaurus sp., Mastodonsaurus sp., and Cyclotosaurus intermedius (Temnospondyli, Stereospondyli).
(A) Longitudinal section (1437.2–2) of an intercentrum of Metoposaurus sp. (MB.Am.1437.2). (B) Transverse section (84213–1) of an intercentrum of Mastodonsaurus sp. (SMNS 84213A). (C) Transverse section (1437.11–1) of an intercentrum of Cyclotosaurus intermedius (MB.Am.1437.11). (D) Close-up of (A), in polarized light; remodeled trabecula that contains a core of primary calcified cartilage. (E) Close-up of (B), in normal transmitted light; remnants of calcified cartilage in the core of a trabecula. (F) Close-up of (C), in polarized light; spongy periosteal bone. Dotted line in (A)-(C) indicates the border between periosteal and endochondral bone. In all centra, dorsal is to the top. Scale bars in (A)-(C) equal 5mm, in (D)-(F) 100μm. Abbreviations: cc—calcified cartilage; eb—endochondral bone; ec—external cortex; lb—lamellar bone; pb—periosteal bone; PFB—parallel fibered bone.
Fig 6
Fig 6. Vertebral histology of Plagiosuchus sp. and Gerrothorax sp. (Temnospondyli, Stereospondyli, Plagiosauridae).
(A) Transverse section (52266–1) of a centrum of Plagiosuchus sp. (SMNS 52266A). (B) Transverse section (52266–3) of a centrum of Plagiosuchus sp. (SMNS 52266B). (C) Transverse section (52266–5) of a centrum of Plagiosuchus sp. (SMNS 52266C). (D) Transverse section (83451–3) of a centrum of Gerrothorax sp. (SMNS 83451B). (E) Close-up of (C), in polarized light; highly vascularized structure of the periosteal region. (F) Close-up of (C), in polarized light; remnants of calcified cartilage in the core of trabeculae of the endochondral region. Dotted line in (A)-(D) indicates the border between periosteal and endochondral bone. In all centra, dorsal is to the top. Scale bars in (A)-(D) equal 5mm, in (E)-(F) 100μm. Abbreviations: cc—calcified cartilage; eb—endochondral bone; lb—lamellar bone; pb—periosteal bone; PFB—parallel fibered bone; PO—primary osteon; SO—secondary osteon.
Fig 7
Fig 7. Vertebral histology of Archeria sp. and Proterogyrinus sp. (Anthracosauria, Embolomeri).
(A) Transverse section (1533–1) of an indetermined centrum of Archeria sp. (MB.Am. 1533). (B) Transverse section (1969.4-1P) of a pleurocentrum of Proterogyrinus sp. (CMNH 1969–4). (C) Close-up of (A), in polarized light; notochordal canal surrounded by bone arranged in circular rows. (D) Close-up of (A), in normal transmitted light; two-parted periosteal cortex with a compact external layer and a loose internal layer. (E) close-up of (B), in normal transmitted light; high amount of calcified cartilage in the dorsal peaks of the pleurocentrum. The dotted line in (A) and (B) indicates the border between periosteal and endochondral bone. In all centra, dorsal is to the top. Scale bars for (A) and (B) equal 5mm, (C)-(E) equal 500μm. Abbreviations: cc—calcified cartilage; eb—endochondral bone; ec—external cortex; ic—internal cortex; N—notochordal canal; pb—periosteal bone; PFB—parallel fibered bone.
Fig 8
Fig 8. Vertebral histology of Discosauriscus sp. and D. austriacus (Seymouriamorpha).
(A) Transverse section (KO187-1) of a pleurocentrum of Discosauriscus sp. (DE.KO.187). (B) Transverse section (K52-1) of a pleurocentrum of Discosauriscus austriacus (Z15568 [K52]). (C) Close-up of (A), in polarized light; strongly remodeled endochondral region. (D) Close-up of (A), in normal transmitted light; thin compact and nearly avascular periosteal region. (E) Close-up of (B), in polarized light; compact, lamellar bone in the neural arch. Dotted line in (A) and (B) indicates the border between periosteal and endochondral bone. In all centra, dorsal is to the top. Scale bars in (A) and (B) equal 1mm, in (C)-(E) 200μm. Abbreviations: eb—endochondral bone; ec—external cortex; lb—lamellar bone; N—notochordal canal; NA—neural arch; NC—neural canal; pb—periosteal bone; PFB—parallel fibered bone.
Fig 9
Fig 9. Vertebral histology of Seymouria sp. (Seymouriamorpha).
(A) Transverse section (73499) of a pleurocentrum of Seymouria sp. (OMNH 73499). (B) Close-up of (A), in normal transmitted light; remodeled trabecula with secondary lamellar bone on its surface. (C) Close-up of (A), in normal transmitted light; neural arch with a highly spongy structure. Dotted line in (A) indicates the border between periosteal and endochondral bone. In the centrum, dorsal is to the top. Scale bar in (A) equals 5mm, in (B) and (C) 100μm. Abbreviations: eb—endochondral bone; ER—erosion room; lb—lamellar bone; N—notochordal canal; NA—neural arch; NC—neural canal; pb—periosteal bone; PFB—parallel fibered bone; PVC—primary vascular canal.
Fig 10
Fig 10. Vertebral histology of Chroniosaurus dongusensis (Chroniosuchia, Chroniosuchidae).
(A) Transverse section (3585–220) of a pleurocentrum of Chroniosaurus dongusensis (PIN 3585–220). (B) Transverse section (3585–214) of an intercentrum of Chroniosaurus dongusensis (PIN 3585–214). (C) Transverse section (3585–218) of an intercentrum of Chroniosaurus dongusensis (PIN 3585–218). (D) Close-up of (A), in normal transmitted light; spongy periosteal region with large erosion rooms. (E) Close-up of B, in normal transmitted light; cartilaginous structure of the dorsal area of the intercentrum. (F) Close-up of (C), in normal transmitted light; remnants of calcified cartilage on the internal surface of the notochordal canal. Dotted line in (A)-(C) indicates the border between periosteal and endochondral bone. In all centra, dorsal is to the top. Scale bars in (A)-(C) equal 1mm, in (D)-(F) 100μm. Abbreviations: cc—calcified cartilage; eb—endochrondral bone; ec—external cortex; ER—erosion room; HA—haemal arch; N—notochordal canal; pb—periosteal bone.
Fig 11
Fig 11. Vertebral histology of Bystrowiella schumanni (Chroniosuchia, Bystrowianidae).
(A) Transverse section (81872–1) of a pleurocentrum of Bystrowiella schumanni (SMNS 81872A). (B) Transverse section (81872–6) of an intercentrum of Bystrowiella schumanni (SMNS 81872E). (C) Close-up of (A), in normal transmitted light; notochordal canal surrounded by a two-layered bone structure. (D) Close-up of (A), in normal transmitted light; two-layered periosteal cortex with a compact external layer and a loose internal layer. (E) Close-up of (B), in polarized light; strongly remodeled endochondral region. Dotted line in (A) and (B) indicates the border between periosteal and endochondral bone. In all centra, dorsal is to the top. Scale bars in (A) and (B) equal 1mm, in (C)-(E) 200μm. Abbreviations: eb—endochondral bone; ec—external cortex; ic—internal cortex; lb—lamellar bone; N—notochordal canal; pb—periosteal bone; PFB—parallel fibered bone.
Fig 12
Fig 12. Vertebral histology of Nectridea indet. and Diplocaulus magnicornis (Lepospondyli, Nectridea).
(A) Transverse section (2511) of a pleurocentrum of Nectridea indet. (FMNH UR 2511). (B) Longitudinal section (2510) of a pleurocentrum of Diplocaulus magnicornis (FMNH UR 2510). (C) Close-up of (A), in polarized light; two-layered periosteal cortex with a compact external layer and a spongy internal layer. (D) Close-up of (B), in normal transmitted light; neural arch penetrated by numerous Sharpey’s fibers. (E) Close-up of (B), in polarized light; remnants of calcified cartilage on the concave articular surfaces of the centrum. Dotted line in (A) indicates the border between periosteal and endochondral bone. In all centra, dorsal is to the top. Scale bars in (A) and (B) equal 5mm, in (C)-(E) 100μm. Abbreviations: cc—calcified cartilage; eb—endochondral bone; ec—external cortex; ER—erosion room; GM—growth mark; ic—internal cortex; N—notochordal canal; NA—neural arch; NC—neural canal; pb—periosteal bone; PO—primary osteon; ShF—Sharpey’s fibers.
Fig 13
Fig 13. Vertebral histology of Microbrachis sp. (Lepospondyli, “Microsauria”).
(A) Transverse section (854–1) of a pleurocentrum of Microbrachis sp. (MB.Am.854). (B) Longitudinal section (865) of a pleurocentrum of Microbrachis sp. (MB.Am.865). (C) Close-up of (A), in normal transmitted light; notochordal canal surrounded by large cell lacunae. (D) Close-up of (A), in polarized light; compact, avascular lamellar periosteal bone. (E) Close-up of (B), in normal transmitted light; concave articular surfaces composed of large cell lacunae. Dotted line in (A) and (B) indicates the border between periosteal and endochondral bone. In all centra, dorsal is to the top. Scale bars in (A) and (B) equal 1mm, in (C)-(E) 200μm. Abbreviations: cl- cell lacuna; eb—endochondral bone; ER—erosion room; lb—lamellar bone; N—notochordal canal; pb—periosteal bone.
Fig 14
Fig 14. Distribution of periosteal and endochondral bone in the vertebral centra investigated in this study.
After [4, 10, 65, 66]. The sizes of the vertebral elements are not to scale and have been redrawn from [, , , , , –73]. Grey: periosteal bone; blue: endochondral bone.
See this image and copyright information in PMC

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