†No significance should be attached to the order of authorship.
DEVELOPMENT AND EVOLUTIONARY ORIGINS OF VERTEBRATE SKELETOGENIC AND ODONTOGENIC TISSUES
Version of Record online: 21 JAN 2008
Volume 65, Issue 3, pages 277–373, August 1990
How to Cite
SMITH, M. M. and HALL, B. K. (1990), DEVELOPMENT AND EVOLUTIONARY ORIGINS OF VERTEBRATE SKELETOGENIC AND ODONTOGENIC TISSUES. Biological Reviews, 65: 277–373. doi: 10.1111/j.1469-185X.1990.tb01427.x
- Issue online: 21 JAN 2008
- Version of Record online: 21 JAN 2008
- Received 13 November 1989, revised and accepted 20 February 1990
This review deals with the following seven aspects of vertebrate skeletogenic and odontogenic tissues.
- 1The evolutionary sequence in which the tissues appeared amongst the lower craniate taxa.
- 2The topographic association between skeletal (cartilage, bone) and dental (dentine, cement, enamel) tissues in the oldest vertebrates of each major taxon.
- 3The separate developmental origin of the exo- and endoskeletons.
- 4The neural-crest origin of cranial skeletogenic and odontogenic tissues in extant vertebrates.
- 5The neural-crest origin of trunk dermal skeletogenic and odontogenic tissues in extant vertebrates.
- 6The developmental processes that control differentiation of skeletogenic and odontogenic tissues in extant vertebrates.
- 7Maintenance of developmental interactions regulating skeletogenic/odontogenic differentiation across vertebrate taxa. We derive twelve postulates, eight relating to the earliest vertebrate skeletogenic and odontogenic tissues and four relating to the development of these tissues in extant vertebrates and extrapolate the developmental data back to the evolutionary origin of vertebrate skeletogenic and odontogenic tissues. The conclusions that we draw from this analysis are as follows.
- 8The dermal exoskeleton of thelodonts, heterostracans and osteostracans consisted of dentine, attachment tissue (cement or bone), and bone.
- 9Cartilage (unmineralized) can be inferred to have been present in heterostracans and osteostracans, and globular mineralized cartilage was present in Eriptychius, an early Middle Ordovician vertebrate unassigned to any established group, but assumed to be a stem agnathan.
- 10Enamel and possibly also enameloid was present in some early agnathans of uncertain affinities. The majority of dentine tubercles were bare.
- 11The contemporaneous appearance of cellular and acellular bone in heterostracans and osteostracans during the Ordovician provides no clue as to whether one is more primitive than the other.
- 12We interpret aspidin as being developmentally related to the odontogenic attachment tissues, either closer to dentine or a form of cement, rather than as derived from bone.
- 13Dentine is present in the stratigraphically oldest (Cambrian) assumed vertebrate fossils, at present some only included as Problematica, and is cladistically primitive, relative to bone.
- 14The first vertebrate exoskeletal skeletogenic ability was expressed as denticles of dentine.
- 15Dentine, the bone of attachment associated with dentine, the basal bone to which dermal denticles are fused and cartilage of the Ordovician agnathan dermal exoskeleton were all derived from the neural crest and not from mesoderm. Therefore the earliest vertebrate skeletogenic/odontogenic tissues were of neural-crest origin.
- 16Given the separate developmental and evolutionary origin of the cranial exo- and endoskeletons (both derivatives of the cranial neural crest) we conclude that bone (of attachment) was the primary skeletogenic tissue in the exoskeleton (cartilage being secondary), but that uncalcified cartilage was the primary skeletogenic tissue in the endoskeleton (bone – perichondral – being secondary).
- 17Using evidence from developmental biology we conclude that the trunk neural crest of Ordovician agnathans was odontogenic, forming both dentine and bone of attachment of the trunk dermal exoskeleton.
- 18Initiation of differentiation of skeletogenic and odontogenic tissues is controlled epigenetically by one or more epithelial-mesenchymal interactions in epigenetic cascades.
- 19Changes in timing of steps in these epigenetic cascades provides an evolutionary mechanism for altering the types of skeletogenic/odontogenic tissues and/or structures formed.
- 20The appearance of epithelial-mesenchymal interactions and the origin of the skeletogenic/odontogenic neural crest at the outset of vertebrate evolution provided the developmental basis for the evolutionary origin of vertebrate skeletogenic and odontogenic tissues and for the appearance and evolution of the vertebrate skeleton.