The integumentary skeleton of tetrapods: origin, evolution, and development

Abstract

Although often overlooked, the integument of many tetrapods is reinforced by a morphologically and structurally diverse assemblage of skeletal elements. These elements are widely understood to be derivatives of the once all-encompassing dermal skeleton of stem-gnathostomes but most details of their evolution and development remain confused and uncertain. Herein we re-evaluate the tetrapod integumentary skeleton by integrating comparative developmental and tissue structure data. Three types of tetrapod integumentary elements are recognized: (1) osteoderms, common to representatives of most major taxonomic lineages; (2) dermal scales, unique to gymnophionans; and (3) the lamina calcarea, an enigmatic tissue found only in some anurans. As presently understood, all are derivatives of the ancestral cosmoid scale and all originate from scleroblastic neural crest cells. Osteoderms are plesiomorphic for tetrapods but demonstrate considerable lineage-specific variability in size, shape, and tissue structure and composition. While metaplastic ossification often plays a role in osteoderm development, it is not the exclusive mode of skeletogenesis. All osteoderms share a common origin within the dermis (at or adjacent to the stratum superficiale) and are composed primarily (but not exclusively) of osseous tissue. These data support the notion that all osteoderms are derivatives of a neural crest-derived osteogenic cell population (with possible matrix contributions from the overlying epidermis) and share a deep homology associated with the skeletogenic competence of the dermis. Gymnophionan dermal scales are structurally similar to the elasmoid scales of most teleosts and are not comparable with osteoderms. Whereas details of development are lacking, it is hypothesized that dermal scales are derivatives of an odontogenic neural crest cell population and that skeletogenesis is comparable with the formation of elasmoid scales. Little is known about the lamina calcarea. It is proposed that this tissue layer is also odontogenic in origin, but clearly further study is necessary. Although not homologous as organs, all elements of the integumentary skeleton share a basic and essential relationship with the integument, connecting them with the ancestral rhombic scale.

Sauropod dinosaur osteoderms from the Late Cretaceous of Madagascar

“…The structural organization (compact cortex, cancellous core) and bone histology of the juvenile specimen (UA 9331) are broadly comparable with those of other archosaurs [1][2][3][4]7 . In contrast, the gross anatomical and microscopic structure of the adult-sized specimen (FMNH PR 2342) is unique.…”

“…The shape and surface texture of Rapetosaurus osteoderms indicates that these elements were low in relief and embedded in the integument as in other vertebrates [1][2][3]14,16 . As evidenced from extant taxa, all osteoderms form and reside within the dermis, either adjacent to the interface between the strata superficiale and compactum, or exclusively within the stratum superficiale, and are overlain by the epidermis [1][2][3][14][15][16][17] . The surface texture of Rapetosaurus osteoderms is consistent with the hypothesis that, as in crown group archosaurs, these structures were overlain by epidermal scales [1][2][3] .…”

“…Instead, we hypothesize that Rapetosaurus (and probably most titanosaurs) was characterized by a small number of osteoderms. Furthermore, unlike many osteoderm-bearing archosaurs [1][2][3] , these elements did not develop pervasively throughout the dermis but were probably restricted to the isolated regions of the integument. Whereas previous descriptions had reported the presence of articulating mosaics of osteoderms from the Maevarano formation 5 , we reinterpret these 'mosaics' as the fragmentary remains of individual adult-sized cavitied elements that were crushed post-mortem.…”

“…As evidenced from extant taxa, all osteoderms form and reside within the dermis, either adjacent to the interface between the strata superficiale and compactum, or exclusively within the stratum superficiale, and are overlain by the epidermis [1][2][3][14][15][16][17] . The surface texture of Rapetosaurus osteoderms is consistent with the hypothesis that, as in crown group archosaurs, these structures were overlain by epidermal scales [1][2][3] . The hollow nature of the adult specimen is unique, and we speculate that the juvenile morph remodels to achieve the adult form.…”

“…1c-e). Computed tomographic (CT) scans demonstrate that the pristinely preserved outer cortex of dense, compact bone is underlain by a cancellous core of bony trabeculae similar to that of other amniote osteoderms [1][2][3][4] ( Fig. 1e).…”