Plesiomorphically, the integumentary skeleton of osteichthyans consists of numerous rhombic scales organized into obliquely oriented rows. The scales are thick and localized within the stratum superficiale deep to the epidermis and firmly fixed to the stratum compactum by numerous Sharpey's fibers. Combined, this investiture of scales forms the near continuous scale-jacket (sensu Gemballa & Bartsch, 2002) across the body axis. Rhombic scales have two structural forms, corresponding to the ray-finned/lobe-finned dichotomy: actinopterygians have ganoid scales whereas sarcopterygians have cosmoid scales. Both scale types consist of multiple skeletal tissues (including hypermineralized tissues and a thick bony base), and both demonstrate an evolutionary trend towards reduction. Unlike cosmoid scales, which are entirely extinct, ganoid scales are still found in two lineages of living actinopterygians, polypterids (bichirs and reedfish) and lepisosteids (gars).
Ganoid scales of basal actinopterygians
Ganoid scales are characterized by ganoine (see Hypermineralized (capping) tissues above), overlying a region composed of orthodentine (Goodrich, 1907). True ganoid scales (in the strict sense of having multiple layers of ganoine) are considered apomorphic for actinopterygians, with well-documented examples dating back to the Devonian, 410 million years ago (Goodrich, 1907; Gross, 1968b, 1969, 1971b; Schultze, 1966, 1968, 1977; Märss, 2001; Schultze & Märss, 2004; Benton & Donoghue, 2007). Three types of ganoid scales are currently recognized: palaeoniscoid (in extinct basal actinopterygian lineages), polypteroid (used here for the scales of polypteriforms), and lepidosteoid (in lepisosteiforms).
Among the earliest, most basal actinopterygians (e.g. Andreolepis hedei from the late Silurian, 420 Ma; Gross, 1968b, 1969, 1971b; Janvier, 1971; Schultze, 1977; Märss, 2001; Schultze & Märss, 2004; Botella et al. 2007), individual palaeoniscoid scales are composed of a thick plate of cellular bone capped on the surface by multiple layers of tubular dentine (Fig. 12A). Superimposed on each layer of dentine is a thin monolayer of acellular crystalline tissue, reported to be either ganoine (Richter & Smith, 1995; Märss, 2001) or enameloid (Botella et al. 2007). Similar scales (cellular bone, tubular dentine, and a monolayer of ganoine) are also reported for Dialipina salgueiroensis (Devonian, 370 Ma; Schultze, 1977; Schultze & Cumbaa, 2001). Based in part on the interpretation of these elements as palaeoniscoid-type scales, it has been suggested that Andreolepis and Dialipina are either basal actinopterygians or more basal osteichthyans, if ganoid scales are plesiomorphic compared to cosmoid (Janvier, 1996; Märss, 2001; Schultze & Cumbaa, 2001; Benton & Donoghue, 2007; Botella et al. 2007).
Figure 12. Actinopterygii. Schematic illustrations of palaeoniscoid-type ganoid scales. (A) Andreolepis (late Silurian). (B) Cheirolepis (middle Devonian). (C) Moythomasia (late Devonian). (D) Scanilepis (Triassic). Palaeoniscoid-type ganoid scales grow by deposition of successive layers of dentine and ganoine (= cf. odontocomplexes) (A,C) or apposition of successive odontodes (B,D) onto a deep basal plate made of cellular bone. Scale bars: A,C,D: 100 µm; B: 125 µm.
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The earliest undisputed actinopterygians are from the middle to late Devonian (Janvier, 1996). Articulated remains of taxa such as Cheirolepis (Pearson & Westoll, 1979) and Moythomasia (Gross, 1950; Jessen, 1968, 1972; Gardiner, 1984) have palaeoniscoid scales (Fig. 12B,C), consisting of a superficial region of multilayered ganoine covering a region of dentine, and a thick basal plate of vascularized bone (Goodrich, 1907; Ørvig, 1978a,b,c; Sire, 1990). Palaeoniscoid scales are known only from the fossil record, with the most recent examples dating to the Jurassic (200–150 Ma) as in Scanilepis (Fig. 12D). Unlike more derived ganoid scales, most palaeoniscoid scales lack peg-and-socket articulations, likely resulting in a less flexible scale-jacket (Gemballa & Bartsch, 2002).
Polypteroid scales are unique to Polypteriformes (Cladistia) (Fig. 13A). These scales are structurally characterized by an additional tissue layer, elasmodine (see section Plywood-like tissues above), nested between two vascularized regions, dentine above and bone below (Sire et al. 1987). As has been demonstrated, the presence of elasmodine is a key feature in linking polypteroid scales with elasmoid scales (Sire, 1989, 1995; see Evolutionary scenario below).
The third type of ganoid scale, lepisosteoid, is found in Lepisosteiformes (Ginglymodi). Lepisosteoid scales are unique in lacking both elasmodine and dentine (Fig. 13B). Multilayered ganoid is directly apposed to the upper surface of the bony basal plate, which has relatively few blood vessels but numerous nonvascular (and enigmatic) canals of Williamson (Goodrich, 1907; Sire, 1994; Sire & Meunier, 1994). Both polypteroid and lepisosteoid scales date back, at least, to the late Cretaceous, 80–100 Ma (Dutheil, 1999; Janvier, 2007).
Notwithstanding their comparable morphological appearance, polypteroid and lepisosteoid scales demonstrate distinctly dissimilar modes of development. In polypteroid scales, the earliest stages of development are similar to those of elasmoid scales (Sire & Akimenko, 2004; Sire, unpublished data), and scales from young Polypterus senegalus closely resemble elasmoid scales (Sire, 1989). Of particular importance is the recognition that polypteroid scales develop from an odontogenic condensation. Similar to elasmoid scales, immature polypteroid scales are localized superficially within the dermis, adjacent to the interface with the epidermis. They initially form as a patchy layer of well-mineralized woven-fibered tissue. Along the deep margin of this layer, orthogonally arranged collagen lamellae are added, creating the plywood-like elasmodine. At this time, the developing polypteroid scale is framed above and below by capillary networks. In response to the presence of adjacent capillaries, cells along the upper surface continue to deposit woven-fibered matrix, encircling the blood vessels and thus creating vascular canals. These cells do not become trapped within the matrix but their elongate cell processes remain embedded in the matrix, defining the cells as odontoblasts and the tissue as dentine (see Structural diversity of dentines above). With continued deposition, odontoblasts and dentine matrix encroach increasingly towards the interface between the dermis and epidermis. Before contact with the basal surface of the epidermis is established, these superficial odontoblasts disappear. Concurrently, the overlying basal epidermal cells differentiate into ameloblasts. The ameloblasts make contact with the dentine surface and begin to deposit ganoine matrix (Sire et al. 1987; Sire, 1994). At this time the deep margin of developing polypteroid scales are lined by cells (elasmoblasts), which continue to deposit elasmodine. Likely in response to the presence of nearby capillaries, the extracellular matrix accumulating along the deepest margin of the elasmodine surface abruptly changes from highly organized elasmodine to a woven-fibered bone matrix. This alteration of extracellular matrix suggests a change from odontogenic to osteogenic contributions. Once growth of the scale slows down, deposition of the woven-fibered bone gives way to parallel-fibered, and then plywood-like organized lamellar bone. During this phase of ossification the scale incorporates numerous pre-existing collagen fibers of the stratum compactum, giving rise to Sharpey's fibers (Sire et al. 1987; Sire, 1989).
In contrast to polypteriforms, development of lepisosteoid scales demonstrates no evidence (inferred or otherwise) of an odontogenic contribution of the mesenchymal cells (e.g. no dentine deposited). The developing scales have no direct relationship with the epidermis, and do not pass through a transitory elasmoid scale-like phase (Nickerson, 1893; Sire, 1994; Sire & Huysseune, 2003). Lepisosteoid scales develop from an osteogenic primordium composed of numerous, closely packed osteoblast-like cells that deposit collagen and other extracellular matrix components within the stratum compactum of the dermis. Ossification begins within the centre of the osteogenic primordium. Following the appearance of woven-fibered bone, parallel-fibered and then lamellar bone is deposited on the superficial and deep margins, and Sharpey's fibers are incorporated from the surrounding stratum compactum. As growth continues, the superficial scale surface contacts the basalmost cells of the epidermis. Similar to polypteroid scales, the skeletogenic cells located at the superficial surface (in this case osteoblasts) retreat before the contact is established and the bordering basal epidermal cells differentiate into ameloblasts, and ganoine matrix is deposited.
Ganoid scales are also known for a variety of extinct Amiiformes (a lineage close to Teleostei), including sinamiids (early Triassic, 250 Ma), and Caturus furcatus (Jurassic, 200–150 Ma), a species close to extinct and living bowfins. These scales were thin, cycloid in shape and covered with a layer of ganoine (Schultze, 1996; Grande & Bemis, 1998). Amiiformes were long considered the sister group of Lepisosteiformes but this relationship is currently debated (Inoue et al. 2003; Hurley et al. 2007). Consequently, the exact histological structure of the ganoid scales in extinct amiiforms and determining whether elasmodine is present is of considerable interest.
In contrast to their relatives described above, in most amiiforms individual scales are reduced in thickness, lack the bony base, and are of elasmoid type. In the only living species, Amia calva, each scale has a thin, ornamented upper layer, similar to the external layer of teleost elasmoid scales, and a well-developed basal plate made of elasmodine organized into a twisted plywood-like arrangement (Meunier et al. 1978; Meunier, 1981), consistent with their identification as elasmoid scales (discussed below). Although scale development in bowfins remains unknown, the structural similarity of these elements with the teleost elasmoid scale provides strong support for their derivation from odontogenic condensations. Furthermore, the evolution of amiiform scales may parallel that of elasmoid scales, i.e. both derived from an ancestral polypteroid type (see Plywood-like tissues and Ganoid scales of basal actinopterygians above).
Without question, the elasmoid scale is the most common integumentary skeletal element among living vertebrates, including most of the 26 000 species of teleosts, Amia calva (discussed above), extant representatives of non-tetrapodan sarcopterygians (coelacanths and lungfish) and some gymnophionan amphibians (see below and Vickaryous et al. this Issue). Elasmoid scales are thin, imbricated, collagenous plates (Bertin, 1944). Although remarkably diverse in morphology and ornamentation (including both ctenoid and cycloid shapes), all elasmoid scales are fundamentally similar in structure (review in Huysseune & Sire, 1998; Sire & Akimenko, 2004). Each scale is composed of three layers (Fig. 13C). The first to form is the thin, ornamented external layer composed of a well-mineralized, woven-fibered tissue comparable with the dentine layer of polypteroid scales. As the elasmoid scale develops, this external layer expands at its lateral margins. Deep to the external layer is the relatively thick, basal plate composed of elasmodine (see Plywood-like tissues above). Elasmodine mineralizes slowly as the hydroxyapatite crystals do not penetrate deep within the collagen lamellae and for some taxa such as coelacanths, elasmodine remains unmineralized. The last and most superficial layer to form is the limiting layer. The limiting layer is deposited on the external layer surface, but has a restricted distribution in the posterior field of the scale facing the epidermis. Shortly after being deposited the limiting layer becomes hypermineralized (see section Hypermineralized (capping) tissues above). Unlike osseous tissues (see Ganoid scales of basal actinopterygians above, and following section), elasmodine does not become anchored to the deep dermis by Sharpey's fibers.
Scutes and dermal plates
Among some early chondrosteans (e.g. Saurichthys; early Triassic to early Jurassic, 250–200 Ma), elements of the integumentary skeleton resemble lepisosteoid scales: a bony base capped by a superficial region of multilayered ganoine. In most living Acipenseriformes (sturgeons and paddlefish) and related fossil taxa [e.g. the early Triassic form Birgeria (Ørvig, 1978a)], ganoine is lost and thus individual scales (bony plates, scutes) are composed exclusively of cellular, parallel-fibered bone (Bemis et al. 1997). A lepisosteoid-type ganoid scale origin for chondrostean bony plates is supported by developmental data demonstrating a strong parallel between early skeletogenesis of these two elements (Sewertzoff, 1932; Sire, unpubl. data).
Among various teleosts, elasmoid-type scales are replaced by plates of cell-rich bone. In armoured catfish (callichthyids, loricariids and doradids), these bony elements are capped by a layer of hyaloine, creating what are known as scutes (see Hypermineralized (capping) tissues above; Sire, 1993; Sire & Meunier, 1993) (Fig. 13D). These scutes (as well as fin rays and cranial bones) are ornamented with dermal denticles which are tooth-like elements (Sire & Huysseune, 1996; Sire, 2001). For other taxa including gasterosteiforms, tetraodontiforms and syngnathiforms, no capping tissue forms and the resulting dermal plates are composed exclusively of bone (Fig. 13E).
Both dermal plates and scutes begin ossification deep in the dermis, from an osteogenic primordium. As the bony plate begins to deposit osteoid and woven-fibered bone, pre-existing collagen fibers from the surrounded dermis are integrated into the matrix, in addition to various bone matrix components deposited by the osteoblasts. With continued ossification, this primordium becomes progressively surrounded by parallel-fibered bone, and eventually by a region made of plywood-organized lamellar bone, in which are incorporated Sharpey's fibers.