Teleost Skeletal Plasticity: Modulation, Adaptation, and Remodelling
The vertebrate skeleton is a plastic organ system and the skeleton of teleosts is no exception. Epigenetic factors during development influence skeletal anatomy, mechanical properties, and meristic characters. The adult teleost skeleton undergoes changes connected to mechanical adaptation, repair, mineral homeostasis, sexual maturation, and aging. Vestiges, rudiments, atavisms, hyperostotic bones, additional tooth rows, and variable numbers of vertebral bodies are prominent examples of variable characters. Morphological changes require changes of skeletal structures on the cellular level, including modulation, transdifferentiation, and remodelling. Alterations at the cellular level are best understood by acknowledging those characters that distinguish teleost skeletons from mammalian skeletons: (a) the absence of osteocytes in most species of teleosts; (b) abundant mononucleated osteoclasts that perform non-lacunar bone resorption; (c) a phosphorous- rather than a calcium-driven mineral homeostasis; and (d) a variety of tissue types intermediate between bone and cartilage. This brief account of teleost skeletal plasticity shows that the teleost skeleton is a lifelong plastic organ system. Using examples, also from our own studies, we provide examples of skeletal plasticity at various hierarchical levels.

Adaptation of internal bone structures and tooth morphology in the lower pharyngeal jaw in response to mechanical load in the cichlid Astatoreochromis alluaudi. (A) Animal raised on soft food. (B) Animal raised on hard food. In this animal the amount of bone (dark gray) in the lower pharyngeal jaw increases and the teeth (light gray) acquire a molariform shape. Modified after Witten and Huysseune (2009), see also Huysseune et al. (1994) for further details.

Remodelling and plasticity of vertebral bodies in Atlantic salmon (Salmo salar). (A) The elongation of adjacent vertebral bodies (white asterisk) compensates for the compression of vertebral bodies (white arrowhead). (B) Compression as shown in (A) can lead to the complete fusion of vertebral bodies. The figure shows the result of a complete fusion, a process in which three fused vertebral bodies are remodeled into one normal shaped vertebral body, indicated by supernumerary haemal and neural arches (white arrowheads). Modified after Witten et al. (2006), see also this reference for developmental stages of vertebral fusion; see Sambraus et al. (2014) for the occurrence of vertebral body compression and fusion in wild Atlantic salmon.

The relationship between temperature and the number of vertebral bodies according to Fowler (1970). The bold black line represents the general relationship between vertebral numbers in teleost fishes and temperature. At lower rearing temperatures more vertebral bodies develop. Less vertebral bodies develop at higher temperatures. For particular species, a U-shaped relationship between temperature and vertebral body number has been observed (light gray lines). The minimum number of vertebral bodies develops at the species-specific temperature optimum with a tendency to increase vertebral body numbers at lower and at higher temperatures. Modified after Fowler (1970).

Variation in caudal fin endoskeleton development in Danio rerio, modified after Bensimon-Brito et al. (2012a). (A) The fully developed caudal fin endoskeleton contains modified haemal arches, respectively haemal spines, named hypurals. A gap in the row of hypurals is represented by the diastema. (B) Characteristic development of cartilaginous hypural anlagen in an animal of 6 mm standard length. The basis of H4 is typically broad (anteriorly extended). (C) A variation of hypural development shows the rudiment of H3 instead of a broadened basis of H4. (D) Similar developmental variation as in (C), but the cartilaginous rudiment of H3 is connected to H4. See Bensimon-Brito et al. (2012a) for a detailed description and for other variations (rudiments and vestiges) during caudal fin development of D. rerio. Bone, black; cartilage, dark gray; notochord light gray; H, hypurals; Ph, parhypural; HsPu2, haemal spine of preural vertebral body 2; Nc, notochord. The nomenclature of elements follows the new polyural interpretation according to Schultze and Arratia (2013) and Wiley et al., 2015, in this volume.

Atavistic reappearance of a 4th tooth row, modified after Shkil et al. (2010). (A) The pharyngeal jaws of Barbus intermedius are characterized by the presence of three rows of teeth. (B) 10% of the animals in a population have a 4th tooth row. Shkil et al. (2010) show that this natural phenomenon can also be obtained in experiments by the inhibition of thyroxin.

(A) X-ray, showing the regular patterning of the dentition in wild Atlantic salmon, modified after Huysseune et al. (2007). The position of a functional tooth is followed by a developing replacement tooth in the next tooth position, followed by a tooth anlage and an old tooth in resorption in the subsequent position. (B) X-ray showing that the highly regular patterning of tooth replacement (no edentulous stage prior to spawning) is lost in salmon that stay in the river over the winter after spawning. Several functional teeth are completely resorbed (white arrowheads). Other functional teeth are neither resorbed nor shed, indicated by the complete mineralization of the tooth basis (white asterisk). The black asterisk points to the basis of a resorbed tooth. Regular tooth patterning is restored in animals that return to the sea after the winter. See also Witten et al. (2005).

X-ray, showing the start of hyperostotic bone formation at haemal arches and haemal spines in Pagrus pagrus, 41.7 cm SL. The X-ray shows vertebral bodies 13–20. See Smith-Vaniz et al. (1995) and Smith-Vaniz and Carpenter (2007) for a comprehensive treatment of the regular occurrence of hyperostotic bone outgrowth.

(A) Intramedullary tooth development at the dentary of the cichlid Oreochromis niloticus. Histological section stained with haematoxylin. Alveolar bone, black asterisks; developing teeth, black arrowheads. (B) Development and tooth eruption require bone resorption and bone remodelling. The plain histological staining in (A) does not reveal signs of resorption: multinucleated osteoclasts and resorption lacunae are not visible. The identification of osteoclasts by demonstrating the osteoclast specific enzyme tartrate resistant acids phosphatase (TRAP) reveals the presence of bone resorbing cells and the location of bone resorption (black staining, red in original preparation). See Witten and Huysseune (2009) for more details and further references.
Contributor Notes
Associate Editor: G. Arratia.