Skeletal Morphogenesis and Anomalies in Gilthead Seabream: A Comprehensive Review

Abstract

The gilthead seabream, one of the most important species in Mediterranean aquaculture, with an increasing status of exploitation in terms of production volume and aquafarming technologies, has become an important research topic over the years. The accumulation of knowledge from several studies conducted during recent decades on their functional and biological characteristics has significantly improved their aquacultural aspects, namely their reproductive success, survival, and growth. Despite the remarkable progress in the aquaculture industry, hatchery conditions are still far from ideal, resulting in frequent abnormalities at the beginning of intensive culture, entailing significant economic losses. Those deformities are induced during the embryonic and post-embryonic periods of life, and their development is still poorly understood. In the present review, we created a comprehensive synthesis that covers the various aspects of skeletal morphogenesis and anomalies in the gilthead seabream, highlighting the genetic, environmental, and nutritional factors contributing to bone deformities and emphasized the potential of the gilthead seabream as a model organism for understanding bone morphogenesis in both aquaculture and translational biological research. This review article addresses the existing lack in the literature regarding gilthead seabream bone deformities, as there are currently no comprehensive reviews on this subject.

Keywords: bone deformities; craniofacial anomalies; genes; gilthead seabream; models; ossification pattern; skeletal morphogenesis; spinal deformities.

Figure 1

The ossification pattern of gilthead seabream larvae (a) at 33 DPH, (b) at 43 DPH, (c) at 53 DPH. Double-stained larvae showed alician blue-stained cartilaginous structures and alizarin red-stained bony structures. Fr, frontal; Ttm, taenia tecti medialis; Et, epiphysial tectum; Sc, sclerotic; Lp, lamina precerebralis; Rc, rostral cartilage; Pm, premaxillary; Mx, maxillary; De, dentary; Br, branchiostegal rays; Cl, cleithrum; Co-Sca, coraco scapular cartilage; Pp, parapophyse; Ha, hemal arches; Hy, hypural; Ep, epural; Na, neural arches. Scale bar: 0.5 mm. Schematic representation adapted from [12].

Figure 2

The teleostean operculum complex organization. Schematic representation adapted from [41].

Figure 3

Different forms of the opercular complex abnormalities in gilthead seabream larvae aged 13–53 DPH. (a) Hypoplastic operculum, (b) reduced opercle (white arrows) and lack of interopercle (asterisks), (c) folded opercular bones toward the gills chamber leading to the exposition of gill arches, (d) outside folded operculum, (e) wave-like gill caver (red line) modulating a branchiostegal membrane (blue line), (f) spring-like gill caver with exposed gill arches, (g) combined shortened-folded operculum, (h) hyperplastic branchiostegal membrane, (i) folded branchiostegal rays in the gill chamber. Scale bars: 200 µm. Figure is adapted from Mhalhel et al. [12].

Figure 4

Stereomicrograph of different abnormality types of the maxillaries and premaxillaries in gilthead seabream. (a) Normal anatomy of maxillaries (Ma), premaxilaries (PM), and rostral cartilage (Rc), in a seabream larva (9.5 mm TL), (b) size reduction in the premaxillaries; (c) narrowing of maxillaries (arrow) and complete absence of the premaxillaries. Adapted from Fragkoulis et al., 2018 [44].

Figure 5

X-ray of gilthead seabream with different forms of spinal deformities. (a) Normal anatomy of cervical, abdominal, and caudal regions of the vertebral column. Inter-vertebrae space is highlighted with an arrow, and swim bladder is indicated with a star; (b) apical X-ray of seabream caudal region with scoliosis (highlighted with arrows); (c) X-ray of seabream with coexisting two main deformities of the vertebral column lordosis and vertebral compression. (a,b) Are adapted from Boursiaki et al., 2019 [48], while (c) is adapted from Berellis et al., 2015 [49].

Figure 6

Typical forms of skeletal abnormalities in gilthead seabream larvae from the three groups of larvae at 53 DPH. (a) Rectangular slender vertebral body (white asterisks), and bifurcated neural spine (arrow); (b) cubic thick vertebral body (black asterisks); (c) the last caudal vertebra (v), preceding the urostyle (u), is triangular-shaped with detached neural spine (arrow). The absence of the three epurals (white circle), lack of the fifth hypural, and fusion of the third and fourth hypural (black asteriks); (d) bifurcated neural spine (black arrow); (e) detached neural spine (arrow). The circle indicates a normal epural arrangement; (f) normal hypural arrangement (1st to 5th hypurals) and absence of the three epurals (white circle). Scale bars (a,b): 100 µm, and (c–f): 50 µm. The figure was adapted from Mhalhel et al. [12].

Figure 7

Caudal-fin deformities in gilthead seabream. (a) Lateral twisting of the whole caudal complex, (b) incomplete formation of dorsal fin in juvenile S. aurata, (c) duplication of caudal fin, and (d) complete lack of anal fin in juvenile S. aurata. The figure was adapted from Koumoundouros et al. [51].

Figure 8

Relative gene expression of (a) ECM components and (b) transcription factors in gilthead seabream vertebral column fragments of control animals (CT) or specimens with lordosis (LD) or lordosis–scoliosis–kyphosis (LSK). Results are shown as the mean ± SEM. Distinct letters denote statistically significant differences among groups (p < 0.05). The figure was adapted from Riera-Heredia et al. [64].