Temperature is a primary factor affecting early development of fish larvae and can regulate fish metabolism and feeding behavior during fish ontogeny (Kestemont and Baras 2001; Ma 2014). Furthermore, studies have demonstrated that the inappropriate range of temperature can lead to high mortality and body malformation on fish larvae (Lein et al. 1997; Ørnsrud et al. 2004; Ludwig and Lochmann 2009).
Jaw and skeletal malformations are often associated with poor growth and low survival of fish larvae and are a major bottleneck for efficient production of marine fish juveniles for aquaculture (Koumoundouros 2010; Boglione et al. 2013a, b). Jaw malformation can reduce fish survival and devalue fish quality on market (Barahona-Fernandes 1982; Cobcroft et al. 2004; Ma et al. 2014c). Jaw and skeletal malformations have been frequently observed on fish species in aquaculture such as striped trumpeter Latris lineata (Cobcroft et al. 2012), gilthead sea bream Sparus aurata (Andrades et al. 1996; Prestinicola et al. 2013), and yellowtail kingfish Seriola lalandi (Cobcroft et al. 2004). Lein et al. (1997) demonstrated that the increase of water temperature can induce jaw deformities. Under suboptimal temperatures, significant deformities of gill-cover and skeleton occur on gilthead seabream Sparus aurata (Georgakopoulou et al. 2010) and cranial deformities on European sea bass Dicentrarchus labrax (Georgakopoulou et al. 2007). In golden pompano Trachinotus ovatus, over 33 % of fish population exhibited at least one type of malformation during the larval period (Ma et al. 2014c; Zheng et al. 2014), but it is unclear if temperature leads to jaw deformities in this species. Therefore, it is necessary to explore the relationship between temperature and jaw deformity during early ontogeny of golden pompano larvae.
Skeletogenesis is a process of cell differentiation and proliferation in chondrocytes, osteoblasts, osteocytes and osteoclasts, and these cells determine the size, shape and mineral composition of bone structure (Nijweide et al. 1986; Karsenty and Wagner 2002; Phan et al. 2004). The gene expression during skeletogenesis is affected by both genetic and abiotic factors (Boglione et al. 2013a, b). Therefore, unveiling gene networks may provide insights into the potential mechanisms of skeletal malformations. The abiotic and biotic factors could induce skeleton deformity, while the gene expression drives the functional change of organs mediated by environmental factors.
In vertebrates, bone morphogenetic proteins (BMPs) control bone formation at different cell developmental states (e.g., stem cells, proliferative and hypertrophic chondrocytes, maturing osteoblast) (Hogan 1996a, b; Alaee et al. 2014; Windhausen et al. 2015). BMPs are genetically conserved in the animal kingdom, and their biological importance is reflected through functional and structural redundancy of different BMPs in a single species (Razdorov and Vukicevic 2012). For instance, BMPs 1, 2 and 3 can stimulate osteoblast, and play an important role in bone fracture healing (Grgurevic et al. 2011). BMPs 2, 4 and 6 are involved in skeletogenesis, especially in differentiation of chondrocytes to form cartilage, and both differentiation and maturation of the chondrocytes in the osteoblastic lineage will give a rise to bone formation (Rickard et al. 1994; Minina et al. 2001; Canalis et al. 2003; Wan and Cao 2005). Although the expression of BMP genes have been studied in several fish species, our understanding on these genes are limited to their discrepant expression at different developmental stage but not on the change body structure and function (Myers et al. 2002; Marques et al. 2014; Palomino et al. 2014; Tiago et al. 2014; Marques et al. 2015). In marine fish, the expression of BMP genes has been studied when fish larvae are under different supply of nutrients such as vitamins and lipids (Villeneuve et al. 2005a, b, 2006). Recently, BMP genes have been used to evaluate the hyperthermic effects on the skeletal malformation of fish larvae (Ytteborg et al. 2010). Up to present, information on the expression of BMPs in golden pompano is rare despite a high frequency of jaw deformation during the period of larval fish development. Investigation on the expression of BMPs in the ontogeny of golden pompano may provide a hint on the reason associated with jaw malformation in fish larvae during osteogenesis.
Golden pompano belongs to the Carangidae family and is a potential species for aquaculture diversification (Guo et al. 2014). Although the early ontogenetic development of digestive functionality (Ma et al. 2014a, b) and weaning strategies have been studied on golden pompano (Ma et al. 2014d), high jaw malformation during the early developmental stages has severely compromised production efficiency of this fish species in hatcheries. Our previous studies have identified the type, position, and frequency of jaw and skeletal malformations in golden pompano larvae (Ma et al. 2014c; Zheng et al. 2014), but factors causing skeletal malformation on this fish have never been evaluated. This paper aims to understand the impact of water temperature on jaw malformation of golden pompano larvae from the perspective of BMP expression on 18 DPH when jaw deformity starts to occur when weaning starts. The results of this study may contribute to improvement of fish quality and production efficiency in farming golden pompano and other marine fish larvae.