3.8 Divergent expression of opsin genes
Opsin expression plays a key role in facilitating fish ecological adaption and evolution (Hofmann & Carleton 2009). To determine functional changes in the expanded genes, we performed expression analysis of opsin via RNA-seq of the retina tissue of C. undulatus . A total of 44,028,650 clean reads were obtained, and 3,849 genes showed higher expression (FPKM > 15), accounting for 17.3% of the total retina-expressed genes. Genes highly expressed in the retina include genes encoding retinal dehydrogenase 5 (FPKM: 15.34), which catalyzes the final step in the biosynthesis of 11-cis retinaldehyde to produce a light-sensitive chromophore (Skorczyk- Werneret al. 2015). Genes encoding retinal dehydrogenase 9 (FPKM: 26.98) are capable of converting 9-cis retinal to corresponding retinol with high efficiency. In contrast, the gene encoding retinol dehydrogenase 10 (FPKM: 18.63) converts all-trans-retinol to all-trans-retinal, which plays a profound role in chromophore generation at the level of rhodopsin (Tian et al. 2013). The cluster analysis of opsin genes showed divergent expression (Fig. 9).SWS2 a, SWS2 d, and Rh1 b are expressed in the retina, whereas SWS1 , SWS2 c, Rh1 a, and Rh2 b were expressed in other areas instead of the retina, suggesting functional changes after gene duplication, and acquisition of novel functions (Porath-Krause et al. 2016).
It is interesting to note that LWS1 was not expressed in any tissue. In many fishes, LWS1 and SWS2 spectrally reside in a head-to-tail pattern (Mackin et al. 2019), while in beetles,SWS2 was lost recently, and the sensitivity of SWS2 to blue wavelengths was restored by LWS1 extra copies (Sharkeyet al. 2017). It has been reported that labrid species have shown diverse expression of opsin genes in adaption of variable visual sensitivities to drive phenotypic diversity and behavioral ecologies (Phillips et al. 2016). A recent study found that the expression of the LWS1/SWS2 gene is a stochastic event, and exhibits a switch between opsin genes, even copies of which are triggered by the endocrine signal thyroid hormone (Mackin et al. 2019). This mechanism of opsin expression is useful to provide alternative adaption of visual cues in the developmental stages of organisms, the environment, and behavior. The alternative expression of opsin genes may be used to adapt to different photic environments for juveniles growing into C. undulatus adults, which live in different habitats (Sadovy et al. 2003), and opsin expression variation is also highly correlated to feeding strategy in damsels with herbivorous feeders (Stieb et al. 2017). Furthermore, C. undulatus is a protogynous hermaphrodite, changing sex from female to male around 8-9 years of age (Sadovy et al. 2003), and environmental stimuli, such as a unique mating behavior during spawning aggregations, is a primary trigger of sex change (Todd et al. 2019). Opsin gene expression divergence is believed to be responsible for detecting and discriminating between mating partners (Sandkam et al. 2017). Our results showed that the opsin gene expression pattern plays an important role in visual plasticity, development, behavior, and reproduction.