Heterochronic opsin expression due to early light deprivation results in drastically shifted visual sensitivity in a cichlid fish: Possible role of thyroid hormone signaling

Abstract

During early ontogeny, visual opsin gene expression in cichlids is influenced by prevailing light regimen. Red light, for example, leads to an early switch from the expression of short-wavelength sensitive to long-wavelength sensitive opsins. Here, we address the influence of light deprivation on opsin expression. Individuals reared in constant darkness during the first 14 days post-hatching (dph) showed a general developmental delay compared with fish reared under a 12:12 hr light-dark cycle (control group). Several characters including pigmentation patterns and eye development, appeared later in dark-reared individuals. Quantitative real-time PCR and fluorescent in situ hybridization at six time points during the 14 days period revealed that fish from the control group expressed opsin genes from 5 dph on and maintained a short-wavelength sensitive phenotype (sws1, rh2b, and rh2a). Onset of opsin expression in dark-reared Midas cichlids was delayed by 4 days and visual sensitivity rapidly progressed toward a long-wavelength sensitive phenotype (sws2b, rh2a, and lws). Shifts in visual sensitivities toward longer wavelengths are mediated by thyroid hormone (TH) in many vertebrates. Compared to control fish, dark-reared individuals showed elevated dio3 expression levels - a validated proxy for TH concentration - suggesting higher circulating TH levels. Despite decelerated overall development, ontogeny of opsin gene expression was accelerated, resulting in retinae with long-wavelength shifted predicted sensitivities compared to light-reared individuals. Indirect evidence suggests that this was due to altered TH metabolism.

Habitat light sets the boundaries for the rapid evolution of cichlid fish vision, while sexual selection can tune it within those limits

“…Escobar‐Camacho et al (2016) found that the same three opsins were expressed in all of three different studied Amazonian cichlids, suggesting that Amazonian cichlids generally have a limited opsin repertoire. Although sampled representatives of Central American lineages expressed the same three cone opsins in our study, they appear to be generally less constrained in their visual repertoire as recent studies found more visual diversity among them, with at least some of them also expressing sws1 , sws2b and rh2b in certain habitat types or developmental stages (Härer, Meyer, & Torres‐Dowdall, 2018; Karagic, Härer, Meyer, & Torres‐Dowdall, 2018).…”

Evolution in caves: selection from darkness causes spinal deformities in teleost fishes

“…Melatonin is involved in the regulation of growth and development, and minimal light thresholds are needed for proper larval development in most fishes [18]. Indeed, dark-raised A. citrinellus have a disrupted thyroid metabolism [13], a downstream target of melatonin [18]. Not surprisingly, surgical removal of the pineal gland has been reported to cause spinal deformities in vertebrates [23].…”

“…Laboratory-reared Midas cichlids originated from a mixed-sex stock tank comprising wild-caught individuals collected in Lake Nicaragua in 2010 and 2013. For the experiment, conducted in 2017, embryos from an A. citrinellus brood were divided into 12 groups 2 days post-fertilization (n ¼ 10 each); six were placed in a 12 L : 12 D cycle and six in constant darkness (for details, see [13]). Two weeks after hatching, the percentages of surviving fish and of those with spinal deformities were quantified.…”

Reverting ontogeny: rapid phenotypic plasticity of colour vision in cichlid fish

“…Expression levels of opsin genes were based on qPCR data of two technical replicates and mean threshold cycle (Ct) values were used for subsequent analysis. Before and after the 14-day experimental period, expression of cone opsins was calculated proportionally to overall cone opsin expression (incorporating qPCR efficiencies) as previously described [4,14]. For fish reared under either blue or red light for 118 and 132 days, we tested whether treatment or age has an effect on cone opsin expression by using a nonparametric equivalent to a two-way ANOVA, the Scheirer–Ray–Hare test [17].…”

“…During ontogeny, many cichlid species shift opsin expression from short- to long-wavelength sensitivity [10]. Phenotypic plasticity in opsin expression seems to be rather common during this ontogenetic progression but appears to be restricted once the adult visual phenotype has been reached [5,14], but see [6,15]. Amphilophus astorquii , our study species, shows a paedomorphic visual phenotype, which might allow this species to maintain some degree of plasticity into adulthood, at least in the same direction as the ontogenetic progression (towards longer wavelengths) [4].…”