Phylogenetic analysis and ontogenetic changes in the cone opsins of the western mosquitofish (Gambusia affinis)

Lecchini

et al. 2022

Preprint

Developmental changes to the visual systems of animals are often associated with ecological shifts. Reef fishes experience a change in habitat between larval life in the shallow open ocean to juvenile and adult life on the reef. Some species also change their lifestyle over this period and become largely nocturnal. While these ecological transitions are well documented, little is known about the ontogeny of nocturnal reef fish vision. Here, we used histology and transcriptomics to investigate visual development in 12 representative species from both subfamilies, Holocentrinae (squirrelfishes) and Myripristinae (soldierfishes), in the nocturnal coral reef fish family, Holocentridae. Results revealed that the visual systems of holocentrids are initially well-adapted to photopic conditions with pre-settlement larvae having high cone densities, high cone opsin gene expression, a broad cone opsin gene repertoire (8 genes) and a multibank retina (i.e., stacked layers of rods) comprising up to two rod banks. At reef settlement, holocentrids started to invest more in their scotopic visual system and upregulated genes involved in cell differentiation/proliferation. By adulthood, they had well-developed scotopic vision with a rod-dominated multibank retina comprising 5-17 rod banks, increased summation of rods onto ganglion cells, high rod opsin gene expression, reduced cone opsin gene expression and repertoire (1-4 genes) and upregulated phototransduction genes. Finally, although the two subfamilies shared similar ecologies across development, their visual systems diverged after settlement, with Myripristinae investing more in scotopic vision than Holocentrinae. Hence, both ecology and phylogeny likely determine the development of the holocentrid visual system.

Section: Opsin Gene Expression Over Developmentmentioning

confidence: 86%

Development of dim-light vision in the nocturnal coral reef fish family, Holocentridae

Lecchini

et al. 2022

Preprint

“…Furthermore, they stopped expressing most of their cone opsin genes, only retaining cone opsins sensitive to the mid-range (bluegreen; sws2a and rh2) wavelengths that dominate the reef at night. This is in contrast with changes in most diurnal fishes, which do not reduce the number of cone opsins expressed over ontogeny (Takechi and Kawamura 2005;Shand et al 2008;Cortesi et al 2016;Tettamanti et al 2019;Chang et al 2020).…”

Section: Opsin Gene Expression Over Developmentmentioning

confidence: 89%

Development of dim-light vision in the nocturnal reef fish family Holocentridae. I: Retinal gene expression

Journal of Experimental Biology

Lecchini

et al. 2022

Developmental changes to the visual systems of animals are often associated with ecological shifts. Reef fishes experience a change in habitat between larval life in the shallow open ocean to juvenile and adult life on the reef. Some species also change their lifestyle over this period and become nocturnal. While these ecological transitions are well documented, little is known about the ontogeny of nocturnal reef fish vision. Here, we used transcriptomics to investigate visual development in 12 representative species from both subfamilies, Holocentrinae (squirrelfishes) and Myripristinae (soldierfishes), in the nocturnal coral reef fish family, Holocentridae. Results revealed that the visual systems of holocentrids are initially well-adapted to photopic conditions with pre-settlement larvae having high cone opsin gene expression and a broad cone opsin gene repertoire (8 genes). At reef settlement, holocentrids started to invest more in their scotopic visual system and compared to adults, showed upregulation of genes involved in cell differentiation/proliferation. By adulthood, they had well-developed scotopic vision with high rod opsin gene expression, reduced cone opsin gene expression and repertoire (1-4 genes) and upregulated phototransduction genes. Finally, although the two subfamilies shared similar ecologies across development, their visual systems diverged after settlement, with Myripristinae investing more in scotopic vision than Holocentrinae. Hence, both ecology and phylogeny likely determine the development of the holocentrid visual system.

“…As found in N. brevirostris , the opsin genes are differentially expressed between life stages in A. triostegus . Ontogenetic changes in opsin gene expression are often related to changes in habitat and diet (Chang et al, 2020; Fogg et al, 2022; Lupše et al, 2021; Shand et al, 2008; Tettamanti et al, 2019). Indeed, A. triostegus larvae rapidly increase expression of the green-sensitive cone opsins ( i .…”

Section: Discussionmentioning

confidence: 99%

Developing and adult reef fish show rapid, reversible light-induced plasticity in their visual system

Gache

et al. 2022

Preprint

The visual capabilities of fish are optimised for their ecology and light environment over evolutionary time. Similarly, fish vision can adapt to regular changes in light conditions within their lifetime, e.g., ontogenetic or seasonal variation. However, we do not fully understand how vision responds to irregular short-term changes in the light environment, e.g., algal blooms and light pollution. In this study, we investigated the effect of short-term exposure to unnatural light conditions on opsin gene expression and retinal cell densities in larval and adult diurnal reef fish (convict surgeonfish; Acanthurus triostegus). Results revealed phenotypic plasticity in the retina across ontogeny, particularly in the larvae. The most substantial differences at both molecular and cellular levels were found under constant dim light, while constant bright light or simulated artificial light at night had a lesser effect. Under dim light, larvae and adults increased expression of the cone opsin genes, sws2a, rh2c and lws, within a few days and larvae also decreased densities of cones, inner nuclear layer cells and ganglion cells. These changes likely enhanced vision under the altered light conditions. Thus, our study suggests that plasticity mainly comes into play when conditions are extremely different to the species’ natural light environment, i.e., a diurnal fish in ‘constant night’. Finally, in a rescue experiment on adults, shifts in opsin expression were reverted within 24 hours. Overall, our study showed rapid, reversible light-induced changes in the retina of A. triostegus, demonstrating phenotypic plasticity in the visual system of a reef fish throughout life.