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

Abstract

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.

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

“…Conversely, the top 15 DEGs upregulated in adults were primarily involved in visual perception and aerobic respiration ( Table 2 ). Notably, the DEGs also included several developmental transcription factors (TFs) ( Fogg and de Busserolles, 2022 ). In the larvae, this included upregulation of otx2 and otx5 , while in adults, the TFs, nr2e3 and rorb were upregulated.…”

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

“…e ., sws2a, rh2c and lws ). However, visual plasticity was less pronounced in adults, potentially due to ongoing development in settlement larvae (Besson, 2017; Fogg et al, 2022; Shand, 1997). Nevertheless, our findings are intriguing since they indicate that A. triostegus shows opsin gene expression plasticity in both developing and adult fishes, similar to findings in some freshwater fishes [ e .…”

“…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 .…”

“…Since continuous exposure to high-intensity light can cause retinal degeneration (Bernardos et al, 2007; Vera & Migaud, 2009), retinas of fish exposed to 24L were inspected for signs of degeneration prior to analysis. Subsequently, retinal cell densities were estimated from transverse retinal sections as described previously (Fogg et al, 2022; Shand, 1997). Briefly, in Fiji, retinal images were cropped to obtain 100 μm-wide strips, the number of cone outer segments (OS), outer nuclear layer (ONL) nuclei, INL nuclei and GC layer nuclei were counted for three sections per sample using the cell counter plugin and the density of each cell type per 0.01 mm 2 of retina was calculated.…”

“…However, vision may also be plastic within the lifetime of an individual, such as during its development (Evans & Fernald, 1993; Pankhurst, 1987; Shand, 1997; Shand et al, 2000; Siebeck & Marshall, 2007) and between seasons (Shimmura et al, 2017; Stieb et al, 2016). For example, a shift to a nocturnal lifestyle during ontogeny has been correlated with scotopic remodelling of the retina in reef fishes (Fogg et al, 2022; Shand, 1997). These ontogenetic and seasonal variations are regular, predictable alterations to the light environment that a species will have encountered over many preceding generations, potentially allowing genetic signals to contribute to adaption, such as has been found in killifish (Fuller et al, 2005) and damselfish (Stieb et al, 2016).…”