Development of dim-light vision in the nocturnal reef fish family Holocentridae. II: Retinal morphology

Abstract

Ontogenetic changes in the habitats and lifestyles of animals are often reflected in their visual systems. Coral reef fishes start life in the shallow open ocean but inhabit the reef as juveniles and adults. Alongside this change in habitat, some species also change lifestyles and become nocturnal. However, it is not fully understood how the visual systems of nocturnal reef fishes develop and adapt to these significant ecological shifts over their lives. Therefore, we used a histological approach to examine visual development in the nocturnal coral reef fish family, Holocentridae. We examined seven representative species spanning both subfamilies, Holocentrinae (squirrelfishes) and Myripristinae (soldierfishes). Pre-settlement larvae showed strong adaptation for photopic vision with high cone densities and had also started to develop a multibank retina (i.e., multiple rod layers), with up to two rod banks present. At reef settlement, holocentrids showed increased investment in their scotopic visual system, with higher rod densities and higher summation of rods onto the ganglion cell layer. By adulthood, they had well-developed scotopic vision with a highly rod-dominated multibank retina comprising 5-17 rod banks and enhanced summation of rods onto the ganglion cell layer. Lastly, the ecological demands of the two subfamilies were similar throughout their lives, yet their visual systems differed after settlement, with Myripristinae showing a more pronounced investment in scotopic vision than Holocentrinae. Thus, it is likely that both ecology and phylogeny contribute to the development of the holocentrid visual system.

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

“…Conversely, adult holocentrids showed upregulation of nr2e3 and rorb , both of which are involved in the development of rod photoreceptors ( Chen et al, 2005 ; Jia et al, 2009 ; Xie et al, 2019 ). The upregulation of TFs involved in rod formation in adults correlates well with the higher rod densities ( Fogg et al, 2022 ) and rod opsin gene expression at this stage. Additionally, nr2e3 is also known to suppress the expression of numerous cone-specific genes ( Chen et al, 2005 ), and thus, may also play a role in the developmental decrease in cone opsin gene expression in the holocentrids.…”

“…Finally, the most highly upregulated genes in adults were mainly involved in photoreception and aerobic respiration ( Table 2 ), while most of the GO terms enriched in adults were related to aerobic respiration and metabolism ( ). The upregulation of photoreception genes in adults is congruent with their higher photoreceptor densities ( Fogg et al, 2022 ) and implies that adults have a higher investment in vision than larvae. In contrast, the enrichment of genes and processes linked to metabolism may be related to general physiological differences between settlement larvae and adults (e.g.…”

“…rh1 , rhodopsin-like middle-wavelength sensitive 1 (rod opsin); rh2 , rhodopsin-like middle-wavelength sensitive 2; sws2 , short-wavelength-sensitive 2; lws , long-wavelength-sensitive. Morphological data from Fogg et al (2022) . …”

“…For example, butterflies show developmental changes in visual gene expression alongside changes in eye structure and therefore, some of the stage-specific expression differences were attributed to cellular composition ( Ernst and Westerman, 2021 ). Similarly, since the holocentrid retina undergoes cellular remodelling during development ( Fogg et al, 2022 ), it is likely that some of the expression changes simply facilitate these structural changes. Indeed, numerous processes relating to cellular development (e.g.…”

Multiple rod layers increase the speed and sensitivity of vision in nocturnal reef fishes

“…They mainly inhabit shallow depth ranges, however, a few species dwell as deep as 640 metres (25, 26). Holocentrids are nocturnal (27) and as such, they have a typical dim light-adapted visual system with large eyes (9), a rod-dominated retina (12, 28), a short focal length (15), a high summation of rods onto ganglion cells (GC) (29) and rh1 genes with spectral sensitivities that are tuned to the dominant wavelengths at their prevalent depth (30). They also possess a highly developed multibank retina, with up to 7 and 17 banks in squirrelfishes and soldierfishes, respectively (12).…”