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. Summary statementCoral reef fishes in the family Holocentridae remodel their retina at the cellular and molecular levels to adapt to a nocturnal lifestyle during development.