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

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 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.

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

“…Details of all animals used in this study are given in . Animal collection and developmental staging followed methods outlined in greater detail in Fogg et al (2022) . Briefly, pre-settlement larvae were collected using light traps and settlement larvae were collected using a crest net ( Lecchini et al, 2004 ; Besson et al, 2017 ).…”

Developing and adult reef fish show rapid light‐induced plasticity in their visual system

“…and lws, increased proportional expression of sws2a and rh2c, and increased double cone expression of rh2c. Notably, visual plasticity was less pronounced in adults, potentially due to population differences between the two collection locations (i.e., Moorea Island for juveniles and Lizard Island for adults) or due to ongoing development in juveniles (Besson, 2017;Fogg et al, 2022a;Shand, 1997).…”

Developmental changes of opsin gene expression in ray-finned fishes (Actinopterygii)

“…The developmental shift in habitat preference is often suggested to drive ontogenetic changes in opsin expression (e.g. cichlids: [ 21 , 33 ]; black bream: [ 34 ]; eel: [ 35 ]; squirrelfishes and soldierfishes: [ 36 ]; clown anemonefish: [ 37 ]; damselfishes: [ 38 ]; bluefin killifish: [ 39 ]; gambusia: [ 40 ]; rainbow trout: [ 41 ]; dottybacks: [ 42 ]; starry flounder: [ 43 ]; deep-sea fishes: [ 10 , 44 ]). However, habitat-related changes of photic conditions solely do not always result in different and stage-specific visual system modifications, as seen in the Atlantic cod [ 18 ] or the spotted unicornfish [ 45 ].…”

“…However, habitat-related changes of photic conditions solely do not always result in different and stage-specific visual system modifications, as seen in the Atlantic cod [ 18 ] or the spotted unicornfish [ 45 ]. Shifts in diet (planktivory, carnivory and herbivory) and activity patterns (diurnal, nocturnal and crepuscular) [ 36 , 46 , 47 ], in addition to developmental or phylogenetic constraints seem to also play a role in shaping the visual diversity of fishes and potential age-related shifts of it.…”