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Microhabitat partitioning correlates with opsin gene expression in coral reef cardinalfishes (Apogonidae)

Vertebrates exhibit diverse visual systems that vary in terms of morphology, number and distribution of spectrally distinct photoreceptor types, visual opsin genes and gene expression levels. In fish, such adaptations are driven by two main factors: differences in the light environment and behavioural tasks, including foraging, predator avoidance and mate selection. Whether visual systems also adapt to small-scale spectral differences in light, between microhabitats, is less clear. We suggest that differences in microhabitat use by cardinalfishes (Apogonidae) on coral reefs drive morphological and molecular adaptations in their visual systems. To test this, we investigated diurnal microhabitat use in 17 cardinalfish species and assessed whether this correlated with differences in visual opsin gene expression and eye morphology. We found that cardinalfishes display six types of partitioning behaviours during the day, ranging from specialists found exclusively in the water column to species that are always hidden inside the reef matrix. Using data on visual opsin gene expression previously characterized in this family, it was discovered that species in exposed habitats had increased expression of the short-wavelength sensitive violet opsin (SWS2B) and decreased expression of the dim-light active rod opsin (RH1). Species of intermediate exposure, on the other hand, expressed opsins that are mostly sensitive to the blue-green central part of the light spectrum (SWS2As and RH2s), while fishes entirely hidden in the reef substrate had an increased expression of the long-wavelength sensitive red opsin (LWS). We found that eye size relative to body size significantly differed between cardinalfish species, and relative eye size decreased with an increase in habitat exposure. Retinal topography did not show co-adaptation with microhabitat use, but instead with feeding mode. We suggest that, although most cardinalfishes are nocturnal foragers, their visual systems are also adapted to both the light intensity and the light spectrum of their preferred diurnal microhabitat.