A Deep Phylogenetic Split Between Short- and Long-Wavelength-Tuned Visual Systems in Surgeonfishes (Acanthuridae)

Abstract

The light environment, coupled with ecology, is widely thought to drive visual adaptation, creating species-specific visual niches. However, coral reef ecosystems experience continuous spatiotemporal variations in light conditions, and mechanisms such as phenotypic plasticity may be essential for coral reef animals to adjust to such changing sensory requirements. It remains unclear how widespread colour vision plasticity is, or the extent to which ecology and phylogeny drive plasticity in coral reef fishes. Using a comparative transcriptomic approach across 22 species, we aimed to investigate visual plasticity within a prominent coral reef fish family, surgeonfishes (Acanthuridae), in response to changes in the light environment throughout development and across seasons in adults. Surprisingly, we uncovered a deep phylogenetic split (~42 mya) in visual opsin gene expression profiles, with Nasinae expressing a shorter-shifted palette than Acanthurinae, which coincides with the divide between water-column and benthic-feeding modalities during the speciation of their last common ancestor. However, opsin gene expression showed little variation in response to seasonal or ontogenetic shifts in the light environment, nor in the broad functional feeding groups extant species from both subfamilies fall under. Thus, the invariable visual gene expression observed in present-day surgeonfishes appears to be dictated by phylogenetic inertia, despite rapid diversification into a range of ecological niches. This suggests that spectral tuning into two main modalities, short and long, reduces the need for visual plasticity, allowing larger and more mobile coral reef fishes to conduct visually guided behaviours across the entire range of light environments they encounter.