Abstract
Catadromous fishes migrate between ocean and freshwater during particular phases of their life cycle. The dramatic environmental changes shape their physiological features, e.g. visual sensitivity, olfactory ability, and salinity tolerance. Anguilla marmorata, a catadromous eel, migrates upstream on dark nights, following the lunar cycle. Such behavior may be correlated with ontogenetic changes in sensory systems. Therefore, this study was designed to identify changes in spectral sensitivity and opsin gene expression of A. marmorata during upstream migration. Microspectrophotometry analysis revealed that the tropical eel possesses a duplex retina with rod and cone photoreceptors. The λmax of rod cells are 493, 489, and 489 nm in glass, yellow, and wild eels, while those of cone cells are 508, and 517 nm in yellow, and wild eels, respectively. Unlike European and American eels, Asian eels exhibited a blue-shifted pattern of rod photoreceptors during upstream migration. Quantitative gene expression analyses of four cloned opsin genes (Rh1f, Rh1d, Rh2, and SWS2) revealed that Rh1f expression is dominant at all three stages, while Rh1d is expressed only in older yellow eel. Furthermore, sequence comparison and protein modeling studies implied that a blue shift in Rh1d opsin may be induced by two known (N83, S292) and four putative (S124, V189, V286, I290) tuning sites adjacent to the retinal binding sites. Finally, expression of blue-shifted Rh1d opsin resulted in a spectral shift in rod photoreceptors. Our observations indicate that the giant mottled eel is color-blind, and its blue-shifted scotopic vision may influence its upstream migration behavior and habitat choice.
Highlights
Fish habitats are highly diverse, ranging from the deep sea to the upper reaches of freshwater rivers in the mountains, and from the tropics to the Arctic; the photic conditions in these environments vary greatly in terms of turbidity, color, and brightness
Yellow eels were collected in two different ways: four specimens were bought from an eel farm (22u44950.199N 120u32943.099E) and consent/permission was obtained from an eel farm owner in Pingtung County, while two specimens were caught upstream of the Laomei Stream (25u15925.999N 121u32911.499E) in northern Taiwan
Rh1d was only expressed in older eels, while SWS2 was not detected at any stage. These findings suggest that A. marmorata may require Rh1f and Rh2 opsin during upstream migration, and this observation is consistent with the MSP data
Summary
Fish habitats are highly diverse, ranging from the deep sea to the upper reaches of freshwater rivers in the mountains, and from the tropics to the Arctic; the photic conditions in these environments vary greatly in terms of turbidity, color, and brightness. The spectral sensitivities of rod and cone photoreceptors of deep-water fishes adapt to match the blue-shifted spectral bandwidth of ambient light [3,4]. In order to adapt to photo-environment changes from freshwater to seawater, the salmon express blue opsin insteand of UV gene(s) in the single cone [11]. The spectral sensitivities of rod photoreceptors in two catadromous freshwater eels, European and American eels, are modified by alterations in chromophore and opsin gene usage during ontogenesis and spawning migration; it should be noted that spectral tuning via opsin shift (rather than A1/A2 shifts) was first observed in eels [12,13,14,15,16]
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