The Giant Mottled Eel, Anguilla marmorata, Uses Blue-Shifted Rod Photoreceptors during Upstream Migration

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.

Gene expression patterns of novel visual and non-visual opsin families in immature and mature Japanese eel males

“…The asterisk above each bar indicates significant differences according to the unpaired t test (*P < 0.05, **P < 0.01). Full-size DOI: 10.7717/peerj.8326/ fig-6 the giant mottled eel showed only one type of cone cell that detected a limited range of the optical spectrum (λmax) of 500 nm to 535 nm (Wang et al, 2014). Japanese eels are genetically and ecologically similar European eels; thus, it is presumed that they can For the artificially induced sexual maturation, hCG was intraperitoneally injected to the experimental fish group (n = 6) at a concentration of 1 IU/g body weight.…”

“…(European eel, A. anguilla and Japanese eel, A. japonica and giant mottled eel, A. marmorata) (Wang et al, 2014), Rh2 (European eel and giant mottled eel) (Cottrill et al, 2009), and SWS2 (European eel and giant mottled eel) (Wang et al, 2014). Molecular biological studies on photo sensitivities of these visual pigments and studies on the expression mechanism of photoreceptors according to ecological stages (glass eel, yellow eel, and silver eel) have been actively conducted.…”

Peer Review #1 of "Gene expression patterns of novel visual and non-visual opsin families in immature and mature Japanese eel males (v0.1)"

“…A study suggested that the European eel has two types of cone opsin subfamily, Rh2 (or MWS) and SWS2 cones, so it can distinguish colors (Cottrill et al, 2009). However, the giant mottled eel showed only one type of cone cell that detected a limited range of the optical spectrum (λmax) of 500 nm to 535 nm (Wang et al, 2014). Japanese eels are genetically and ecologically similar European eels; thus, it is presumed that they can recognize colors through two types of cone opsin.…”

“…To date, photoreceptor studies on Anguillid have identified fresh water rhodopsin (FWO) (Zhang et al, 2000), deep-sea rhodopsin (DSO) (Zhang et al, 2000), Rh1d (European eel, A. anguilla and Japanese eel, A. japonica and giant mottled eel, A. marmorata) (Wang et al, 2014), Rh2 (European eel and giant mottled eel) (Cottrill et al, 2009), and SWS2 (European eel and giant mottled eel) (Wang et al, 2014). Molecular biological studies on photo sensitivities of these visual pigments and studies on the expression mechanism of photoreceptors according to ecological stages (glass eel, yellow eel, and silver eel) have been actively conducted.…”

Multiple population structure of the giant eel Anguilla marmorata in Thua Thien Hue, Vietnam base on COI sequences

“…The species has a catadromous life-history strategy with distances from several hundred to thousands of kilometers when they were white grass eels from North ocean to South East Asian sea (Linh et al 2010). During migration between oceans and freshwater during special stages of the life cycle, strong environmental changes have shaped not only their physiological characteristics (Wang et al 2014) but also the genetic structure of eels (El-Nabi et al 2017). Besides, upheaval conditions of river management, water containment, over shing, and pollution may have in uenced the movement of upstream eels (Wasserman et al 2011) and downstream (Huyen and Phu 2015) led to the increase of population decline risk, on way back to oceans with mature and reproduction (Linh et al 2010).…”