Simultaneous Expression of UV and Violet SWS1 Opsins Expands the Visual Palette in a Group of Freshwater Snakes.

Snakes are known to express a rod visual opsin and two cone opsins, only (SWS1, LWS), a reduced palette resulting from their supposedly fossorial origins. Dipsadid snakes in the genus Helicops are highly visual predators that successfully invaded freshwater habitats from ancestral terrestrial-only habitats. Here, we report the first case of multiple SWS1 visual pigments in a vertebrate, simultaneously expressed in different photoreceptors and conferring both UV and violet sensitivity to Helicops snakes. Molecular analysis and in vitro expression confirmed the presence of two functional SWS1 opsins, likely the result of recent gene duplication. Evolutionary analyses indicate that each sws1 variant has undergone different evolutionary paths with strong purifying selection acting on the UV-sensitive copy and dN/dS ∼1 on the violet-sensitive copy. Site-directed mutagenesis points to the functional role of a single amino acid substitution, Phe86Val, in the large spectral shift between UV and violet opsins. In addition, higher densities of photoreceptors and SWS1 cones in the ventral retina suggest improved acuity in the upper visual field possibly correlated with visually guided behaviors. The expanded visual opsin repertoire and specialized retinal architecture are likely to improve photon uptake in underwater and terrestrial environments, and provide the neural substrate for a gain in chromatic discrimination, potentially conferring unique color vision in the UV-violet range. Our findings highlight the innovative solutions undertaken by a highly specialized lineage to tackle the challenges imposed by the invasion of novel photic environments and the extraordinary diversity of evolutionary trajectories taken by visual opsin-based perception in vertebrates.

Simultaneous expression of UV and violet SWS1 opsins expands the visual palette in a group of freshwater snakes

Snakes are known to express a rod visual opsin and two cone opsins, only (SWS1, LWS), a reduced palette resulting from their supposedly fossorial origins. Dipsadid snakes in the genus Helicops are highly visual predators that successfully invaded freshwater habitats from ancestral terrestrial-only habitats. Here, we report the first case of multiple SWS1 visual pigments in a vertebrate, simultaneously expressed in different photoreceptors and conferring both UV and violet sensitivity to Helicops snakes. Molecular analysis and in vitro expression confirmed the presence of two functional SWS1 opsins, likely the result of recent gene duplication. Evolutionary analyses indicate that each sws1 variant has undergone different evolutionary paths with strong purifying selection acting on the UV-sensitive copy and dN/dS ∼1 on the violet-sensitive copy. Site-directed mutagenesis points to the functional role of a single amino acid substitution, Phe86Val, in the large spectral shift between UV and violet opsins. In addition, higher densities of photoreceptors and SWS1 cones in the ventral retina suggest improved acuity in the upper visual field possibly correlated with visually guided behaviors. The expanded visual opsin repertoire and specialized retinal architecture are likely to improve photon uptake in underwater and terrestrial environments, and provide the neural substrate for a gain in chromatic discrimination, potentially conferring unique color vision in the UV–violet range. Our findings highlight the innovative solutions undertaken by a highly specialized lineage to tackle the challenges imposed by the invasion of novel photic environments and the extraordinary diversity of evolutionary trajectories taken by visual opsin-based perception in vertebrates.

Lens transmittance shapes ultraviolet sensitivity in the eyes of frogs from diverse ecological and phylogenetic backgrounds.

The amount of short wavelength (ultraviolet (UV), violet and blue) light that reaches the retina depends on the transmittance properties of the ocular media, especially the lens, and varies greatly across species in all vertebrate groups studied previously. We measured the lens transmittance in 32 anuran amphibians with different habits, geographical distributions and phylogenetic positions and used them together with eye size and pupil shape to evaluate the relationship with diel activity pattern, elevation and latitude. We found an unusually high lens UV transmittance in the most basal species, and a cut-off range that extends into the visible spectrum for the rest of the sample, with lenses even absorbing violet light in some diurnal species. However, other diurnal frogs had lenses that transmit UV light like the nocturnal species. This unclear pattern in the segregation of ocular media transmittance and diel activity is shared with other vertebrates and is consistent with the absence of significant correlations in our statistical analyses. Although we did not detect a significant phylogenetic effect, closely related species tend to have similar transmittances, irrespective of whether they share the same diel pattern or not, suggesting that anuran ocular media transmittance properties might be related to phylogeny.

A dune with a view: the eyes of a neotropical fossorial lizard.

BACKGROUND: Lizards are excellent models to study the adaptations of the visual system to different scenarios, and surface-dwelling representatives have been relatively well studied. In contrast, very little is known about the functional anatomy of the eyes of fossorial lineages, and properties such as the light transmission by the ocular media have never been characterised in any fossorial species. Some lizards in the family Gymnophthalmidae endemic to the sand dunes of North Eastern Brazil have evolved sand-burrowing habits and nocturnal activity. Lizards in the sister group to Gymnophthalmidae, the family Teiidae, have decidedly diurnal and epigeal lifestyles, yet they are equally poorly known in terms of visual systems. We focussed on the eye anatomy, photoreceptor morphology and light transmittance properties of the ocular media and oil droplets in the gymnophthalmid Calyptommatus nicterus and the teiid Ameivula ocellifera. RESULTS: The general organisation of the eyes of the fossorial nocturnal C. nicterus and the epigeal diurnal A. ocellifera is remarkably similar. The lenses are highly transmissive to light well into the ultraviolet part of the spectrum. The photoreceptors have the typical cone morphology, with narrow short outer segments and oil droplets. The main difference between the two species is that C. nicterus has only colourless oil droplets, whereas A. ocellifera has colourless as well as green-yellow and pale-orange droplets. CONCLUSIONS: Our results challenge the assumption that fossorial lizards undergo loss of visual function, a claim that is usually guided by the reduced size and external morphology of their eyes. In the case of C. nicterus, the visual system is well suited for vision in bright light and shows specialisations that improve sensitivity in dim light, suggesting that they might perform some visually-guided behaviour above the surface at the beginning or the end of their daily activity period, when light levels are relatively high in their open dunes habitat. This work highlights how studies on the functional anatomy of sensory systems can provide insights into the habits of secretive species.

Reconstructing reef fish communities using fish otoliths in coral reef sediments.

Little is known about long-term changes in coral reef fish communities. Here we present a new technique that leverages fish otoliths in reef sediments to reconstruct coral reef fish communities. We found over 5,400 otoliths in 169 modern and mid-Holocene bulk samples from Caribbean Panama and Dominican Republic mid-Holocene and modern reefs, demonstrating otoliths are abundant in reef sediments. With a specially-built reference collection, we were able to assign over 4,400 otoliths to one of 56 taxa (35 families) though mostly at genus and family level. Many otoliths were from juvenile fishes for which identification is challenging. Richness (by rarefaction) of otolith assemblages was slightly higher in modern than mid-Holocene reefs, but further analyses are required to elucidate the underlying causes. We compared the living fish communities, sampled using icthyocide, with the sediment otolith assemblages on four reefs finding the otolith assemblages faithfully capture the general composition of the living fish communities. Radiocarbon dating performed directly on the otoliths suggests that relatively little mixing of sediment layers particularly on actively accreting branching coral reefs. All otolith assemblages were strongly dominated by small, fast-turnover fish taxa and juvenile individuals, and our exploration on taxonomy, functional ecology and taphonomy lead us to the conclusion that intense predation is likely the most important process for otolith accumulation in reef sediments. We conclude that otolith assemblages in modern and fossil reef sediments can provide a powerful tool to explore ecological changes in reef fish communities over time and space.

Variable vision in variable environments: the visual system of an invasive cichlid (Cichla monoculus) in Lake Gatun, Panama.

An adaptive visual system is essential for organisms inhabiting new or changing light environments. The Panama Canal exhibits such variable environments owing to its anthropogenic origin and current human activities. Within the Panama Canal, Lake Gatun harbors several exotic fish species including the invasive peacock bass (Cichla monoculus), a predatory Amazonian cichlid. In this research, through spectral measurements and molecular and physiological experiments, we studied the visual system of C. monoculus and its adaptive capabilities. Our results suggest that (1) Lake Gatun is a highly variable environment, where light transmission changes throughout the canal waterway, and that (2) C. monoculus has several visual adaptations suited for this red-shifted light environment. Cichla monoculus filters short wavelengths (∼400 nm) from the environment through its ocular media and tunes its visual sensitivities to the available light through opsin gene expression. More importantly, based on shifts in spectral sensitivities of photoreceptors alone, and on transcriptome analysis, C. monoculus exhibits extreme intraspecific variation in the use of vitamin A1/A2 chromophore in their photoreceptors. Fish living in turbid water had higher proportions of vitamin A2, shifting sensitivities to longer wavelengths, than fish living in clear water. Furthermore, we also found variation in retinal transcriptomes, where fish from turbid and clear waters exhibited differentially expressed genes that vary greatly in their function. We suggest that this phenotypic plasticity has been key in the invasion success of C. monoculus.