Neoteny in visual system development of the spotted unicornfish,<i>Naso brevirostris</i>(Acanthuridae)

Tettamanti, Valerio; Busserolles, Fanny de; Lecchini, David; Marshall, Justin; Cortesi, Fabio

doi:10.1101/691774

Cited by 8 publications

(13 citation statements)

References 100 publications

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“…Analyzing opsin expression levels in the larval and/or early-juvenile anemonefish retina may also reveal whether the shorter-wavelength-sensitive SWS1α is expressed during earlier life stages and whether an ontogenetic shift from SWS1α to SWS1β coincides with change(s) in light environment, particularly during the settlement stage when pelagic larvae return to the reef to seek a host anemone. Ontogenetic changes in cone opsin expression levels as a response to change in habitat have been reported in other reef fishes, for example, spotted unicornfish ( Naso brevirostris ) ( Tettamanti et al 2019 ) and dusky dottyback ( Pseudochromis fuscus ) ( Cortesi et al 2016 ). Alternatively, the SWS1α opsin may be expressed in other tissues and/or organs, where animal opsins have been demonstrated to serve other sensory modalities, for example, nonimage forming vision, thermosensation, hearing (see review by Leung and Montell [2017] ), taste ( Leung et al 2020 ), or potentially a nonsensory related function such as early eye and cranial development (see Novales Flamarique et al 2021 ).…”

Section: Discussionmentioning

confidence: 80%

Molecular Evolution of Ultraviolet Visual Opsins and Spectral Tuning of Photoreceptors in Anemonefishes (Amphiprioninae)

Mitchell

Cheney

Lührmann

et al. 2021

Genome Biology and Evolution

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Many animals including birds, reptiles, insects, and teleost fishes can see ultraviolet (UV) light (shorter than 400 nm), which has functional importance for foraging and communication. For coral reef fishes, shallow reef environments transmit a broad spectrum of light, rich in UV, driving the evolution of diverse spectral sensitivities. However, the identities and sites of the specific visual genes that underly vision in reef fishes remain elusive and are useful in determining how evolution has tuned vision to suit life on the reef. We investigated the visual systems of 11 anemonefish (Amphiprioninae) species, specifically probing for the molecular pathways that facilitate UV-sensitivity. Searching the genomes of anemonefishes, we identified a total of eight functional opsin genes from all five vertebrate visual opsin subfamilies. We found rare instances of teleost UV-sensitive SWS1 opsin gene duplications, that produced two functionally-coding paralogs (SWS1α and SWS1β) and a pseudogene. We also found separate green sensitive RH2A opsin gene duplicates not yet reported in the family Pomacentridae. Transcriptome analysis revealed false clown anemonefish (Amphiprion ocellaris) expressed one rod opsin (RH1) and six cone opsins (SWS1β, SWS2B, RH2B, RH2A-1, RH2A-2, LWS) in the retina. Fluorescent in-situ hybridisation highlighted the (co-)expression of SWS1β with SWS2B in single cones, and either RH2B, RH2A, or RH2A together with LWS in different members of double cone photoreceptors (two single cones fused together). Our study provides the first in-depth characterisation of visual opsin genes found in anemonefishes and provides a useful basis for the further study of UV-vision in reef fishes.

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Section: Discussionmentioning

confidence: 80%

Molecular Evolution of Ultraviolet Visual Opsins and Spectral Tuning of Photoreceptors in Anemonefishes (Amphiprioninae)

Mitchell

Cheney

Lührmann

et al. 2021

Genome Biology and Evolution

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“…).Analysing opsin expression levels in the larval and/or early-juvenile anemonefish retina may also reveal whether the shorter-wavelength sensitive SWS1α is expressed during earlier life stages, and whether an ontogenetic shift from SWS1α to SWS1β occurs as a response to change(s) in light environment, particularly during the settlement stage when pelagic larvae return to the reef to seek a host anemone. Ontogenetic changes in cone opsin expression levels as a response to change in habitat have been reported in other reef fishes including the spotted unicornfish (Naso brevirostris)(Tettamanti et al 2019) and dusky dottyback (P. fuscus). Alternatively, the SWS1α opsin may be expressed in other tissues and/or organs, where animal opsins have been demonstrated to serve other sensory modalities including non-image forming vision, thermosensation, hearing (see review by…”

mentioning

confidence: 73%

Seeing Nemo: molecular evolution of ultraviolet visual opsins and spectral tuning of photoreceptors in anemonefishes (Amphiprioninae)

Mitchell

Cheney

Chung

et al. 2020

Preprint

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Many animals can see short-wavelength or ultraviolet (UV) light (shorter than 400 nm) undetectable to human vision. UV vision may have functional importance in many taxa including for foraging and communication in birds, reptiles, insects and teleost fishes.Shallow coral reefs transmit a broad spectrum of light and are rich in UV; driving the evolution of diverse spectral sensitivities in teleost reef fishes, including UV-sensitivity.However, the identities and sites of the specific visual genes that underly vision in reef fishes remain elusive and are useful in determining how molecular evolution has tuned vision to meet the ecological demands of life on the reef. We investigated the visual systems of eleven anemonefish (Amphiprioninae) species, specifically probing for the molecular pathways that facilitate UV-sensitivity. Searching the genomes of anemonefishes, we identified a total of seven functional visual genes from all five vertebrate opsin gene subfamilies. We found rare instances of UV-sensitive SWS1 opsin gene duplications, that produced two functional paralogs (SWS1α and SWS1β) and a pseudogene. We also found separate RH2A opsin gene duplicates which has not been previously reported in the family Pomacentridae. Finally, we report on the visual opsin gene expression levels measured in the adult retina of the false clown anemonefish (Amphiprion ocellaris), and their photoreceptor spectral sensitivities measured using microspectrophotometry.

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“…This has shown that for example the RH2A paralogs found in Amazonian cichlids have a shared ancestry with the RH2A paralogs in African and Neotropical cichlids (Escobar-Camacho et al, 2017). Also, in the spotted unicornfish, Naso brevirostris, removing the converted regions recovered the sister relationship between its RH2A and RH2B copies (Tettamanti et al, 2019). In general, gene conversion appears to be an important evolutionary mechanism for visual opsins [e.g., for SWS2 (Cortesi et al, 2015), and LWS (Cortesi et al, 2021;Escobar-Camacho et al, 2020;Sandkam et al, 2017)], that quite possibly assists in keeping their function restricted to a certain spectral-sensitivity range.…”

Section: Resultsmentioning

confidence: 98%

“…The transcriptomic reads were then mapped again against each species-specific reference dataset with the Lowest Sensitivity settings. The number of reads that mapped to each copy were then used to calculate the proportion (in %) of expression of each opsin type from the total cone opsin expression as per de Busserolles et al, 2017 andTettamanti et al, 2019.…”

Section: Transcriptome Analysismentioning

confidence: 99%

Multiple ancestral and a plethora of recent gene duplications during the evolution of the green sensitive opsin genes (RH2) in teleost fishes

Musilová

Cortesi

2021

Preprint

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Vertebrates have four visual cone opsin classes that, together with a light-sensitive chromophore, provide sensitivity from the ultraviolet to the red wavelengths of light. The rhodopsin-like 2 (RH2) opsin is sensitive to the centre blue-green part of the spectrum, which is the most prevalent light underwater. While various vertebrate groups such as mammals and sharks have lost the RH2 gene, in teleost fishes this opsin has continued to proliferate. By investigating the genomes of 115 teleost species, we find that RH2 shows an extremely dynamic evolutionary history with repeated gene duplications, gene losses and gene conversion affecting entire orders, families and species. At least four ancestral duplications provided the substrate for todays RH2 diversity with duplications occurring in the common ancestors of Clupeocephala, Neoteleostei, and Acanthopterygii. Following these events, RH2 has continued to duplicate both in tandem and during lineage specific genome duplications. However, it has also been lost many times over so that in the genomes of extant teleosts, we find between zero to eight RH2 copies. Using retinal transcriptomes in a phylogenetic representative dataset of 30 species, we show that RH2 is expressed as the dominant green-sensitive opsin in almost all fish lineages. The exceptions are the Osteoglossomorpha (bony tongues and mooneyes) and several characin species that have lost RH2, and tarpons, other characins and gobies which do not or only lowly express the gene. These fishes instead express a green-shifted long-wavelength-sensitive LWS opsin. Our study highlights the strength of using modern genomic tools within a comparative framework to elucidate the detailed evolutionary history of gene families.

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Neoteny in visual system development of the spotted unicornfish,Naso brevirostris(Acanthuridae)

Abstract: 15

Cited by 8 publications

References 100 publications

Molecular Evolution of Ultraviolet Visual Opsins and Spectral Tuning of Photoreceptors in Anemonefishes (Amphiprioninae)

Molecular Evolution of Ultraviolet Visual Opsins and Spectral Tuning of Photoreceptors in Anemonefishes (Amphiprioninae)

Seeing Nemo: molecular evolution of ultraviolet visual opsins and spectral tuning of photoreceptors in anemonefishes (Amphiprioninae)

Multiple ancestral and a plethora of recent gene duplications during the evolution of the green sensitive opsin genes (RH2) in teleost fishes

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