The Cone Opsin Repertoire of Osteoglossomorph Fishes: Gene Loss in Mormyrid Electric Fish and a Long Wavelength-Sensitive Cone Opsin That Survived 3R

Liu, Dawei; Wang, Feng‐Yu; Lin, Jinn-Jy; Thompson, Ammon; Lu, Ying; Vo, Derek; Yan, Hong; Zakon, Harold H.

doi:10.1093/molbev/msy241

Cited by 20 publications

(29 citation statements)

References 55 publications

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“…Since the vertebrate common ancestor, some teleost lineages have gained additional opsin copies through duplications so that they now have more opsins than other vertebrates (Davies et al, 2012;Musilova et al, 2019a;Rennison et al, 2012). These extra copies are sometimes the result of the teleost-specific whole genome duplication (Escobar-Camacho et al, 2019a;Liu et al, 2016;Liu et al, 2019;Morrow et al, 2011), but can also result from duplications specific to particular lineages, e.g. the tandem duplications of the SWS2 and RH2 genes that are shared across Actinopterygians Parry et al, 2005).…”

Section: Gene Duplications and Lossesmentioning

confidence: 99%

Seeing the rainbow: mechanisms underlying spectral sensitivity in teleost fishes

Carleton

Escobar‐Camacho

Stieb

et al. 2020

Journal of Experimental Biology

111

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Among vertebrates, teleost eye diversity exceeds that found in all other groups. Their spectral sensitivities range from ultraviolet to red, and the number of visual pigments varies from 1 to over 40. This variation is correlated with the different ecologies and life histories of fish species, including their variable aquatic habitats: murky lakes, clear oceans, deep seas and turbulent rivers. These ecotopes often change with the season, but fish may also migrate between ecotopes diurnally, seasonally or ontogenetically. To survive in these variable light habitats, fish visual systems have evolved a suite of mechanisms that modulate spectral sensitivities on a range of timescales. These mechanisms include: (1) optical media that filter light, (2) variations in photoreceptor type and size to vary absorbance and sensitivity, and (3) changes in photoreceptor visual pigments to optimize peak sensitivity. The visual pigment changes can result from changes in chromophore or changes to the opsin. Opsin variation results from changes in opsin sequence, opsin expression or co-expression, and opsin gene duplications and losses. Here, we review visual diversity in a number of teleost groups where the structural and molecular mechanisms underlying their spectral sensitivities have been relatively well determined. Although we document considerable variability, this alone does not imply functional difference per se. We therefore highlight the need for more studies that examine species with known sensitivity differences, emphasizing behavioral experiments to test whether such differences actually matter in the execution of visual tasks that are relevant to the fish.

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Section: Gene Duplications and Lossesmentioning

confidence: 99%

Seeing the rainbow: mechanisms underlying spectral sensitivity in teleost fishes

Carleton

Escobar‐Camacho

Stieb

et al. 2020

Journal of Experimental Biology

111

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“…Third, the choice of outgroup (parietopsin or pinopsin) does not affect the position of the LWS2 gene. Together, these analyses suggest either (1) the presence of an ancient gene duplication event of the LWS gene in the ancestor of teleost and holostean fishes (i.e., Neopterygii) which was retained only in the goby family, or (2) a teleost-specific event, possibly identical to that reported for characins and bony tongues [67], with a subsequent concerted goby-specific sequence diversification in exons 2, 3, and 5.…”

Section: Sensory Perception Genes: Visionmentioning

confidence: 62%

“…Second, the distant phylogenetic position is supported by trees based on individual exons, which indicate a low probability of a compromised phylogenetic signal, e.g., due to the partial gene conversion (see Additional file 3: Figure S2 for an exon-based tree). Three of four exons cluster at the same position as the whole gene, while the fourth exon (exon 4) cluster with the genes resulting from a more recent teleost-specific LWS duplication specific to Astyanax and Scleropages [67]. Third, the choice of outgroup (parietopsin or pinopsin) does not affect the position of the LWS2 gene.…”

Section: Sensory Perception Genes: Visionmentioning

confidence: 99%

The round goby genome provides insights into mechanisms that may facilitate biological invasions

et al. 2020

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Background: The invasive benthic round goby (Neogobius melanostomus) is the most successful temperate invasive fish and has spread in aquatic ecosystems on both sides of the Atlantic. Invasive species constitute powerful in situ experimental systems to study fast adaptation and directional selection on short ecological timescales and present promising case studies to understand factors involved the impressive ability of some species to colonize novel environments. We seize the unique opportunity presented by the round goby invasion to study genomic substrates potentially involved in colonization success. Results: We report a highly contiguous long-read-based genome and analyze gene families that we hypothesize to relate to the ability of these fish to deal with novel environments. The analyses provide novel insights from the large evolutionary scale to the small species-specific scale. We describe expansions in specific cytochrome P450 enzymes, a remarkably diverse innate immune system, an ancient duplication in red light vision accompanied by red skin fluorescence, evolutionary patterns of epigenetic regulators, and the presence of osmoregulatory genes that may have contributed to the round goby's capacity to invade cold and salty waters. A recurring theme across all analyzed gene families is gene expansions. Conclusions: The expanded innate immune system of round goby may potentially contribute to its ability to colonize novel areas. Since other gene families also feature copy number expansions in the round goby, and since other Gobiidae also feature fascinating environmental adaptations and are excellent colonizers, further long-read genome approaches across the goby family may reveal whether gene copy number expansions are more generally related to the ability to conquer new habitats in Gobiidae or in fish.

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“…The presence of LWS2 opsins in both Osteoglossiformes and Characiformes suggests that LWS2-green sensitivity evolved in an early ancestor dated after TGD but before the split of Osteoglossomorpha and Clupeocephala (around 240 MYA) (Hughes et al 2018). This implies that LWS2 opsins have been maintained in Osteoglossiformes and Characiformes for at least over 300 million years (Liu et al 2018), while they have been lost in several other teleosts. Indeed, there is evidence that most duplicated genes were lost in the first 60 million years after TGD (Inoue et al 2015).…”

Section: Discussionmentioning

confidence: 99%

Visual pigment evolution in Characiformes: the dynamic interplay of teleost whole-genome duplication, surviving opsins and spectral tuning

Escobar‐Camacho

Carleton

Narain

et al. 2019

Preprint

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33Vision represents an excellent model for studying adaptation, given the genotype-to-34 phenotype-map that has been characterized in a number of taxa. Fish possess a diverse 35 range of visual sensitivities and adaptations to underwater light making them an 36 excellent group to study visual system evolution. In particular, some speciose but 37 understudied lineages can provide a unique opportunity to better understand aspects of 38 visual system evolution such as opsin gene duplication and neofunctionalization. In this 39 study, we characterized the visual system of Neotropical Characiformes, which is the 40 result of several spectral tuning mechanisms acting in concert including gene 41 duplications and losses, gene conversion, opsin amino acid sequence and expression 42 variation, and A 1 /A 2 -chromophore shifts. The Characiforms we studied utilize three cone 43 opsin classes (SWS2, RH2, LWS) and a rod opsin (RH1). However, the characiform's 44 entire opsin gene repertoire is a product of dynamic evolution by opsin gene loss 45 (SWS1, RH2) and duplication (LWS, RH1). The LWS-and RH1-duplicates originated 46 from a teleost specific whole-genome duplication as well as characiform-specific 47 duplication events. Both LWS-opsins exhibit gene conversion and, through substitutions 48 in key tuning sites, one of the LWS-paralogs has acquired spectral sensitivity to green 49 light. These sequence changes suggest reversion and parallel evolution of key tuning 50 sites. In addition, characiforms exhibited species-specific differences in opsin 51 expression. Finally, we found interspecific and intraspecific variation in the use of A 1 /A 2 -52 chromophores correlating with the light environment. These multiple mechanisms may 53 be a result of the highly diverse visual environments where Characiformes have evolved. 54 55 58 relates to the environment. Evolutionary studies of genes such as the ones involved in 59 the first steps of vision can provide valuable insights in the acquisition of new functions 60 and their adaptive significance. In vertebrates, vision starts when light reaches the retina61 and is detected by rod (night vision) or cone (diurnal vision) photoreceptors.62 Photoreceptors are packed with visual pigments that are composed of two components: 63 an opsin protein with seven α-helices enclosing a ligand-binding pocket, and a light-64 sensitive chromophore, 11-cis retinal (Bowmaker 2008; Yokoyama 2008). There can be 65 3 multiple cone types containing different visual pigments that absorb light maximally in 66 different parts of the wavelength spectrum. 67 68 There are four classes of cone pigments encoded by opsin genes among vertebrates: a 69 short-wave class (SWS1) sensitive to ultraviolet-violet light (350-400 nm), a second 70 short-wave class (SWS2) sensitive to violet-blue (410-490 nm), a middle-wave class 71 (RH2) sensitive to green (480-535 nm), and a middle-to long-wave class (LWS) 72 sensitive to the green and red spectral region (490-570 nm) (Bowmaker and Hunt 2006; 73 Bowmaker 2008). All four ...

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The Cone Opsin Repertoire of Osteoglossomorph Fishes: Gene Loss in Mormyrid Electric Fish and a Long Wavelength-Sensitive Cone Opsin That Survived 3R

Cited by 20 publications

References 55 publications

Seeing the rainbow: mechanisms underlying spectral sensitivity in teleost fishes

Seeing the rainbow: mechanisms underlying spectral sensitivity in teleost fishes

The round goby genome provides insights into mechanisms that may facilitate biological invasions

Visual pigment evolution in Characiformes: the dynamic interplay of teleost whole-genome duplication, surviving opsins and spectral tuning

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