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

Abstract

Vision represents an excellent model for studying adaptation, given the genotype-tophenotype-map that has been characterized in a number of taxa. Fish possess a diverse range of visual sensitivities and adaptations to underwater light making them an excellent group to study visual system evolution. In particular, some speciose but understudied lineages can provide a unique opportunity to better understand aspects of visual system evolution such as opsin gene duplication and neofunctionalization. In this study, we characterized the visual system of Neotropical Characiformes, which is the result of several spectral tuning mechanisms acting in concert including gene duplications and losses, gene conversion, opsin amino acid sequence and expression variation, and A 1 /A 2 -chromophore shifts. The Characiforms we studied utilize three cone opsin classes (SWS2, RH2, LWS) and a rod opsin (RH1). However, the characiform's entire opsin gene repertoire is a product of dynamic evolution by opsin gene loss (SWS1, RH2) and duplication (LWS, RH1). The LWS-and RH1-duplicates originated from a teleost specific whole-genome duplication as well as characiform-specific duplication events. Both LWS-opsins exhibit gene conversion and, through substitutions in key tuning sites, one of the LWS-paralogs has acquired spectral sensitivity to green light. These sequence changes suggest reversion and parallel evolution of key tuning sites. In addition, characiforms exhibited species-specific differences in opsin expression. Finally, we found interspecific and intraspecific variation in the use of A 1 /A 2chromophores correlating with the light environment. These multiple mechanisms may be a result of the highly diverse visual environments where Characiformes have evolved.

Multiple ancestral duplications of the red-sensitive opsin gene (LWS) in teleost fishes and convergent spectral shifts to green vision in gobies

“…S1). We also find that Elopiformes (tarpons, ladyfish and relatives) in addition to the bony tongues and characins have retained the LWS2 copy, which emerged during 3R (Liu et al 2019; Escobar-Camacho et al 2020). Since LWS in non-teleost ray-finned fishes (bichir, sturgeon, gar and bowfin) is ancestral to the LWS1-3 paralogs found in modern teleosts, it is likely that all three duplicates originated in the teleost ancestor (Fig.…”

“…Interestingly, at their origin ~ 320 Mya, teleosts underwent a third round of whole-genome duplication (3R) (Ravi and Vankatesh 2018) and two extant opsin gene duplicates, one RH1 (Chen et al, 2018) and one LWS (Liu et al 2019), have been attributed to this event. The ancestral LWS 2 duplicate, has long been overlooked but has recently been described from bony tongues (Osteglossiformes) and characins (Characiformes) (Liu et al 2019; Escobar-Camacho et al 2020).…”

“…Most teleosts possess a single LWS copy ( LWS1 ) which is sensitive from the yellow to red spectrum (Carleton et al 2020), or they might have lost the gene altogether (Musilova et al 2019). LWS2 in extant species, but likely already in the ancestor shortly after its duplication, has shifted its spectral sensitivity to shorter, green-wavelengths as compared to LWS1 (Escobar-Camacho et al 2020). This is similar to the green shifted MWS/LWS duplicate in primates, which re-enabled trichromatic vision after the loss of RH2 in the mammalian ancestor (Carvalho et al, 2017).…”

“…This is similar to the green shifted MWS/LWS duplicate in primates, which re-enabled trichromatic vision after the loss of RH2 in the mammalian ancestor (Carvalho et al, 2017). Concurrently, both bony tongues and characins have either lost or have severely reduced the expression of the green-sensitive RH2 , suggesting that there is a trade-off between the overlap of opsin spectral sensitivities and the potential for evolutionary retention (Liu et al 2019; Escobar-Camacho et al 2020). Interestingly, a shift towards shorter spectral sensitivities can also be found in some more recent LWS1 duplicates but also between different alleles of the same gene (Seehausen et al 2008; Sandkam et al 2018).…”

Evolution, inactivation and loss of short wavelength‐sensitive opsin genes during the diversification of Neotropical cichlids

“…Conversely, freshwater fishes appear more likely to retain SWS1 if they inhabit shallower, clearwater environments where UV light is able to penetrate (Lin et al, 2018). Despite the utility of UV vision in many freshwater habitats, recent efforts to more extensively sample freshwater fish opsin diversity have suggested that loss of UV sensitivity may be more widespread (Escobar‐Camacho et al, 2019, 2020; Weadick et al, 2012). This may be a result of variation in the pattern and degree of attenuation of light across the visual spectrum in different freshwater habitats.…”