Convergent Phenotypic Evolution of Rhodopsin for Dim-Light Sensing across Deep-Diving Vertebrates

Abstract

Rhodopsin comprises an opsin attached to a retinal chromophore, and is the only visual pigment conferring dim-light vision in vertebrates. On activation by photons, the retinal group becomes detached from the opsin, which is then inactive until it is recharged. Of all vertebrate species, those that dive face unique visual challenges, experiencing rapid decreases in light level and hunting in near darkness. Here we combine sequence analyses with functional assays to show that the rhodopsin pigments of four divergent lineages of deep diving vertebrates have undergone convergent increases in their retinal release rate. We compare gene sequences and detect parallel amino acids between penguins and diving mammals, and perform mutagenesis to show that a single critical residue fully explains the observed increases in retinal release rate in both the emperor penguin and beaked whale. At the same time, we find that other shared sites have no significant effect on retinal release, implying that convergence does not always signify adaptive significance. We propose that accelerated retinal release confers rapid rhodopsin recharging, enabling the visual systems of diving species to adjust quickly to changing light levels as they descend through the water column. This contrasts with nocturnal species, where adaptation to darkness has been attributed to slower retinal release rates.

New Insight Into Visual Adaptation in the Mudskipper Cornea: From Morphology to the Cornea-Related COL8A2 Gene

“…Our results revealed a significant correlation between COL8A2 evolution and maximum diving depth (Figure 8), which indicated selection on genes imposed by diving depth. This conclusion is consistent with the finding of a previous study on RH1 that water depth adaptation has a significant impact on the evolution of vision (Sugawara et al, 2005;Dungan et al, 2016;Xia et al, 2021). In addition, the analysis of differential selection further confirmed that COL8A2 was subject to differential selection among different aquatic environments (Table 2 and Figure 7).…”

“…For example, the visual system of the Mariana lionfish (Pseudoliparis swirei) has been severely degraded due to its adaptation to darkness (Jiang et al, 2019). In many deep-diving groups, the rhodopsin RH1 gene, which mainly mediates scotopic vision (Lythgoe and Dartnall, 1970;Yokoyama et al, 2008), has not only evolved rapidly but also mutated in amino acid (AA) sequences with similar functional properties, resulting in adaptive evolution of protein functions (Xia et al, 2021). In addition, in the color vision system, cone cells and related genes (SWS1, LWS, etc.)…”

Accelerated evolution of dim-light vision-related arrestin in deep-diving amniotes

“…The divergent evolution of cetacean SAG has been suggested to be associated with their deep diving, and a key substitution (Q69R) has been verified for having a role in increasing the formation of rhodopsin Meta II (Chiu, 2019). In addition to their specialized rhodopsins (significantly faster retinal release rates and possibly faster dark adaptation; Xia et al, 2021;Dungan and Chang, 2022), SAG could be another gene contributing to the acute dim-light vision of deep-diving species, by regulating Meta II formation and thus possibly accelerating the rod dark adaptation (Frederiksen et al, 2016). Since the key substitution found in whales (Chiu, 2019) is not shared with penguins and seals (Supplementary Figure S2), their potential fast adaptation to deep-diving visual perception via rod arrestin might be due to different molecular mechanisms.…”

“…For cetaceans, since ARR3 pseudogenes were found in some species (Supplementary Figure S1), and they have experienced widespread losses of opsin and some other visual genes (Meredith et al, 2013;Springer et al, 2016;McGowen et al, 2020), the significantly higher ω value for the ARR3 sequences is unlikely due to adaptation to color vision. Apart from phenotypic evolution of rhodopsin in deep-diving vertebrates (Xia et al, 2021), rhodopsin function has also been measured for the ancestor of Archosaur, which was shown to have a similar transducin activation rate as that of bovine rhodopsin (Chang et al, 2002). We therefore carried out evolutionary analyses of the archosaur SAG and ARR3 sequences to determine whether their visual arrestins experienced adaptive evolution.…”

“…Some of these species, such as beaked whale and elephant seal (Robinson et al, 2012;Berrow et al, 2018), can dive deeper than 1,000 m below sea level, into the aphotic zone (Warrant and Locket, 2004), for predation. Interestingly, the dim-light visual pigment rhodopsin from these species have been reported to possess key phenotypic substitutions that allow fast retinal release rates, which could be adaptive for rapid dim-light sensing needed during diving (Xia et al, 2021). Both adaptive and divergent evolution of SAG has been reported in birds, reptiles and mammals (Wu et al, 2016(Wu et al, , 2018Schott et al, 2019), including whales (Chiu, 2019;McGowen et al, 2020), however, the role of rod arrestin in dim-light adaptation in these deep-diving taxa has not been fully resolved.…”