The ability of vertebrates to occupy diverse niches has been linked to the spectral properties of rhodopsin, conferring rod-based vision in low-light conditions. More recent insights have come from nonspectral kinetics, including the retinal release rate of the active state of rhodopsin, a key aspect of scotopic vision that shows strong associations with light environments in diverse taxa. We examined the retinal release rates in resurrected proteins across early vertebrates and show that the earliest forms were characterized by much faster rates of retinal release than more recent ancestors. We also show that scotopic vision at the origin of tetrapods is a derived state that arose via at least 4 major shifts in retinal release rate. Our results suggest that early rhodopsin had a function intermediate to that of modern rod and cone pigments and that its well-developed adaptation to low light is a relatively recent innovation since the origin of tetrapods.

The visual ability and associated photic niche of early mammals is debated. The theory that ancestral mammals were nocturnal is supported by diverse adaptations. However, others argue that photopigment repertoires of early mammals are more consistent with a crepuscular niche, and support for this also comes from inferred spectral tuning of middle/long wavelength-sensitive (M/LWS) opsin sequences. Functional studies have suggested that the M/LWS pigment in the ancestor of Mammalia was either red- or green-sensitive; however, these were based on outdated phylogenies with key lineages omitted. By performing the most detailed study to date of middle/long-wave mammalian color vision, we provide the first experimental evidence that the M/LWS pigment of amniotes underwent a 9-nm spectral shift towards shorter wavelengths in the Mammalia ancestor, exceeding predictions from known critical sites. Our results suggest early mammals were yellow-sensitive, possibly representing an adaptive trade-off for both crepuscular (twilight) and nocturnal (moonlight) niches.

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.

Ultraviolet (UV)-sensitive visual pigment and its corresponding ability for UV vision was retained in early mammals from their common ancestry with sauropsids. Subsequently, UV-sensitive pigments, encoded by the short wavelength-sensitive 1 (SWS1) opsin gene, were converted to violet sensitivity or have lost function in multiple lineages during the diversification of mammals. However, many mammalian species, including most bats, are suggested to retain a UV-sensitive pigment. Notably, some cave-dwelling fruit bats and high duty cycle echolocating bats have lost their SWS1 genes, which are proposed to be due to their roosting ecology and as a sensory trade-off between vision and echolocation, respectively. Here, we sequenced SWS1 genes from ecologically diverse bats and found that this gene is also non-functional in both common vampire bat (Desmodus rotundus) and white-winged vampire bat (Diaemus youngi). Apart from species with pesudogenes, our evolutionary and functional studies demonstrate that the SWS1 pigment of bats are UV-sensitive and well-conserved since their common ancestor, suggesting an important role across major ecological types. Given the constrained function of SWS1 pigments in these bats, why some other species, such as vampire bats, have lost this gene is even more interesting and needs further investigation.

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