Dataset Information

Evolutionary replacement of UV vision by violet vision in fish.

ABSTRACT: The vertebrate ancestor possessed ultraviolet (UV) vision and many species have retained it during evolution. Many other species switched to violet vision and, then again, some avian species switched back to UV vision. These UV and violet vision are mediated by short wavelength-sensitive (SWS1) pigments that absorb light maximally (lambda(max)) at approximately 360 and 390-440 nm, respectively. It is not well understood why and how these functional changes have occurred. Here, we cloned the pigment of scabbardfish (Lepidopus fitchi) with a lambda(max) of 423 nm, an example of violet-sensitive SWS1 pigment in fish. Mutagenesis experiments and quantum mechanical/molecular mechanical (QM/MM) computations show that the violet-sensitivity was achieved by the deletion of Phe-86 that converted the unprotonated Schiff base-linked 11-cis-retinal to a protonated form. The finding of a violet-sensitive SWS1 pigment in scabbardfish suggests that many other fish also have orthologous violet pigments. The isolation and comparison of such violet and UV pigments in fish living in different ecological habitats will open an unprecedented opportunity to elucidate not only the molecular basis of phenotypic adaptations, but also the genetics of UV and violet vision.

SUBMITTER: Tada T

PROVIDER: S-EPMC2765098 | biostudies-literature | 2009 Oct

REPOSITORIES: biostudies-literature

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Evolutionary replacement of UV vision by violet vision in fish.

Tada Takashi T Altun Ahmet A Yokoyama Shozo S

Proceedings of the National Academy of Sciences of the United States of America 20090928 41

The vertebrate ancestor possessed ultraviolet (UV) vision and many species have retained it during evolution. Many other species switched to violet vision and, then again, some avian species switched back to UV vision. These UV and violet vision are mediated by short wavelength-sensitive (SWS1) pigments that absorb light maximally (lambda(max)) at approximately 360 and 390-440 nm, respectively. It is not well understood why and how these functional changes have occurred. Here, we cloned the pigm ...[more]

PMID: 19805066

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Project description:BackgroundOne of the most striking features of avian vision is the variation in spectral sensitivity of the short wavelength sensitive (SWS1) opsins, which can be divided into two sub-types: violet- and UV- sensitive (VS & UVS). In birds, UVS has been found in both passerines and parrots, groups that were recently shown to be sister orders. While all parrots are thought to be UVS, recent evidence suggests some passerine lineages may also be VS. The great bowerbird (Chlamydera nuchalis) is a passerine notable for its courtship behaviours in which males build and decorate elaborate bower structures.ResultsThe great bowerbird SWS1 sequence possesses an unusual residue combination at known spectral tuning sites that has not been previously investigated in mutagenesis experiments. In this study, the SWS1 opsin of C. nuchalis was expressed along with a series of spectral tuning mutants and ancestral passerine SWS1 pigments, allowing us to investigate spectral tuning mechanisms and explore the evolution of UV/violet sensitivity in early passerines and parrots. The expressed C. nuchalis SWS1 opsin was found to be a VS pigment, with a λmax of 403 nm. Bowerbird SWS1 mutants C86F, S90C, and C86S/S90C all shifted λmax into the UV, whereas C86S had no effect. Experimentally recreated ancestral passerine and parrot/passerine SWS1 pigments were both found to be VS, indicating that UV sensitivity evolved independently in passerines and parrots from a VS ancestor.ConclusionsOur mutagenesis studies indicate that spectral tuning in C. nuchalis is mediated by mechanisms similar to those of other birds. Interestingly, our ancestral sequence reconstructions of SWS1 in landbird evolution suggest multiple transitions from VS to UVS, but no instances of the reverse. Our results not only provide a more precise prediction of where these spectral sensitivity shifts occurred, but also confirm the hypothesis that birds are an unusual exception among vertebrates where some descendants re-evolved UVS from a violet type ancestor. The re-evolution of UVS from a VS type pigment has not previously been predicted elsewhere in the vertebrate phylogeny.

Project description:Many species of fish rely on their visual systems to interact with conspecifics and these interactions can lead to collective behavior. Individual-based models have been used to predict collective interactions; however, these models generally make simplistic assumptions about the sensory systems that are applied without proper empirical testing to different species. This could limit our ability to predict (and test empirically) collective behavior in species with very different sensory requirements. In this study, we characterized components of the visual system in two species of cyprinid fish known to engage in visually dependent collective interactions (zebrafish Danio rerio and golden shiner Notemigonus crysoleucas) and derived quantitative predictions about the positioning of individuals within schools. We found that both species had relatively narrow binocular and blind fields and wide visual coverage. However, golden shiners had more visual coverage in the vertical plane (binocular field extending behind the head) and higher visual acuity than zebrafish. The centers of acute vision (areae) of both species projected in the fronto-dorsal region of the visual field, but those of the zebrafish projected more dorsally than those of the golden shiner. Based on this visual sensory information, we predicted that: (a) predator detection time could be increased by >1,000% in zebrafish and >100% in golden shiners with an increase in nearest neighbor distance, (b) zebrafish schools would have a higher roughness value (surface area/volume ratio) than those of golden shiners, (c) and that nearest neighbor distance would vary from 8 to 20 cm to visually resolve conspecific striping patterns in both species. Overall, considering between-species differences in the sensory system of species exhibiting collective behavior could change the predictions about the positioning of individuals in the group as well as the shape of the school, which can have implications for group cohesion. We suggest that more effort should be invested in assessing the role of the sensory system in shaping local interactions driving collective behavior.

Dataset Information

Evolutionary replacement of UV vision by violet vision in fish.

Publications

Evolutionary replacement of UV vision by violet vision in fish.

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