Functional trade-offs and environmental variation shaped ancient trajectories in the evolution of dim-light vision
Trade-offs between protein stability and activity can restrict access to evolutionary trajectories, but widespread epistasis may facilitate indirect routes to adaptation. This may be enhanced by natural environmental variation, but in multicellular organisms this process is poorly understood. We inv...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2018-10-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/35957 |
| _version_ | 1811180462376222720 |
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| author | Gianni M Castiglione Belinda SW Chang |
| author_facet | Gianni M Castiglione Belinda SW Chang |
| author_sort | Gianni M Castiglione |
| collection | DOAJ |
| description | Trade-offs between protein stability and activity can restrict access to evolutionary trajectories, but widespread epistasis may facilitate indirect routes to adaptation. This may be enhanced by natural environmental variation, but in multicellular organisms this process is poorly understood. We investigated a paradoxical trajectory taken during the evolution of tetrapod dim-light vision, where in the rod visual pigment rhodopsin, E122 was fixed 350 million years ago, a residue associated with increased active-state (MII) stability but greatly diminished rod photosensitivity. Here, we demonstrate that high MII stability could have likely evolved without E122, but instead, selection appears to have entrenched E122 in tetrapods via epistatic interactions with nearby coevolving sites. In fishes by contrast, selection may have exploited these epistatic effects to explore alternative trajectories, but via indirect routes with low MII stability. Our results suggest that within tetrapods, E122 and high MII stability cannot be sacrificed—not even for improvements to rod photosensitivity. |
| first_indexed | 2024-04-11T09:02:29Z |
| format | Article |
| id | doaj.art-2139e218d8f54a10b6eac83984b906b3 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:02:29Z |
| publishDate | 2018-10-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-2139e218d8f54a10b6eac83984b906b32022-12-22T04:32:43ZengeLife Sciences Publications LtdeLife2050-084X2018-10-01710.7554/eLife.35957Functional trade-offs and environmental variation shaped ancient trajectories in the evolution of dim-light visionGianni M Castiglione0https://orcid.org/0000-0002-0768-4236Belinda SW Chang1https://orcid.org/0000-0002-6525-4429Department of Cell and Systems Biology, University of Toronto, Toronto, Canada; Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, CanadaDepartment of Cell and Systems Biology, University of Toronto, Toronto, Canada; Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Canada; Centre for the Analysis of Genome Evolution and Function, University of Toronto, Toronto, CanadaTrade-offs between protein stability and activity can restrict access to evolutionary trajectories, but widespread epistasis may facilitate indirect routes to adaptation. This may be enhanced by natural environmental variation, but in multicellular organisms this process is poorly understood. We investigated a paradoxical trajectory taken during the evolution of tetrapod dim-light vision, where in the rod visual pigment rhodopsin, E122 was fixed 350 million years ago, a residue associated with increased active-state (MII) stability but greatly diminished rod photosensitivity. Here, we demonstrate that high MII stability could have likely evolved without E122, but instead, selection appears to have entrenched E122 in tetrapods via epistatic interactions with nearby coevolving sites. In fishes by contrast, selection may have exploited these epistatic effects to explore alternative trajectories, but via indirect routes with low MII stability. Our results suggest that within tetrapods, E122 and high MII stability cannot be sacrificed—not even for improvements to rod photosensitivity.https://elifesciences.org/articles/35957rhodopsinprotein evolutionintramolecular epistasis |
| spellingShingle | Gianni M Castiglione Belinda SW Chang Functional trade-offs and environmental variation shaped ancient trajectories in the evolution of dim-light vision eLife rhodopsin protein evolution intramolecular epistasis |
| title | Functional trade-offs and environmental variation shaped ancient trajectories in the evolution of dim-light vision |
| title_full | Functional trade-offs and environmental variation shaped ancient trajectories in the evolution of dim-light vision |
| title_fullStr | Functional trade-offs and environmental variation shaped ancient trajectories in the evolution of dim-light vision |
| title_full_unstemmed | Functional trade-offs and environmental variation shaped ancient trajectories in the evolution of dim-light vision |
| title_short | Functional trade-offs and environmental variation shaped ancient trajectories in the evolution of dim-light vision |
| title_sort | functional trade offs and environmental variation shaped ancient trajectories in the evolution of dim light vision |
| topic | rhodopsin protein evolution intramolecular epistasis |
| url | https://elifesciences.org/articles/35957 |
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