Functional trade-offs and environmental variation shaped ancient trajectories in the evolution of dim-light vision

• Published in: eLife Vol. 7
• Main Authors: Castiglione, Gianni M, Chang, Belinda Sw
• Format: Journal Article
• Language: English
• Published: England eLife Sciences Publications Ltd 26.10.2018; eLife Sciences Publications, Ltd
• Subjects: Adaptation, Biological; Animals; Binding sites; Biochemistry and Chemical Biology; Biological Evolution; Biology; Epistasis; Epistasis, Genetic; Evolution; Evolutionary Biology; Fiber optics; intramolecular epistasis; Light; Photopigments; Photosensitivity; Pigments; protein evolution; Proteins; Rhodopsin; Rhodopsin - genetics; Selection, Genetic; Vertebrates; Vision; Vision, Ocular - physiology; Canada; rhodopsin; evolutionary biology; chemical biology; protein evolution; biochemistry; none; intramolecular epistasis
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.35957

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 E122, but instead, selection appears to have entrenched E122 in tetrapods epistatic interactions with nearby coevolving sites. In fishes by contrast, selection may have exploited these epistatic effects to explore alternative trajectories, but 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.