Elucidation of phenotypic adaptations: Molecular analyses of dim-light vision proteins in vertebrates

• Authors: Shozo Yokoyama, Emory University; Takashi Tada, Emory University; Huan Zhang, University of Connecticut; Lyle Britt, National Oceanic and Atmospheric Administration
• Journal Title: Proceedings of the National Academy of Sciences
• Volume: Volume 105, Number 36
• Publisher: National Academy of Sciences | 2008-09-09, Pages 13480-13485
• Type of Work: Article | Post-print: After Peer Review
• Publisher DOI: http://doi.org/10.1073/pnas.0802426105
• Subjects: Biology, General
• Keywords: molecular adaptation; rhodopsin

Abstract

Vertebrate ancestors appeared in a uniform, shallow water environment, but modern species flourish in highly variable niches. A striking array of phenotypes exhibited by contemporary animals is assumed to have evolved by accumulating a series of selectively advantageous mutations. However, the experimental test of such adaptive events at the molecular level is remarkably difficult. One testable phenotype, dim-light vision, is mediated by rhodopsins. Here, we engineered 11 ancestral rhodopsins and show that those in early ancestors absorbed light maximally (λmax) at 500 nm, from which contemporary rhodopsins with variable λmaxs of 480–525 nm evolved on at least 18 separate occasions. These highly environment-specific adaptations seem to have occurred largely by amino acid replacements at 12 sites, and most of those at the remaining 191 (≈94%) sites have undergone neutral evolution. The comparison between these results and those inferred by commonly-used parsimony and Bayesian methods demonstrates that statistical tests of positive selection can be misleading without experimental support and that the molecular basis of spectral tuning in rhodopsins should be elucidated by mutagenesis analyses using ancestral pigments.