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

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 ( max) at 500 nm, from which contemporary rhodopsins with variable maxs 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 (Ϸ94%) 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. molecular adaptation ͉ rhodopsin

Evolutionary replacement of UV vision by violet vision in fish

“…To understand possible selective advantages of the evolutionary switches between UV and violet vision (5), we must identify critical amino acid changes that cause such functional changes and relate UV and violet vision of organisms to their ecological environments and life styles (6,7). Living in diverse and reasonably well-defined light environments, fish offer the best opportunity to elucidate the molecular bases for the spectral tuning and adaptive evolution of SWS1 pigments at the same time (8).…”

The origin of adaptive phenotypes

“…The data of Yokoyama et al (3) provided an ideal opportunity to test whether codon-based methods can indeed be used to identify adaptive evolution. Because those authors knew the amino acid replacements that have led to adaptive changes in rhosopsins, they could test whether these same residues are identified by the codon-based methods.…”

“…Yokoyama et al (3) were able to identify the molecular basis of functionally significant changes in dim-light vision of vertebrates. But their approach could not necessarily determine the population processes that originally gave rise to those changes; in particular, there was no direct evidence that natural selection was actually involved in fixing adaptive changes.…”

“…This vast outpouring of pseudoDarwinian hype has been genuinely harmful to the credibility of evolutionary biology as a science. It is to be hoped that the work of Yokoyama et al (3) will help put an end to these distressing tendencies. By incorporating experimental evidence regarding the phenotypic effects of reconstructed evolutionary changes, this study sets a new standard for studies of adaptive evolution at the molecular level.…”

“…Yokoyama et al (3) used phylogenetic methods to reconstruct the relationships among vertebrate rhodopsin genes and to predict the sequences ancestral to present-day rhodopsins. Moreover, combining informatics with laboratory work, they engineered 11 of these predicted ancestral rhodopsins and determined their max values.…”