Visual sensitivities tuned by heterochronic shifts in opsin gene expression

Karen L Carleton,J Todd Streelman,William N Mcfarland,Ellis R Loew,Michael R Kidd,Tyrone C Spady

doi:10.1186/1741-7007-6-22

Abstract

BackgroundCichlid fishes have radiated into hundreds of species in the Great Lakes of Africa. Brightly colored males display on leks and vie to be chosen by females as mates. Strong discrimination by females causes differential male mating success, rapid evolution of male color patterns and, possibly, speciation. In addition to differences in color pattern, Lake Malawi cichlids also show some of the largest known shifts in visual sensitivity among closely related species. These shifts result from modulated expression of seven cone opsin genes. However, the mechanisms for this modulated expression are unknown.ResultsIn this work, we ask whether these differences might result from changes in developmental patterning of cone opsin genes. To test this, we compared the developmental pattern of cone opsin gene expression of the Nile tilapia, Oreochromis niloticus, with that of several cichlid species from Lake Malawi. In tilapia, quantitative polymerase chain reaction showed that opsin gene expression changes dynamically from a larval gene set through a juvenile set to a final adult set. In contrast, Lake Malawi species showed one of two developmental patterns. In some species, the expressed gene set changes slowly, either retaining the larval pattern or progressing only from larval to juvenile gene sets (neoteny). In the other species, the same genes are expressed in both larvae and adults but correspond to the tilapia adult genes (direct development).ConclusionDifferences in visual sensitivities among species of Lake Malawi cichlids arise through heterochronic shifts relative to the ontogenetic pattern of the tilapia outgroup. Heterochrony has previously been shown to be a powerful mechanism for change in morphological evolution. We found that altering developmental expression patterns is also an important mechanism for altering sensory systems. These resulting sensory shifts will have major impacts on visual communication and could help drive cichlid speciation.

Highlights

Cichlid fishes have radiated into hundreds of species in the Great Lakes of Africa
We have found that their visual systems are highly diverse, with some of the most variable visual pigments known in vertebrates [1,2]
These included visual pigments from six distinct spectral classes from the ultraviolet to the long wavelength sensitive (LWS) pigments

Summary

Introduction

Cichlid fishes have radiated into hundreds of species in the Great Lakes of Africa. In addition to differences in color pattern, Lake Malawi cichlids show some of the largest known shifts in visual sensitivity among closely related species. These shifts result from modulated expression of seven cone opsin genes. The amino acid sequence of the opsin determines the spectral absorbance of the pigment. Spectral tuning of the pigment occurs through amino acid substitutions at sites directed into the retinal binding pocket [3]. Visual pigment absorbance may be tuned to the environment, in aquatic systems. Owing to the tight correspondence between opsin sequence and function, opsins are an excellent system for the study of molecular adaptation [8]

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Conclusion