Multiple rod-cone and cone-rod photoreceptor transmutations in snakes: evidence from visual opsin gene expression

Abstract

In 1934, Gordon Walls forwarded his radical theory of retinal photoreceptor 'transmutation'. This proposed that rods and cones used for scotopic and photopic vision, respectively, were not fixed but could evolve into each other via a series of morphologically distinguishable intermediates. Walls' prime evidence came from series of diurnal and nocturnal geckos and snakes that appeared to have pure-cone or pure-rod retinas (in forms that Walls believed evolved from ancestors with the reverse complement) or which possessed intermediate photoreceptor cells. Walls was limited in testing his theory because the precise identity of visual pigments present in photoreceptors was then unknown. Subsequent molecular research has hitherto neglected this topic but presents new opportunities. We identify three visual opsin genes, rh1, sws1 and lws, in retinal mRNA of an ecologically and taxonomically diverse sample of snakes central to Walls' theory. We conclude that photoreceptors with superficially rod- or cone-like morphology are not limited to containing scotopic or photopic opsins, respectively. Walls' theory is essentially correct, and more research is needed to identify the patterns, processes and functional implications of transmutation. Future research will help to clarify the fundamental properties and physiology of photoreceptors adapted to function in different light levels.

Keywords: Serpentes; mRNA; retina; vision; visual pigments.

Figure 1.

Retinal photoreceptor complements of colubroid snakes, providing evidence of transmutation as conceived by Walls [2]. Four different morphotypes are illustrated, each showing the different classes of photoreceptors present in the retina of a single species of snake. Arrows indicate the transformation series envisaged by Walls. Photoreceptor images reproduced from Walls [2] with permission from Cranbrook Institute of Science.

Figure 2.

(a) Phylogenetic relationships among those snakes for which visual opsin gene sequence data are available (relationships based on [27]). (b) ML phylogenetic tree of visual opsins showing that rh1, sws1 and lws are present in the sampled snakes, whether or not they have superficially all-cone or all-rod retinas. Taxa in bold are those newly sequenced for this study. Support levels for clades are based on ML bootstrap and Bayesian posterior probability values.