Evolution of the eyes of vipers with and without infrared-sensing pit organs

Abstract

We examined lens and brille transmittance, photoreceptors, visual pigments, and visual opsin gene sequences of viperid snakes with and without infrared-sensing pit organs. Ocular media transmittance was high in both groups. Contrary to previous reports, both small and large single cones occur in pit vipers. Non-pit vipers differ from pit vipers in having a two-tiered retina, but few taxa have been examined for this poorly understood feature. All vipers sampled express rh1, sws1 and lws visual opsin genes. Opsin spectral tuning varies but not in accordance with the presence/absence of pit organs, and not always as predicted from gene sequences. The visual opsin genes were generally under purifying selection, with positive selection at spectral tuning amino acids in RH1 and SWS1 opsins, and at retinal pocket stabilization sites in RH1 or LWS (and without substantial differences between pit and nonpit vipers). A lack of evidence for a sensory trade-off between viperid eyes (in the aspects examined) and pit organs might be explained by the high degree of neural integration of vision and infrared detection; the latter represents an elaboration of an existing sense with addition of a novel sense organ, rather than involving the evolution of a wholly novel sensory system.