Visual system evolution and the nature of the ancestral snake

Abstract

The dominant hypothesis for the evolutionary origin of snakes from 'lizards' (non-snake squamates) is that stem snakes acquired many snake features while passing through a profound burrowing (fossorial) phase. To investigate this, we examined the visual pigments and their encoding opsin genes in a range of squamate reptiles, focusing on fossorial lizards and snakes. We sequenced opsin transcripts isolated from retinal cDNA and used microspectrophotometry to measure directly the spectral absorbance of the photoreceptor visual pigments in a subset of samples. In snakes, but not lizards, dedicated fossoriality (as in Scolecophidia and the alethinophidian Anilius scytale) corresponds with loss of all visual opsins other than RH1 (k max 490-497 nm); all other snakes (including less dedicated burrowers) also have functional sws1 and lws opsin genes. In contrast, the retinas of all lizards sampled, even highly fossorial amphisbaenians with reduced eyes, express functional lws, sws1, sws2 and rh1 genes, and most also express rh2 (i.e. they express all five of the visual opsin genes present in the ancestral vertebrate). Our evidence of visual pigment complements suggests that the visual system of stem snakes was partly reduced, with two (RH2 and SWS2) of the ancestral vertebrate visual pigments being eliminated, but that this did not extend to the extreme additional loss of SWS1 and LWS that subsequently occurred (probably independently) in highly fossorial extant scolecophidians and A. scytale. We therefore consider it unlikely that the ancestral snake was as fossorial as extant scolecophidians, whether or not the latter are para-or monophyletic.

Cone-like rhodopsin expressed in the all cone retina of the colubrid pine snake as a potential adaptation to diurnality

“…In order to demonstrate rod-to-cone transmutation in the retina, there needs to be evidence of a functional rod machinery in a photoreceptor with some rod-like features in a retina that appears, superficially, to consist of only cones. Certainly, the presence of RH1 genes and MSP data suggest transmutation has occurred in several colubrid species (Hart et al, 2012;Sillman et al, 1997;Simões et al, 2015Simões et al, , 2016, but further investigation is required in order to firmly state whether transmutation is present in the retinas of these colubrid snakes, as there are multiple alternate explanations possible (RH1 in the genome but not expressed, rhodopsin expressed but not functional, a cone cell co-opting rhodopsin, etc.). There is only one colubrid snake species for which cellular and molecular evidence for transmutation has been reported: Thamnophis proximus (Schott et al, 2016).…”

“…The family Colubridae is the most speciose family of snakes and encompasses a diverse range of lifestyles and ecologies. Colubrid snakes have recently emerged as a compelling group in which to study visual system evolution and adaptation (Schott et al, 2016;Simões et al, 2015Simões et al, , 2016.…”

Evolutionary transformation of rod photoreceptors in the all-cone retina of a diurnal garter snake

“…opsins, present ancestrally in vertebrates, appear to have been lost early in the evolution of snakes, perhaps as a result of their proposed fossorial origins (10,17,18).…”

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

“…Extraction of mRNA and gDNA, cDNA synthesis, opsin gene amplification and sequencing, MSP and voucher barcoding was done using methods reported by Simõ es et al [12] and detailed in the electronic supplementary material.…”

“…(iii) Chang and co-workers [21,22] l max values, we suggest the former two are likely LWSand SWS1-based visual pigments, respectively. The l max of the 458 nm pigment suggests either an SWS2-or RH2-based pigment but because neither of these have been found in snakes [10][11][12] we consider it more likely to be an RH1-based pigment (with a lower l max value than is typical for vertebrate RH1-based pigments).…”