The photoreceptors and visual pigments of the garter snake ( Thamnophis sirtalis ): a microspectrophotometric, scanning electron microscopic and immunocytochemical study

Sillman, Arnold J.; Govardovskii, V. I.; Röhlich, P.; Southard, Jeffrey; Loew, Ellis R.

doi:10.1007/s003590050096

Cited by 109 publications

(116 citation statements)

References 30 publications

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“…transparent small oil droplets) that allows the transmission of UV wavelengths and suggests the existence of a population of UVS photoreceptors. Loew et al, 2002) and snakes (Sillman et al, 1997;Sillman et al, 1999;Sillman et al, 2001;Macedonia et al, 2009)], the shortsensitive photoreceptor of lacertids is likely of the UVS type. Moreover, sequences of the SWS1 opsin gene strongly suggest that this gene expresses a UVS-type opsin instead of the VS type.…”

Section: Discussionmentioning

confidence: 99%

Ultraviolet vision in lacertid lizards: evidence from retinal structure, eye transmittance, SWS1 visual pigment genes, and behaviour

Lanuza

Font

2014

Journal of Experimental Biology

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Ultraviolet (UV) vision and UV colour patches have been reported in a wide range of taxa and are increasingly appreciated as an integral part of vertebrate visual perception and communication systems. Previous studies with Lacertidae, a lizard family with diverse and complex coloration, have revealed the existence of UV-reflecting patches that may function as social signals. However, confirmation of the signalling role of UV coloration requires demonstrating that the lizards are capable of vision in the UV waveband. Here we use a multidisciplinary approach to characterize the visual sensitivity of a diverse sample of lacertid species. Spectral transmission measurements of the ocular media show that wavelengths down to 300 nm are transmitted in all the species sampled. Four retinal oil droplet types can be identified in the lacertid retina. Two types are pigmented and two are colourless. Fluorescence microscopy reveals that a type of colourless droplet is UV-transmitting and may thus be associated with UV-sensitive cones. DNA sequencing shows that lacertids have a functional SWS1 opsin, very similar at 13 critical sites to that in the presumed ancestral vertebrate (which was UV sensitive) and other UV-sensitive lizards. Finally, males of Podarcis muralis are capable of discriminating between two views of the same stimulus that differ only in the presence/absence of UV radiance. Taken together, these results provide convergent evidence of UV vision in lacertids, very likely by means of an independent photopigment. Moreover, the presence of four oil droplet types suggests that lacertids have a four-cone colour vision system.

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Section: Discussionmentioning

confidence: 99%

Ultraviolet vision in lacertid lizards: evidence from retinal structure, eye transmittance, SWS1 visual pigment genes, and behaviour

Lanuza

Font

2014

Journal of Experimental Biology

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“…Using MSP, Sillman et al [19] detected three pigment classes in Thamnophis sirtalis, with l max values of 360, 554 and 482 nm. The former two can now be attributed to SWS1-and LWS-based pigments with great confidence given a close match between the measured l max values and those predicted from amino acid sequences defined by our DNA sequences of sws1 ( predicted l max 357 nm) and lws (555 nm) (electronic supplementary material, tables S3 and S4).…”

Section: Python Bivittatus Xenopeltis Unicolormentioning

confidence: 99%

“…The former two can now be attributed to SWS1-and LWS-based pigments with great confidence given a close match between the measured l max values and those predicted from amino acid sequences defined by our DNA sequences of sws1 ( predicted l max 357 nm) and lws (555 nm) (electronic supplementary material, tables S3 and S4). The amino acid sequence of T. sirtalis rh1 does not allow a prediction of l max in this case (electronic supplementary material, table S2), but by elimination the 482 nm pigment measured by Sillman et al [19] using MSP must be RH1-based. The expression of rh1 in T. sirtalis supports Sillman et al's [19] suggestion that small single photoreceptors containing an RH1-based pigment are transmuted (cone-like) rods.…”

Section: Python Bivittatus Xenopeltis Unicolormentioning

confidence: 99%

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

et al. 2016

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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.

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“…Reptilian retinas are unique in having multiple retinal configurations (Underwood, 1970) among closely related species, including all-rod (Kojima et al, 1992), rod and cone (Sillman et al, 2001), and all-cone (Sillman et al, 1997). In 1942, physiologist Gordon Walls outlined his theory of transmutation to explain the evolutionary transformation of photoreceptors from one type to another (Walls, 1942).…”

Section: Introductionmentioning

confidence: 99%

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

Bhattacharyya

Darren

Schott

et al. 2017

Journal of Experimental Biology

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Colubridae is the largest and most diverse family of snakes, with visual systems that reflect this diversity, encompassing a variety of retinal photoreceptor organizations. The transmutation theory proposed by Walls postulates that photoreceptors could evolutionarily transition between cell types in squamates, but few studies have tested this theory. Recently, evidence for transmutation and rod-like machinery in an all-cone retina has been identified in a diurnal garter snake (Thamnophis), and it appears that the rhodopsin gene at least may be widespread among colubrid snakes. However, functional evidence supporting transmutation beyond the existence of the rhodopsin gene remains rare. We examined the all-cone retina of another colubrid, Pituophis melanoleucus, thought to be more secretive/burrowing than Thamnophis. We found that P. melanoleucus expresses two cone opsins (SWS1, LWS) and rhodopsin (RH1) within the eye. Immunohistochemistry localized rhodopsin to the outer segment of photoreceptors in the all-cone retina of the snake and all opsin genes produced functional visual pigments when expressed in vitro. Consistent with other studies, we found that P. melanoleucus rhodopsin is extremely blue-shifted. Surprisingly, P. melanoleucus rhodopsin reacted with hydroxylamine, a typical cone opsin characteristic. These results support the idea that the rhodopsincontaining photoreceptors of P. melanoleucus are the products of evolutionary transmutation from rod ancestors, and suggest that this phenomenon may be widespread in colubrid snakes. We hypothesize that transmutation may be an adaptation for diurnal, brighter-light vision, which could result in increased spectral sensitivity and chromatic discrimination with the potential for colour vision.

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The photoreceptors and visual pigments of the garter snake ( Thamnophis sirtalis ): a microspectrophotometric, scanning electron microscopic and immunocytochemical study

Cited by 109 publications

References 30 publications

Ultraviolet vision in lacertid lizards: evidence from retinal structure, eye transmittance, SWS1 visual pigment genes, and behaviour

Ultraviolet vision in lacertid lizards: evidence from retinal structure, eye transmittance, SWS1 visual pigment genes, and behaviour

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

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

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