The all-cone retina of the garter snake: spectral mechanisms and photopigment

Jacobs, Gerald H.; Fenwick, John C.; Crognale, Michael A.; Deegan, Jess F.

doi:10.1007/bf00198980

Cited by 26 publications

(13 citation statements)

References 24 publications

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“…We found no evidence of rods, such as those in, for example, python and boa retinas, which are quite distinct with long, slender inner and outer segments (15,16). This finding is consistent with earlier studies of a closely related species, Thamnophis sirtalis (12)(13)(14), and with the condition described by Walls (4) for diurnal colubrids in general. Four cone types were identified in T. proximus: double cones, large single cones, and two seemingly distinct sizes of small single cones (Fig.…”

Section: T Proximussupporting

confidence: 92%

“…T. proximus RH1 also has the mutation C185S, which has been shown to reduce transducin activation in bovine RH1 (25), which is more typical of cone opsins. Furthermore, the only electrophysiological study of Thamnophis (performed in T. sirtalis) (13) found no evidence for a separate rod (scotopic) visual response. Although these data all point to more cone-like characteristics, despite the rod machinery and ultrastructure, it is clear that further study is needed to explore the functional consequences of this evolutionary transition in Thamnophis and other diurnal colubrids.…”

Section: Discussionmentioning

confidence: 93%

“…Previous studies in the diurnal colubrid Thamnophis have demonstrated an all-cone retina (4,(11)(12)(13)(14), consisting of double cones and large single cones that express a long-wavelength pigment [presumably long wavelengthsensitive opsin (LWS)], and two classes of small single cone, one with a short-wavelength pigment [presumably short wavelengthsensitive 1 opsin (SWS1)] and the other with a middle-wavelength pigment, the identity of which is unclear (14). However, the ancestral condition for colubrids is likely to have been a duplex retina containing both rods and cones, similar to snakes such as pythons and boas, which have rods that express RH1, large single cones that express LWS, and small single cones that express SWS1 ( Fig.…”

mentioning

confidence: 99%

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

Schott

Müller

Yang

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Vertebrate retinas are generally composed of rod (dim-light) and cone (bright-light) photoreceptors with distinct morphologies that evolved as adaptations to nocturnal/crepuscular and diurnal light environments. Over 70 years ago, the "transmutation" theory was proposed to explain some of the rare exceptions in which a photoreceptor type is missing, suggesting that photoreceptors could evolutionarily transition between cell types. Although studies have shown support for this theory in nocturnal geckos, the origins of allcone retinas, such as those found in diurnal colubrid snakes, remain a mystery. Here we investigate the evolutionary fate of the rods in a diurnal garter snake and test two competing hypotheses: (i) that the rods, and their corresponding molecular machinery, were lost or (ii) that the rods were evolutionarily modified to resemble, and function, as cones. Using multiple approaches, we find evidence for a functional and unusually blue-shifted rhodopsin that is expressed in small single "cones." Moreover, these cones express rod transducin and have rod ultrastructural features, providing strong support for the hypothesis that they are not true cones, as previously thought, but rather are modified rods. Several intriguing features of garter snake rhodopsin are suggestive of a more cone-like function. We propose that these cone-like rods may have evolved to regain spectral sensitivity and chromatic discrimination as a result of ancestral losses of middle-wavelength cone opsins in early snake evolution. This study illustrates how sensory evolution can be shaped not only by environmental constraints but also by historical contingency in forming new cell types with convergent functionality. rhodopsin evolution | visual evolution | reptile vision | snake photoreceptors | visual pigment H ow complex structures can arise has long fascinated evolutionary biologists, and the evolution of the eye, as noted by Charles Darwin (1), is perhaps the most famous example. Within the vertebrate eye, the light-sensing photoreceptors are complex, highly specialized cellular structures that can be divided into two general types based on their distinct morphologies and functions: cones, which are active during the day and contain cone opsin pigments, and rods, which mediate dim-light vision and contain rhodopsin (RH1) (2-4). The visual pigments contained in cone photoreceptors are classified into four different subtypes that mediate vision across the visible spectrum from the UV to the red (2). Although most vertebrate retinas are duplex, containing both cones and rods, squamate reptiles (lizards and snakes) are unusual, not only in having highly variable photoreceptor morphologies, but also for several instances of the absence of an entire class of photoreceptors, resulting in simplex retinas composed of only cones or rods (4).In a seminal book published in 1942, Walls (4) hypothesized that, during evolution, vertebrate photoreceptors could transform from one type to another, a process that he termed photoreceptor "transm...

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Section: T Proximussupporting

confidence: 92%

Section: Discussionmentioning

confidence: 93%

mentioning

confidence: 99%

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

Schott

Müller

Yang

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…However, the type of signal these transmuted rods send to the brain is still unknown. Rods and cones are known to have distinct electroretinogram responses, but T. sirtalis is the only colubrid snake with electroretinogram measurements performed at a variety of light levels (Jacobs et al, 1992). However, that study did not record any scotopic (rod) response, nor did it record any photopic response from the SWS1-type photoreceptors, which suggests that the results of the study may be incomplete or that the scotopic pathways in the colubrid eye have degraded.…”

Section: Discussionmentioning

confidence: 87%

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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“…Previous work characterized the spectral sensitivity of the flash ERG in the garter snake, which has an all-cone retina and is also a colubrid snake closely related to the rat snake (Jacobs et al, 1992), but to our knowledge this is the first report of a pattern-evoked electroretinographic response recorded from the rat snake's eye. It is also the first reported use of the cSLO for electrophysiological testing in a reptile model.…”

Section: Discussionmentioning

confidence: 97%

Evaluation of Chronic Stress Induced Neurodegeneration and Treatment Using an In-vivo Retinal Model

Rentmeister-Bryant¹

2004

PsycEXTRA Dataset

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The all-cone retina of the garter snake: spectral mechanisms and photopigment

Cited by 26 publications

References 24 publications

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

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

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

Evaluation of Chronic Stress Induced Neurodegeneration and Treatment Using an In-vivo Retinal Model

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