New insights into the molecular evolution of snake vision

by: Kennedy A Holland, Claremont McKenna College [edited by Lars Schmitz as part of BIOL 167 “Sensory Evolution”, an upper division class at the W.M. Keck Science Department. Written for educational purposes only].

Take a look at the photo below and focus on the unique shape and coloration of the eye.

Figure 1- Green Tree Python

Figure 1. A green tree python, Morelia viridis, has vertical slits that are common in nocturnal predators. Photo from Thor Hakonsen.

From the thin vertical slit spanning the height of the eye, to the wavelength absorbance patterns in the retina, every detail was selected for through evolution. Whether it concerns hunting strategies, circadian rhythm, or preferred habitat, snake species are incredibly diverse and each are well adapted to their unique niche. There is a growing body of evidence that snakes evolved through a burrowing event from ancestral lizards (Simões et al., 2015). Not only could this have affected the anatomy of the snake, but it may also explain the complexity of snake vision. An alternative hypothesis states that the intense variation in snake species is caused by diurnal and nocturnal differences. So how exactly has vision evolved within snake species that have such different lifestyles? That is the overarching question to which Simões et al. (2016a) set out to find the answer.

Although there have been thorough studies of vision in mammals, fish, and birds, not a lot is known regarding how snake vision evolved or how it changes between various species of snakes.

Let’s go over some background information to gain a basic understanding of snake vision before we dive into the most recent and exciting findings of Simões et al. Snakes are vertebrates, and therefore have vertebrate eyes with photoreceptors that are directed towards the back of the eye (Nilsson, 1996; Figure 2). Already we can see a wide range of eye types in different organisms, but variations do not stop there.

Figure 2 - Eye differences

Figure 2. Illustrations of eyes from four different organisms: (a) a vertebrate eye; (b) an arthropod compound eye; (c) a cephalopod lens-eye; (d) a compound eye in polychaete tube-worms and arcoid clams. A snake eye would have the anatomy of eye (a) in this figure. (Nilsson, D. E., 1996).

When light enters the eye, rods and cones in the retina pick up wavelengths and send a signal to the brain via the optic nerve for processing of the image. It has been previously found that snakes have quite variable sets of rod- and cone-like photoreceptors. The amount of diversity within and across snake species is illustrated in Figure 3. Depending on their circadian rhythm, the photoreceptors have evolved and changed shape in response to changes in the snake’s behavior (Simões et al., 2016b). Intuitively, this makes sense, since snakes that are active at night need different vision and light sensitivity than those that are active during the day.

Figure 3 - Rods and Cones

Figure 3. An illustration of the transmutation of cones to rods and vice-versa as explained by Walls, depending on the nocturnal or diurnal behaviors of the snake species. Four varying morphologies of rods and cones within a single species of snake are depicted (Simões et al., 2016b).

 

 

Simões et al. investigated the molecular evolution of snake vision, focusing on the three opsin genes present in most snakes: rh1 (rhodopsin), lws (long-wavelength sensitive), and sws1 (short-wavelength sensitive). The researchers performed a large genomic survey of 69 species of snakes. RNA was extracted from the eye, while lenses and spectacles were stored for subsequent spectral transmission measurements. Various visual opsin genes in the DNA were amplified to obtain fragments and later sequenced to be aligned and compared with published sequences from other reptiles and snakes. The alignment was inspected by eye in order to ensure that the nucleotides and amino acids matched properly. Then, multiple branch-model programs and tests provided information that tracked the evolution of sequence changes.

Specifically, the dN/dS test used in this study determined that all opsin genes evolved through purifying selection, indicating strong functional constraints on the molecular evolution of snake vision.  Hence, snake vision seems to be suited for for their respective lifestyles.

Previous research on visual opsins has linked shifts in amino acid sites to changes in the maximum wavelength absorbance. From this, it is possible to track the changes in wavelength absorbance over time and find correlations with changes in behavior or lifestyle (Figure 4).

Figure 4 - Phylogeny

Figure 4. Snake species phylogeny used in analyses of visual opsin gene evolution. The numbers refer to snake clades:  (1) Scolecophidia; (2) Alethinophidia; (3) Henophidia; (4) Afrophidia; (5) Caenophidia; (6) Viperidae; (7) Colubridae; (8) Natricinae; (9) Dipsadinae; and (10) Colubrinae. The classifications for ecology (squares) and cell patterns (circles) are shown. Empty circles represent species with unknown states, while strikethrough circles show species with no cones in their retinas. Additionally, findings from experiments with the three visual opsin genes are shown on the right, detailing the UV sensitivity potentials and wavelength absorbances for a specific opsin gene, if present in the snake species. (Simões, B. F. et al., 2016a).

You may have noticed that Figure 4 shows which snake species are ultraviolet sensitive. It is no secret to scientists that many snakes are able to see UV light due to a lens that allows UV wavelengths through, and UVS visual pigments. This study confirms this data, providing further information that the snakes which are UV sensitive are mostly nocturnal, allowing them to see better when foraging at night! Simões et al. concluded that the most recent common ancestor of snakes had UV vision. This is consistent with studies showing the existing trend of UV vision in other nocturnal species. Diurnal species, on the other hand, do not have UV sensitive visual pigments and have lenses that block the UV light from entering the eye. If humans had this feature, we wouldn’t have a need for sunglasses! The removal of UV sensitivity is connected with an increase in acuity and not simply for protection from UV rays. This makes vision for diurnal snakes extra detailed for optimal hunting potential. Furthermore, snakes that hunt during the day tend to absorb slightly longer wavelengths than night active species (Simões et al., 2016a; Figure 5).

Figure 5 - Paper Results

Figure 5. Spectral transmission curves are shown for the snakes sampled in this study for (A) lenses and (B) spectacles, including the diurnal or nocturnal tendencies of each species. (C) shows box-plots of wavelengths at which ocular media transmit 50% of the incident illumination (top), and the proportion of UVA transmission (bottom). The box-plots summarize data for the lens (white), spectacle (grey) and a combination of lens and spectacle (black). (Simões, B. F. et al., 2016a).

Although it has been established that the majority of snakes are dichromatic, only seeing two primary colors instead of the three that humans see, trichromacy is speculated to exist in certain species (Davies, W.L., 2009; Simões et al., 2016a). This could be enabled by transmuted cone-like rods for day active snakes, and transmuted rod-like cones in night active snake species (Figure 3). One snake species, the Montpellier snake, only has cones because of its significant diurnal behavior. Additionally, very avid burrowing snake species have lost all of their visual opsins except for rh1 since light sensitivity is more important than color discrimination in dark habitat conditions. This shows that the evolution of snake vision closely matches their hunting behaviors, even at a molecular level, which is fascinating when considering the potential this holds for understanding evolutionary processes in detail.

Walls, back in the 1930’s, came out with the original idea that in saurian eyes, rods and cones can transmute and morph into each other depending on the needs of the species over time (Walls, GL., 1934). Ever since this paper, researchers have supported Walls’ hypothesis by expanding the species studied. Simões et al. have focused on snakes, creating a wider breadth of species that show this pattern of switching rods and cones based on circadian rhythm and hunting strategies. By tracing the changes of specific genes and patterns of rod and cone sets, researchers should be able to establish a phylogenetic history of vision, particularly visual opsin genes. This evolutionary reconstruction can be expanded in future research to provide more information regarding the exact origin of snakes, which remains a question without a definite answer. Although often overlooked in vertebrate studies, snakes are an important addition to the investigation of vision evolution and should continue to be studied moving forward.

 

References

Davies, W.L., Cowing, J.A., Bowmaker, J. K., Carvalho, L.S., Gower, D.J., Hunt, D.M. 2009 Shedding light on serpent sight: the visual pigments of henophidian snakes. Journal of Neuroscience 29(23), 7519-7525. (DOI 10.1523/JNEUROSCI.0517-09.2009)

Nilsson D.E. 1996 Eye ancestry: old genes for new eyes. Current Biology 6, 39–42. (DOI 10.1016/S0960-9822(02)00417-7)

Simões, B. F., Sampaio, F. L., Jared, C., Antoniazzi, M. M., Loew, E. R., Bowmaker, J. K., Rodriguez, A., Hart, N. S., Hunt, D. M., Partridge, J. C. and Gower, D. J. 2015 Visual system evolution and the nature of the ancestral snake. Journal of Evolutionary Biology 28, 1309–1320. (DOI 10.1111/jeb.12663)

Simões, B. F., Sampaio, F. L., Douglas, R.H., Kodandaramaiah, U., Casewell, N. R., Harrison, R. A. Hart, N. S., Partridge, J.C., Hunt, D. M., Gower, D. J. 2016a Visual pigments, ocular filters and the evolution of snake vision. Molecular Biology and Evolution 33(10), 2483-2495. (DOI 10.1093/molbev/msw148)

Simões, B. F., Sampaio, F. L., Loew, E. R., Sanders, K. L., Fisher, R. N., Hart, N. S., Hunt, D. M., Partridge, J. C., Gower, D. J. 2016b Multiple rod-cone and cone-rod photoreceptor transmutations in snakes: evidence from visual opsin gene expression. Proceedings of the Royal Society of London B: Biological Sciences 283, 1823. (DOI 10.1098/rspb.2015.2624)

Walls, GL. 1934 The reptilian retina. I. A new concept of visual-cell evolution. American Journal of Ophthalmology 17, 892-915. (DOI 10.1016/S0002-9394(34)93309-2).

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