Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-31T19:22:15.703Z Has data issue: false hasContentIssue false

15 - Eyes, Vision, and the Origins and Early Evolution of Snakes

from Part IV - Neurobiological Perspectives

Published online by Cambridge University Press:  30 July 2022

By
David J. Gower ,
Einat Hauzman ,
Bruno F. Simões  and
Ryan K. Schott
Edited by
David J. Gower  and
Hussam Zaher
David J. Gower
Affiliation:
Natural History Museum, London
Hussam Zaher
Affiliation:
Universidade de São Paulo
Get access

Summary

The distinctiveness of their eyes has played a major role in debates about snake origins and early evolution, having been interpreted as providing evidence for nocturnal and/or fossorial (and to a lesser degree, aquatic) origins. Much of this evidence came from anatomical studies of snake retinas in the 1900s. More recent morphological and molecular studies have provided further evidence for the distinctness of the snake eye that lacks many of the traits present in lizards. Data remain patchy and are particularly sparse for extant lineages (scolecophidians and non-caenophidian alethinophidians) that bear special importance for inferring traits of the ancestral snake. However, evidence is strong for: (1) the ancestral snake having lost multiple anatomical and molecular genetic components present in the eyes of the ancestral squamate and retained by most lizards; (2) the eye of the ancestral snake being adapted for low-light environments and/or activity cycles but being notably less regressed than that of extant scolecophidians; (3) an elaboration and diversification of the eye within endoglyptodont caenophidian snakes.

Keywords

Squamatalizardevolutionsensory biologyretinaphotoreceptorvisual opsinadaptationvisual ecologytransmutation
Type
Chapter
Information
The Origin and Early Evolutionary History of Snakes , pp. 316 - 348
Publisher: Cambridge University Press
Print publication year: 2022

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Underwood, G., A Contribution to the Classification of Snakes (London: British Museum (Natural History), 1967).Google Scholar
Walls, G. L., The Vertebrate Eye and Its Adaptive Radiation (Bloomfield Hills, MI: Cranbrook Institute of Science, 1942).Google Scholar
Bellairs, A. D’A. and Underwood, G., The origin of Snakes. Biological Reviews, 26 (1951), 193–237.Google Scholar
Caprette, C. L., Lee, M. S. Y., Shine, R., Mokany, A., and Downhower, J. F., The origin of snakes (Serpentes) as seen through eye anatomy. Biological Journal of the Linnean Society, 81 (2004), 469–482.Google Scholar
Simões, B. F., Sampaio, F. L., Jared, C., et al., Visual system evolution and the nature of the ancestral snake. Journal of Evolutionary Biology, 28 (2015), 1309–1320.Google Scholar
Schott, R. K., Van Nynatten, A., Card, D. C., Castoe, T. A., and Change, B. S. W., Shifts in selective pressures on snake phototransduction genes associated with photoreceptor transmutation and dim-light ancestry. Molecular Biology and Evolution, 35 (2018), 1376–1389.Google Scholar
Miralles, A., Marin, J., Markus, D., et al., Molecular evidence for the paraphyly of Scolecophidia and its evolutionary implications. Journal of Evolutionary Biology, 31 (2018), 1782–1793.Google Scholar
Zaher, H., Grazziotin, F. G., Cadle, J. E., et al., Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South American xenodontines: a revised classification and descriptions of new taxa. Papéis Avulsos de Zoologia, 49 (2009), 115–153.CrossRefGoogle Scholar
Hauzman, E., Kalava, V., Bonci, D. M. O., and Ventura, D. F., Characterization of the melanopsin gene (Opn4x) of diurnal and nocturnal snakes. BMC Evolutionary Biology, 19 (2019), 174.CrossRefGoogle ScholarPubMed
Aranda, M. L. and Schmidt, T. M., Diversity of intrinsically photosensitive retinal ganglion cells: circuits and functions. Cellular and Molecular Life Sciences, 78 (2021), 889–907.Google Scholar
Díaz, N. M., Morera, L. P., and Guido, M. E., Melanopsin and the non-visual photochemistry in the inner retina of vertebrates. Photochemistry and Photobiology, 92 (2016), 29–44.Google Scholar
Schott, R. K., Müller, J., Yang, C. G. Y., et al., Evolutionary transformation of rod photoreceptors in the all-cone retina of a diurnal garter snake. Proceedings of the National Academy of Sciences, USA, 113 (2016), 356–361.CrossRefGoogle ScholarPubMed
Bhattacharyya, N., Darren, B., Schott, R. K., Tropepe, V., and Chang, B. S. W., Cone-like rhodopsin expressed in the all-cone retina of the colubrid pine snake as a potential adaptation to diurnality. Journal of Experimental Biology, 220 (2017), 2418–2425.Google Scholar
Hauzman, E., Bonci, D. M. O., Suárez-Villota, E. Y., Neitz, M., and Ventura, D. F., Daily activity patterns influence retinal morphology, signatures of selection, and spectral tuning of opsin genes in colubrid snakes. BMC Evolutionary Biology, 17 (2017), 249–263.Google Scholar
Lamb, T. D., Evolution of phototransduction, vertebrate photoreceptors and retina. Progress in Retinal and Eye Research, 36 (2013), 52–119.Google Scholar
Palczewski, K. and Kiser, P. D., Shedding new light on the generation of the visual chromophore. Proceedings of the National Academy of Sciences, USA, 117 (2020), 19629–19638.CrossRefGoogle ScholarPubMed
Choi, E. H., Daruwalla, A., Suh, S., Leinonen, H., and Palczewski, K., Retinoids in the visual cycle: role of the retinal G protein-coupled receptor. Journal of Lipid Research, 62 (2020), 100040.Google Scholar
Morshedian, A., Kaylor, J. J., Ng, S. Y, et al., Light-driven regeneration of cone visual pigments through a mechanism involving RGR opsin in Müller glial cells. Neuron , 102 (2019), 1172–1183.CrossRefGoogle ScholarPubMed
Davies, W. I. L., Collin, S. P., and Hunt, D. M., Molecular ecology and adaptation of visual photopigments in craniates. Molecular Ecology, 21 (2012), 3121–3158.Google Scholar
Gemmell, N. J., Rutherford, K., Prost, S., et al., The tuatara genome reveals ancient features of amniote evolution. Nature, 584 (2020), 403–409.Google Scholar
Gower, D. J., Fleming, J. F., Pisani, D., et al, Eye-transcriptome and genome-wide sequencing for Scolecophidia: implications for inferring the visual system of the ancestral snake. Genome Biology and Evolution, 13(2021), evab253.Google Scholar
Walls, G. L., The reptilian retina: I. A new concept of visual-cell evolution. American Journal of Ophthalmology, 17 (1934), 892–915.Google Scholar
Walls, G. L., Ophthalmological implications for the early history of the Snakes. Copeia, 1 (1940), 1–8.Google Scholar
Underwood, G., Some suggestions concerning vertebrate visual cells. Vision Research, 8 (1968), 483–488.Google Scholar
Underwood, G., The eye. In Gans, C., Parson, T. S., eds., Biology of the Reptilia, Morphology B. (New York: Academic Press, 1970), pp. 1–97.Google Scholar
Rochon-Duvigneaud, A., Les yeux et la vision des vertébrés (Paris: Masson, 1943).Google Scholar
Mahendra, B. C., Some remarks on the phylogeny of the Ophidia. Anatomischer Anzeiger, 86 (1938), 347–356.Google Scholar
Underwood, G., On lizards of the family Pygopodidae. A contribution to the morphology and phylogeny of the Squamata. Journal of Morphology, 100 (1957), 207–268.Google Scholar
Wilkinson, M., Mauro, D. S., Sherratt, E., and Gower, D. J., A nine-family classification of caecilians (Amphibia: Gymnophiona). Zootaxa, 64 (2011), 41–64.Google Scholar
San Mauro, D., Gower, D. J., Müller, H., et al., Life-history evolution and mitogenomic phylogeny of caecilian amphibians. Molecular Phylogenetics and Evolution, 73 (2014), 177–189.Google Scholar
Senn, D. G., Uber das optische System im Gehirn squamater Reptilien; eine vergleichendmorphologische Untersuchung, unter besonderer Berucksichtigung einiger Wuhlschlangen. Acta Anatomica, 65 (1966), 1–87.Google Scholar
Stingelin, W. and Senn, D. G., Morphological studies on the brain of Sauropsida. Annals of the New York Academy of Sciences, 167 (1969), 156–163.Google Scholar
Senn, D. G. and Northcutt, R. G., The forebrain and midbrain of some squamates and their bearing on the origin of snakes. Journal of Morphology, 140 (1973), 135–151.Google Scholar
Repérant, J., Rio, J. P., Ward, R., et al., Comparative analysis of the primary visual system of reptiles. In Gans, C. and Ulinski, S., eds., Biology of the Reptilia, Vol. 17 (Chicago: University of Chicago Press, 1992), pp. 175–240 Google Scholar
Walls, G. L., The significance of the reptilian ‘spectacle’. American Journal of Ophthalmology, 17 (1934), 1045–1047.Google Scholar
Douglas, R. H. and Jeffery, G., The spectral transmission of ocular media suggests ultraviolet sensitivity is widespread among mammals. Proceedings of the Royal Society B: Biological Sciences, 281 (2014), 20132995.Google Scholar
Hart, N. S., Coimbra, J. P., Collin, S. P., and Westhoff, G., Photoreceptor types, visual pigments, and topographic specializations in the retinas of hydrophiid sea snakes. Journal of Comparative Neurology, 520 (2012), 1246–1261.Google Scholar
Simões, B. F., Sampaio, F. L., Douglas, R. H., et al., Visual pigments, ocular filters and the evolution of snake vision. Molecular Biology and Evolution, 33 (2016), 2483–2495.Google Scholar
Simões, B. F., Gower, D. J., Rasmussen, A. R., et al., Spectral diversification and trans-species allelic polymorphism during the land-to-sea transition in snakes. Current Biology, 30 (2020), 2608–2615.Google Scholar
Douglas, R. H. and Marshall, N. J., A review of vertebrate and invertebrate ocular filters. In Archer, S. N., Djamgoz, M. B. A., Loew, E. R., Partridge, J. C., and Vallerga, S., eds., Adaptive Mechanisms in the Ecology of Vision (The Netherlands: Springer, 1999), pp. 95–162.Google Scholar
Van Doorn, K. and Sivak, J. G., Blood flow dynamics in the snake spectacle. Journal of Experimental Biology, 216 (2013), 4190–4195.Google Scholar
Van Doorn, K. and Sivak, J. G., Spectral transmittance of the spectacle scale of snakes and geckos. Contributions to Zoology, 84 (2015), 1–12.Google Scholar
Da Silva, M. A. O., Heegaard, S., Wang, T., Nyengard, J. R., and Bertelsen, M. F., The spectacle of the ball python (Python regius): a morphological description. Journal of Morphology, 275 (2014), 489–496.Google Scholar
Lauridsen, H., Da Silva, M. A. O., Hansen, K., et al., Ultrasound imaging of the anterior section of the eye of five different snake species. BMC Veterinary Research, 10 (2014), 1–6.Google Scholar
Da Silva, M. A. O., Heegaard, S., Wang, T., et al., Morphology of the snake spectacle reflects its evolutionary adaptation and development. BMC Veterinary Research, 13 (2017), 1–8.Google Scholar
Da Silva, M. A. O., Gade, J. T., Damsgaard, C., et al., Morphology and evolution of the snake cornea. Journal of Morphology, 281 (2020), 240–249.Google Scholar
Sivak, J. G., The role of the spectacle in the visual optics of the snake eye. Vision Research, 17 (1977), 293–298.Google Scholar
Caprette, C. L., Conquering the cold shudder: the origin and evolution of snakes eyes . Unpublished PhD thesis, Ohio State University (2005).Google Scholar
Perry, B. W., Card, D. C., McGlothin, J. W., et al., Molecular adaptations for sensing and securing prey and insight into amniote genome diversity from the garter snake genome. Genome Biology and Evolution, 10 (2018), 2110–2129.CrossRefGoogle ScholarPubMed
Wistow, G. J., Molecular Biology and Evolution of Crystallins: Gene Recruitment and Multifunctional Proteins in the Eye Lens (Heidelberg: Springer-Verlag, 1995).Google Scholar
Röll, B., Multiple origin of diurnality in geckos: evidence from eye lens crystallins. Naturwissenschaften, 88 (2001), 293–296.Google Scholar
Ott, M., Visual accommodation in vertebrates: mechanisms, physiological response and stimuli. Journal of Comparative Physiology A, 192 (2006), 97–111.Google Scholar
Fontenot, C. L., Variation in pupil diameter in North American Gartersnakes (Thamnophis) is regulated by immersion in water, not by light intensity. Vision Research, 48 (2008), 1663–1669.Google Scholar
Munro, D. F., Vertical position of the pupil in the Crotalidae. Herpetologica, 5 (1949), 106–108.Google Scholar
Werner, Y. L., Extreme adaptability to light, in the round pupil of the snake Spalerosophis . Vision Research, 10 (1970), 1159–1160.Google Scholar
Douglas, R. H., The pupillary light responses of animals: a review of their distribution, dynamics, mechanisms and functions. Progress in Retinal and Eye Research, 66 (2018), 17–48.Google Scholar
Brischoux, F., Pizzatto, L., and Shine, R., Insights into the adaptive significance of vertical pupil shape in snakes. Journal of Evolutionary Biology, 23 (2010), 1878–1885.Google Scholar
Pyron, R. A. and Wallach, V., Systematics of the blindsnakes (Serpentes: Scolecophidia: Typhlopoidea) based on molecular and morphological evidence. Zootaxa, 3829 (2014), 1–81.Google Scholar
Gower, D. J., Captain, A., and Thakur, S. S., On the taxonomic status of Uropeltis bicatenata (Günther) (Reptilia: Serpentes: Uropeltidae). Hamadryad, 33 (2008), 64–82.Google Scholar
Giri, V. B., Gower, D. J., Das, A., et al., A new genus and species of natricine snake from northeast India. Zootaxa, 4603 (2019), 241–264.Google Scholar
Underwood, G., On the visual-cell pattern of a homalopsine snake. Journal of Anatomy, 100 (1966), 571–575.Google Scholar
Underwood, G., A comprehensive approach to the classification of higher snakes. Herpetologica, 23 (1967), 161–168.Google Scholar
Rasmussen, J. B., The retina of Psammodynastes pulverulentus (Boie, 1827) and Telescopus fallax (Fleischmann, 1831) with a discussion of their phylogenetic significance (Colubroidea, Serpentes). Journal of Zoological Systematics and Evolutionary Research, 28 (1990), 269–276.Google Scholar
Rasmussen, J. B., An intergeneric analysis of some boogie snakes – Bogert’s (1940) Group XIII and XIV (Boifinae, Serpentes). Vidensk Meddelelser fra Dansk Naturhistorisk Foren, 141 (1979), 97–155.Google Scholar
Rasmussen, J. B., A re-evaluation of the systematics of the African rear-fanged snakes of Bogert’s Groups XII–XVI, including a discussion of some evolutionary trends within Caenophidia. In Proceedings of the International Symposium on African Vertebrates Zoologisches Forschungsinstitut und Museum Alexander Koenig (Bonn, 1985), pp. 531–548.Google Scholar
Simões, B. F., Sampaio, F. L., Loew, E. R., et al., Multiple rod–cone and cone–rod photoreceptor transmutations in snakes: evidence from visual opsin gene expression. Proceedings of the Royal Society B: Biological Sciences, 283 (2016), 20152624.Google Scholar
Schott, R. K., Bhattacharyya, N., and Chang, B. S. W., Evolutionary signatures of photoreceptor transmutation in geckos reveal potential adaptation and convergence with snakes. Evolution, 73 (2019), 1958–1971.Google Scholar
Sillman, A. J., Carver, J. K., and Loew, E. R., The photoreceptors and visual pigments in the retina of a boid snake, the ball python (Python regius). Journal of Experimental Biology, 202 (1999), 1931–1938.CrossRefGoogle ScholarPubMed
Sillman, A. J., Johnson, J. L., and Loew, E. R., Retinal photoreceptors and visual pigments in Boa constrictor imperator . Journal of Experimental Zoology, 290 (2001), 359–365.Google Scholar
Gower, D. J., Sampaio, F. L., Peichl, L., et al., Evolution of the eyes of vipers with and without infrared-sensing pit organs. Biological Journal of the Linnean Society, 126 (2019), 796–823.Google Scholar
Munk, O. and Rasmussen, J. B.. Note on the rod-like photoreceptors in the retina of the snake Telescopus fallax (Fleischmann, 1831). Acta Zoologica, 74 (1993), 9–13.Google Scholar
Miller, W. H. and Snyder, A. W., The tiered vertebrate retina. Vision Research, 17 (1977), 239–255.Google Scholar
Sillman, A. J., Govardovskii, V. I., Rohlich, P., Southard, J. A., and Loew, E. R., The photoreceptors and visual pigments of the garter snake (Thamnophis sirtalis): a microspectrophotometric, scanning electron microscopic and immunocytochemical study. Journal of Comparative Physiology A, 181 (1997), 89–101.Google Scholar
Hauzman, E., Bonci, D. M. O., Grotzner, S. R., et al., Comparative study of photoreceptor and retinal ganglion cell topography and spatial resolving power in dipsadidae snakes. Brain Behavior and Evolution, 84 (2014), 197–213.Google Scholar
Ullmann, J. F. P., Moore, B. A., Temple, S. E., Fernández-Juricic, E., and Collin, S. P., The retinal wholemount technique: a window to understanding the brain and behaviour. Brain, Behavior and Evolution, 79 (2012), 26–44.Google Scholar
Stone, J., The Whole Mount Handbook. A Guide to the Preparation and Analysis of Retinal Wholemounts (Sydney: Maitland Publications, 1981).Google Scholar
Stone, J., Parallel Processing in the Visual System (New York: Plenum, 1983).Google Scholar
Hughes, A., The topography of vision in mammals of contrasting life style: comparative optics and retinal organisation. In Crescitelli, F., Dvorak, C. A., Eder, D. J., et al., eds., The Visual System in Vertebrates. Handbook of Sensory Physiology. Vol. 7 (Heidelberg, Berlin: Springer, 1977), pp. 613–756.CrossRefGoogle Scholar
Schmitz, L., Evolution of retinal topography in coral reef fishes. Journal of Morphology, 280 (2019), S69.Google Scholar
Wong, R. O., Morphology and distribution of neurons in the retina of the American garter snake Thamnophis sirtalis . Journal of Comparative Neurology, 283 (1989), 587–601.Google Scholar
Hauzman, E., Bonci, D. M. O., and Ventura, D. F., Retinal topographic maps: a glimpse into the animals’ visual world. In Heinbockel, T., ed., Sensory Nervous System (London: IntechOpen, 2018), pp. 101–126.Google Scholar
Kalberer, M. and Pedler, C., The visual cells of the alligator: an electron microscopic study. Vision Research, 3 (1963), 323–329.Google Scholar
Pedler, C. and Tilly, R., The nature of the gecko visual cell. Vision Research, 4 (1964), 499–510.Google Scholar
Underwood, G., An overview of venomous snake evolution. In Thorpe, R. S., Wüster, W. and Malhotra, A., eds., Venomous Snake. Ecology, Evolution and Snakebite, The Zoological Society of London (Oxford: Clarendon Press, 1997), pp. 1–13.Google Scholar
Govardovskii, V. I. and Chkheidze, N. I, Retinal photoreceptors and visual pigments in certain snakes. Biological Abstracts, 90 (1989), 1036.Google Scholar
Davies, W. L., Cowing, J. A., Bowmaker, J. K., et al., Shedding light on serpent sight: the visual pigments of henophidian snakes. Journal of Neuroscience, 29 (2009), 7519–7525.Google Scholar
Seiko, T., Kishida, T., Toyama, M., et al., Visual adaptation of opsin genes to the aquatic environment in sea snakes. BMC Evolutionary Biology, 20 (2020), 1–13.Google Scholar
Hauzman, E., Pierotti, M. E., Bhattacharyya, N., et al., Simultaneous expression of UV and violet SWS1 opsins expands the visual palette in a group of freshwater snakes. Molecular Biology and Evolution, 38 (2021), 5225–5240.Google Scholar
Van Nynatten, A., Castiglione, G. M., Gutierrez, E. A., Lovejoy, N. R., and Chang, B. S. W., Recreated ancestral opsin associated with marine to freshwater croaker invasion reveals kinetic and spectral adaptation. Molecular Biology and Evolution, 38 (2021), 2076–2087.Google Scholar
Yokoyama, S., Evolution of dim-light and color vision pigments. Annual Review of Genomics and Human Genetics, 9 (2008), 259–282.Google Scholar
Yokoyama, S., Starmer, W. T., Takahashi, Y., and Tada, T., Tertiary structure and spectral tuning of UV and violet pigments in vertebrates. Gene, 365 (2006), 95–103.Google Scholar
Hunt, D. M. and Peichl, L., S cones: evolution, retinal distribution, development, and spectral sensitivity. Vision Neuroscience, 31 (2014), 115–138.Google Scholar
Yokoyama, S., Yang, H., and Starmer, W. T., Molecular basis of spectral tuning in the red- and green-sensitive (M/LWS) pigments in vertebrates. Genetics, 179 (2008), 2037–2043.Google Scholar
Hunt, D. M. and Collin, S. P., The evolution of photoreceptors and visual photopigments in vertebrates. In Hunt, D. M., Hankins, M. W., Collin, S. P., and Marshall, J. N., eds., Evolution of Visual and Non-visual Pigments (Boston: Springer, 2014), pp. 163–217.Google Scholar
Hauser, F. E., Van Hazel, I. and Chang, B. S. W., Spectral tuning in vertebrate short wavelength-sensitive 1 (SWS1) visual pigments: can wavelength sensitivity be inferred from sequence data? Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 322 (2014), 529–539.Google Scholar
Martin, M., Le Galliard, J. F., Meylan, S., and Loew, E. R., The importance of ultraviolet and near-infrared sensitivity for visual discrimination in two species of lacertid lizards. Journal of Experimental Biology, 218 (2015), 458–465.Google Scholar
Veilleux, C. C. and Cummings, M. E., Nocturnal light environments and species ecology: implications for nocturnal color vision in forests. Journal of Experimental Biology, 215 (2012), 4085–4096.Google Scholar
Hargrave, P. A., McDowell, J. H., Curtis, D. R., et al., The structure of bovine rhodopsin. Biophysics of Structure and Mechanism, 9 (1983), 235–244.Google Scholar
Nathans, J. and Hogness, D. S.. Isolation, sequence analysis, and intron-exon arrangement of the gene encoding bovine rhodopsin. Cell, 34 (1983), 807–814.Google Scholar
Ovchinnikov, Y. A., Rhodopsin and bacteriorhodopsin: structure-function relationships. FEBS Letters, 148 (1982), 179–191.Google Scholar
Schott, R. K., Panesar, B., Card, D. C., et al., Targeted capture of complete coding regions across divergent species. Genome Biology and Evolution, 9 (2017), 398–414.Google Scholar
Katti, C., Stacey-Solis, M., Coronel-Rojas, N. A., and Davies, W. I. L., Opsin-based photopigments expressed in the retina of a South American pit viper, Bothrops atrox (Viperidae). Visual Neuroscience, 35 (2018), e027.Google Scholar
Vonk, F. J., Casewell, N. R., Henkel, C. V., et al., The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system. Proceedings of the National Academy of Sciences, USA, 110 (2013), 20651–20656.Google Scholar
Castoe, T. A., de Koning, A. P. J., Hall, K. T., et al., The Burmese python genome reveals the molecular basis for extreme adaptation in snakes. Proceedings of the National Academy of Sciences, USA, 110 (2013), 20645–20650.Google Scholar
Yin, W., Wang, Z., Li, Q-.Y., et al., Evolutionary trajectories of snake genes and genomes revealed by comparative analyses of five-pacer viper. Nature Communications, 7 (2016), 1–11.Google Scholar
Emerling, C. A., Archelosaurian color vision, parietal eye loss, and the crocodylian nocturnal bottleneck. Molecular Biology and Evolution, 34 (2016), 666–676.Google Scholar
Emerling, C. A. and Springer, M. S., Genomic evidence for rod monochromacy in sloths and armadillos suggests early subterranean history for xenarthra. Proceedings of the Royal Society B: Biological Sciences, 282 (2014), 20142192.Google Scholar
Emerling, C. A. and Springer, M. S., Eyes underground: regression of visual protein networks in subterranean mammals. Molecular Phylogenetics and Evolution, 78 (2014), 260–270.Google Scholar
Springer, M. S., Emerling, C. A., Fugate, N., et al., Inactivation of cone-specific phototransduction genes in rod monochromatic cetaceans. Frontiers in Ecology and Evolution, 4 (2016), 61.Google Scholar
Emerling, C. A., Genomic regression of claw keratin, taste receptor and light-associated genes provides insights into biology and evolutionary origins of snakes. Molecular Phylogenetics and Evolution, 115 (2017), 40–49.Google Scholar
Anisimova, M. and Kosiol, C., Investigating protein-coding sequence evolution with probabilistic codon substitution models. Molecular Biology and Evolution, 26 (2009), 255–271.Google Scholar
Yang, Z., PAML 4: Phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24 (2007), 1586–1591.Google Scholar
Kosakovsky Pond, S. L., Frost, S. D. W., and Muse, S. V., HyPhy: Hypothesis testing using phylogenies. Bioinformatics, 21 (2005), 676–679.Google Scholar
Wertheim, J. O., Murrell, B., Smith, M. D., Kosakovsky Pond, S. L., and Scheffler, K., RELAX: Detecting relaxed selection in a phylogenetic framework. Molecular Biology and Evolution, 32 (2015), 820–832.Google Scholar
Bielawski, J. P. and Yang, Z., A maximum likelihood method for detecting functional divergence at individual codon sites, with application to gene family evolution. Journal of Molecular Evolution, 59 (2004), 121–132.Google Scholar
Schott, R. K., Refvik, S. P., Hauser, F. E., López-Fernández, H., and Chang, B. S. W., Divergent positive selection in rhodopsin from lake and riverine cichlid fishes. Molecular Biology and Evolution, 31 (2014), 1149–1165.Google Scholar
Baker, J. L., Dunn, K. A., Mingrone, J., et al., Functional divergence of the nuclear receptor NR2C1 as a modulator of pluripotentiality during hominid evolution. Genetics, 203 (2016), 905–922.Google Scholar
Jacobs, G. H., Fenwick, J. A., Crognale, M. A., and Deegan, J. F., The all-cone retina of the garter snake: spectral mechanisms and photopigment. Journal of Comparative Physiology A, 170 (1992), 701–707.Google Scholar
Elliott, W. R., Glickman, R. D., Rentmeister-Bryant, H., and Zwick, H., Functional assessment of snake retina using pattern ERG. Investigative Ophthalmology & Visual Science, 44 (2003), 2706–2706.Google Scholar
Glickman, R. D., Elliott, W. R. III, and Kumar, N., Functional and cellular responses to laser injury in the rat snake retina. In Optical Interactions with Tissue and Cells XVIII, 643511, International Society for Optics and Photonics (2007).Google Scholar
Baker, R. A., Gawne, T. J., Loop, M. S., and Pullman, S., Visual acuity of the midland banded water snake estimated from evoked telencephalic potentials. Journal of Comparative Physiology A, 193 (2007), 865–870.CrossRefGoogle ScholarPubMed
Lythgoe, J. N., Ecology of Vision (Oxford: Oxford University Press, 1979).Google Scholar
Rumpff, H., Experimental studies on vision in Indian snakes. Journal of the Bombay Natural History Society, 76 (1979), 475–480.Google Scholar
Szabo, B., Noble, D. W. A., and Whiting, M. J., Learning in non-avian reptiles 40 years on: advances and promising new directions. Biological Reviews, 96 (2021), 331–356.Google Scholar
Terrick, T. D., Mumme, R. L., and Burghardt, G. M., Aposematic coloration enhances chemosensory recognition of noxious prey in the garter snake Thamnophis radix . Animal Behaviour, 49 (1995), 857–866.Google Scholar
Friesen, R., Spatial learning of shelter locations and associative learning of a foraging task in the Cottonmouth, (Agkistrodon piscivorus). Unpublished MSc thesis, Missouri State University (2017).Google Scholar
Aubret, F., Bonnet, X., Pearson, D., and Shine, R., How can blind tiger snakes (Notechis scutatus) forage successfully? Australian Journal of Zoology, 53 (2005), 283–288.Google Scholar
Grace, M. S. and Matsushita, A., Neural correlates of complex behavior: vision and infrared imaging in boas and pythons. In Henderson, R. and Powell, R., eds., Biology of the Boas, Pythons and Related Taxa (Eagle Mountain: Eagle Mountain Publishing), pp. 271–285.Google Scholar
Lee, M. S. Y., Hugall, A. F., Lawson, R., and Scanlon, J. D., Phylogeny of snakes (Serpentes): combining morphological and molecular data in likelihood, Bayesian and parsimony analyses. Systematics and Biodiversity, 5 (2007), 371–389.Google Scholar
Wilcox, T. P., Zwickl, D. J., Heath, T. A., and Hillis, D. M., Phylogenetic relationships of the dwarf boas and a comparison of Bayesian and bootstrap measures of phylogenetic support. Molecular Phylogenetics and Evolution, 25 (2002), 361–371.Google Scholar
Rieppel, O., ‘Regressed’ Macrostomatan Snakes. Fieldiana Life and Earth Sciences, 2012 (2012), 99–103.Google Scholar
Walls, G. L., Visual purple in snakes. Science, 75 (1932), 467–468.Google Scholar
Koch, N. M., Garwood, R. J., and Parry, L. A., Fossils improve phylogenetic analyses of morphological characters. Proceedings of the Royal Society B, 288 (2021), 20210044.Google Scholar
Cundall, D. and Irish, F., The snake skull. In Gans, C., Gaunt, A. S. and Adler, K., eds., Biology of the Reptilia, Vol. 20, Morphology H (Ithaca, NY: Society for the Study of Amphibians and Reptiles, 2008), pp. 349–692.Google Scholar
Wiens, J. J., Hutter, C. R., Mulcahy, D. G., et al., Resolving the phylogeny of lizards and snakes (Squamata) with extensive sampling of genes and species. Biology Letters, 8 (2012), 1043–1046.Google Scholar
Atkins, J. B. and Franz-Odendaal, T. A., The sclerotic ring of squamates: an evo-devo-eco perspective. Journal of Anatomy, 229 (2016), 503–513.Google Scholar
Franz, V., Vergleichende anatomie des wirbeltierauges. In Bolk, L., Goppert, E., Kallius, E. and Lubosch, W., eds., Handbuch der vergleichenden anatomie der wirbeltiere (Urban and Schwarzenberg, Berlin, 1934), pp. 989–1292.Google Scholar
Bellairs, A d’A. and Boyd, J. D., The lachrymal apparatus in lizards and snakes.-II. The anterior part of the lachrymal duct and its relationship with the palate and with the nasal and vomeronasal organs. Proceedings of the Zoological Society of London, 120 (1950), 269–310.Google Scholar
Bellairs, A d’A. and Boyd, J. D., The lachrymal apparatus in lizards and snakes – I. The brille, the orbital glands, lachrymal canaliculi and origin of the lachrymal duct. Proceedings of the Zoological Society of London, 117 (1947), 81–108.Google Scholar
Uetz, P., Freed, P., Aguilar, R. and Hošek, J., The Reptile Database. www.reptile-database.org (accessed March 10, 2021).Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×