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14 - A Glimpse into the Evolution of the Ophidian Brain

from Part IV - Neurobiological Perspectives

Published online by Cambridge University Press:  30 July 2022

By
Agustín Scanferla
Edited by
David J. Gower  and
Hussam Zaher
David J. Gower
Affiliation:
Natural History Museum, London
Hussam Zaher
Affiliation:
Universidade de São Paulo
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Summary

The origin and early evolution of snakes has long been studied, but little research has focused on soft-tissue organs such as the brain. I report data from dissections and 3D reconstructions of the endocasts of diverse species, including the Cretaceous stem snake Dinilysia patagonica in order to provide a comparative evolutionary framework for the snake brain. Snakes are a special case among reptiles because the braincase almost entirely encloses the whole brain, so endocasts provide realistic representations of brain size and shape. Diversity of brain gross anatomy among snakes is remarkable, encompassing two major cerebrotypes occurring in surface-dwelling and burrowing species. The repeated acquisition of the burrowing cerebrotype in different and phylogenetically distant snake clades suggests that brain gross anatomy is surprisingly evolutionary labile in snakes. Brain gross anatomy and other features such as body size and the absence of any unequivocal osteological feature related to burrowing is interpreted as evidence that D. patagonica was surface-dwelling, and that at least some of the early history of snakes occurred above ground.

Keywords

snakesadaptationmorphologyevolutionsensory biologypalaeontologyfossilsendocastecologyecomorphology
Type
Chapter
Information
The Origin and Early Evolutionary History of Snakes , pp. 294 - 315
Publisher: Cambridge University Press
Print publication year: 2022

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References

Schwenk, K., The evolution of chemoreception in squamate reptiles: a phylogenetic approach. Brain, Behaviour and Evolution, 41 (1993), 124–137.Google Scholar
Goris, R. C., Infrared organs of snakes: an integral part of vision. Journal of Herpetology, 45 (2011), 2–14.Google Scholar
Crowe-Riddell, J. M., Williams, R., Chapuis, L., and Sanders, K. L., Ultrastructural evidence of a mechanosensory function of scale organs (sensilla) in sea snakes (Hydrophiinae). Royal Society Open Science, 6 (2019), 182022.CrossRefGoogle ScholarPubMed
Starck, D., Cranio-cerebral relations in recent reptiles. In Gans, C., Northcutt, R. G. and Ulinski, P., eds., Biology of the Reptilia Vol. 9, Neurology A (London: Academic Press, 1979), pp. 1–38.Google Scholar
Senn, D. G., Über das optische System im Gehirn squamater Reptilien. Eine vergleichend-morphologische Untersuchung, unter besonderer Berucksichtigung einiger Wuhlschlangen. Acta Anatomica, 65 (1966), 1–87.Google Scholar
Masai, H., Takatsuji, K., and Sato, Y., Comparative morphology of the telencephalon of the Japanese colubrid snakes under consideration of habit. Journal of Zoological Systematics and Evolutionary Research, 18 (1980), 310–314.Google Scholar
Platel, R., Nouvelles données sur l’encéphalisation des Reptiles Squamates. Zeitschrift für Zoologische Systematik und Evolutionsforschung, 13 (1975), 161–184.Google Scholar
Olori, J. C., Digital endocasts of the cranial cavity and osseous labyrinth of the burrowing snake Uropeltis woodmasoni (Alethinophidia: Uropeltidae). Copeia, 2010 (2010), 14–26.Google Scholar
Allemand, R., Boistel, R., Daghfous, G., et al., Comparative morphology of snake (Squamata) endocasts: evidence of phylogenetic and ecological signals. Journal of Anatomy, 231 (2017), 849–868.CrossRefGoogle ScholarPubMed
Triviño, L. N., Albino, A., Dozo, M. T., and Williams, J. D., First natural endocranial cast of a fossil snake (Cretaceous of Patagonia, Argentina). The Anatomical Record, 301 (2018), 9–20.Google Scholar
Hopson, J. A., Paleoneurology. In Gans, C., Northcutt, R. G., and Ulinski, P., eds., Biology of the Reptilia, Vol. 9, Neurology A (New York: Academic Press, 1979), pp. 39–146.Google Scholar
Donkelaar, H. J., Reptiles. In Nieuwenhuys, R., ten Donkelaar, H. J. and Nicholson, C., eds., The Central Nervous System of Vertebrates (Berlin: Springer, 1998), pp. 1313–1524.Google Scholar
Halpern, M., The telencephalon of snakes. In Ebbesson, S. O. E., ed., Comparative Neurology of the Telencephalon (New York: Plenum Press, 1980), pp. 257–294.Google Scholar
Rudin, W., Untersuchungen am olfaktorischen System der Reptilien. III. Differenzierungsformen einiger olfaktorischer Zentren bei Reptilien. Acta Anatomica, 89 (1974), 481–515.Google Scholar
Saint Girons, H., The pituitary gland. In Gans, C. and Parsons, T. S., eds., Biology of the Reptilia, Vol. 3, Morphology C (London: Academic Press, 1970), pp. 135–199.Google Scholar
Schreibman, M. P., The pituitary gland. In Pang, P. K. T. and Schreibman, M. P., eds., Vertebrate Endocrinology: Fundamentals and Biomedical Implications, Vol. 1 (New York: Academic Press, 1986), pp. 11–55.Google Scholar
Senn, D. G., The saurian and ophidian colliculi posteriores of the midbrain. Acta Anatomica, 74 (1969), 114–120.Google Scholar
Nieuwenhuys, R., Comparative anatomy of the cerebellum. Progress in Brain Research, 25 (1967), 1–93.Google Scholar
Estes, R., Frazzetta, T. H., and Williams, E. E., Studies on the fossil snake Dinilysia patagonica Woodward. I. Cranial morphology. Bulletin Museum of Comparative Zoology of Harvard University, 119 (1970), 25–74.Google Scholar
Zaher, H. and Scanferla, A., The skull of the Upper Cretaceous snake Dinilysia patagonica Smith-Woodward, 1901, and its phylogenetic position revisited. Zoological Journal of the Linnean Society, 164 (2012), 194–238.CrossRefGoogle Scholar
Iwaniuk, A. N., Hurd, P. L., and Wylie, D. R., Comparative morphology of the avian cerebellum: II. Size of folia. Brain, Behavior, and Evolution, 69 (2007), 196–219.CrossRefGoogle ScholarPubMed
Macrì, S., Savriama, Y., Khan, I., and Di-Poï, N., Comparative analysis of squamate brains unveils multi-level variation in cerebellar architecture associated with locomotor specialization. Nature Communications, 10 (2019), 5560.Google Scholar
Hanken, J. and Wake, D. B., Miniaturization of body size: organismal consequences and evolutionary significance. Annual Review of Ecology, Evolution, and Systematics, 24 (1993), 501–519.Google Scholar
Maddin, H. C., Olori, J. C., and Anderson, J. S., A redescription of Carrolla craddocki (Lepospondyli: Brachystelechidae) based on high-resolution CT, and the impacts of miniaturization and fossoriality on morphology. Journal of Morphology, 272 (2011), 722–743.Google Scholar
Lieberman, D. E., Hallgrímsson, B., Liu, W., Parsons, T. E., and Jamniczky, H. A., Spatial packing, cranial base angulation, and craniofacial shape variation in the mammalian skull: testing a new model using mice. Journal of Anatomy, 212 (2008), 720–735.Google Scholar
Senn, D. G. and Northcutt, R. N., The forebrain and midbrain of some squamates and their bearing on the origin of snakes. Journal of Morphology, 140 (1973), 153–152.Google Scholar
Reperant, O. J., Miceli, D., Rio, J.-P., and Weidner, C., The primary optic system in a microphthalmic snake (Calabaria reinhardtii). Brain Research, 408, 233–238.CrossRefGoogle Scholar
Reperant, O. J., Rio, J.-P., Ward, R., et al., Comparative analysis of the primary visual system of reptiles. In Gans, C. and Ulinski, P. S., eds., Sensory Integration. Biology of the Reptilia, Vol. 17, Neurology C (Chicago and London: The University of Chicago Press, 1992) pp. 175–240.Google Scholar
Platel, R., Analyse volumétrique comparée des principales subdivisions télencephaliques chez les reptiles saurines. Journal für Hirnforschung, 21 (1980), 271–291.Google Scholar
Northcutt, R. G., Forebrain and midbrain organization in lizards and its phylogenetic significance. In Greenberg, N. and Maclean, P. D., eds., Behavior and Neurology of Lizards (Rockeville: NIMH, 1978), pp. 11–64.Google Scholar
Gharzi, A., Abbasi, M., and Yusefi, P., Histological studies on the vomeronasal organ of the worm-like snake, Typhlops vermicularis. Journal of Biological Sciences, 13 (2013), 372–378.Google Scholar
Webb, J. K. and Shine, R., To find an ant: trail-following in Australian blindsnakes (Typhlopidae). Animal Behaviour, 43 (1992), 941–948.CrossRefGoogle Scholar
Masai, H., Structural patterns of the optic tectum in Japanese snakes of the family Colubridae in relation to habit. Journal für Hirnforschung, 14 (1973), 367–374.Google Scholar
Catania, K. C., The brain and behavior of the tentacled snake. Annals of New York Academy of Sciences, 1225 (2011), 83–89.Google Scholar
Butler, A. B. and Hodos, W., Comparative Vertebrate Neuroanatomy: Evolution and Adaptation (Hoboken: John Wiley, 2005).Google Scholar
Christensen, C. B., Christensen-Dalsgaard, J., Brandt, C., and Madsen, P. T., Hearing with an atympanic ear: good vibration and poor sound-pressure detection in the royal python, Python regius. Journal of Experimental Biology, 215 (2012), 331–342.Google Scholar
Larsell, O.. The cerebellum of reptiles: lizards and snake. The Journal of Comparative Neurology, 41 (1926) 59–94.Google Scholar
Caldwell, M. W., The Origin Of Snakes: Morphology and the Fossil Record (Boca Raton: Taylor & Francis, 2019).Google Scholar
Palci, A., Hutchinson, M. N., Caldwell, M. W., and Lee, M. S. Y., The morphology of the inner ear of squamate reptiles and its bearing on the origin of snakes. Royal Society Open Science, 4 (2017), 170685.Google Scholar
Garberoglio, F. F., Apesteguia, S., Simoes, T., et al., New skulls and skeletons of the Cretaceous legged snake Najash, and the evolution of the modern snake body plan. Science Advances, 5 (2019), eaax5833.Google Scholar
Garberoglio, F. F., Gómez, R. O., Apesteguia, S., et al., A new specimen with skull and vertebrae of Najash rionegrina (Lepidosauria: Ophidia) from the early Late Cretaceous of Patagonia. Journal of Systematic Palaeontology, 17 (2019), 1533–1550.Google Scholar
Yi, H. and Norell, M. A., The burrowing origin of modern snakes. Science Advances, 1 (2015), e1500743.Google Scholar
Scanferla, A. and Bhullar, B. A. S., Postnatal development of the skull of Dinilysia patagonica (Squamata-Stem Serpentes). The Anatomical Record, 297 (2014), 560–573.Google Scholar
Scanferla, A., Postnatal ontogeny and the evolution of macrostomy in snakes. Royal Society Open Science, 3 (2016), 160612.Google Scholar
Caldwell, M. W. and Albino, A. M., Palaeoenvironment and palaeoecology of three Cretaceous snakes: Pachyophis, Pachyrhachis, and Dinilysia. Acta Palaeontologica Polonica, 46 (2001), 203–218.Google Scholar
Walls, G. L., Ophthalmological implications for the early history of the snakes. Copeia 1940 (1940), 1–8.Google Scholar
Underwood, G., The eye. In Gans, C. and Parsons, T.S., eds., Biology of the Reptilia, Vol. 2, Morphology B (New York: Academic Press, 1970), pp. 1–97.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
Miralles, A., Marin, L., 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
Hsiang, A. Y., Field, D. J., Webster, T. H., et al., The origin of snakes: revealing the ecology, behavior, and evolutionary history of early snakes using genomics, phenomics, and the fossil record. BMC Evolutionary Biology, 15 (2015), 87.Google Scholar
Da Silva, F. O., Fabre, A.-C., Savriama, Y., et al., The ecological origins of snakes as revealed by skull evolution. Nature Communications, 9 (2018), 376.Google Scholar
Zaher, H., Murphy, R. W., Arredondo, J. C., et al., Large-scale molecular phylogeny, morphology, divergence-time estimation, and the fossil record of advanced caenophidian snakes (Squamata: Serpentes). PLoS ONE, 14 (2019), e0216148.Google Scholar

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