The burrowing origin of modern snakes

Yi, Haiyang; Norell, Mark A.

doi:10.1126/sciadv.1500743

Cited by 86 publications

(115 citation statements)

References 24 publications

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“…The morphology of its endosseous labyrinth with short semicircular canals oriented at high angles to each other and the large cavum nasi proprium (Parsons, 1970;David et al, 2010;Paulina-Carabajal et al, 2017) agree with these previous studies, strongly supporting the interpretation that P. quenstedti was a well-adapted terrestrial turtle. However, since its vestibule is not particularly large, in contrast to the condition of truly fossorial taxa (Yi and Norell, 2015) or of the semi-fossorial tortoise Gopherus (Paulina- Carabajal et al, 2017), the present data suggest it was likely not a fossorial taxon. In P. quenstedti, the relatively enlarged vestibule in comparison to the other turtles in this study results from the relatively small semicircular canals.…”

Section: Evolution Of the Turtle Brain Endocastmentioning

confidence: 57%

Sensory Evolution and Ecology of Early Turtles Revealed by Digital Endocranial Reconstructions

2018

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In the past few years, new fossil finds and novel methodological approaches have prompted intensive discussions about the phylogenetic affinities of turtles and rekindled the debate on their ecological origin, with very distinct scenarios, such as fossoriality and aquatic habitat occupation, proposed for the earliest stem-turtles. While research has focused largely on the origin of the anapsid skull and unique postcranial anatomy, little is known about the endocranial anatomy of turtles. Here, we provide 3D digital reconstructions and comparative descriptions of the brain, nasal cavity, neurovascular structures and endosseous labyrinth of Proganochelys quenstedti, one of the earliest stem-turtles, as well as other turtle taxa. Our results demonstrate that P. quenstedti retained a simple tube-like brain morphology with poorly differentiated regions and mediocre hearing and vision, but a well-developed olfactory sense. Endocast shape analysis indicates that an increase in size and regionalization of the brain took place in the course of turtle evolution, achieving an endocast diversity comparable to other amniote groups. Based on the new evidence presented herein, we further conclude that P. quenstedti was a highly terrestrial, but most likely not fossorial, taxon.

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Section: Evolution Of the Turtle Brain Endocastmentioning

confidence: 57%

Sensory Evolution and Ecology of Early Turtles Revealed by Digital Endocranial Reconstructions

2018

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“…Some of these may be an adaptation to the underground life (dibamids, amphisbaenids, pygopodids). Indeed, the view that snakes evolved probably from a burrowing or semi-burrowing ancestors is supported by morphological [95, 96] and molecular data [97]. According to the current knowledge, it seems that the main groups snakes are rather evolutionarily conservative in respect to the anatomy of the VNO and associated structures.…”

Section: Discussionmentioning

confidence: 99%

Embryology of the VNO and associated structures in the grass snake Natrix natrix (Squamata: Natricinae): a 3D perspective

2017

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BackgroundSnakes are considered to be vomerolfaction specialists. They are members of one of the most diverse groups of vertebrates, Squamata. The vomeronasal organ and the associated structures (such as the lacrimal duct, choanal groove, lamina transversalis anterior and cupola Jacobsoni) of adult lizards and snakes have received much anatomical, histological, physiological and behavioural attention. However, only limited embryological investigation into these structures, constrained to some anatomical or cellular studies and brief surveys, has been carried out thus far. The purpose of this study was, first, to examine the embryonic development of the vomeronasal organ and the associated structures in the grass snake (Natrix natrix), using three-dimensional reconstructions based on histological studies, and, second, to compare the obtained results with those presented in known publications on other snakes and lizards.ResultsFive major developmental processes were taken into consideration in this study: separation of the vomeronasal organ from the nasal cavity and its specialization, development of the mushroom body, formation of the lacrimal duct, development of the cupola Jacobsoni and its relation to the vomeronasal nerve, and specialization of the sensory epithelium. Our visualizations showed the VNO in relation to the nasal cavity, choanal groove, lacrimal duct and cupola Jacobsoni at different embryonic stages. We confirmed that the choanal groove disappears gradually, which indicates that this structure is absent in adult grass snakes. On our histological sections, we observed a gradual growth in the height of the columns of the vomeronasal sensory epithelium and widening of the spaces between them.ConclusionsThe main ophidian taxa (Scolecophidia, Henophidia and Caenophidia), just like other squamate clades, seem to be evolutionarily conservative at some levels with respect to the VNO and associated structures morphology. Thus, it was possible to homologize certain embryonic levels of the anatomical and histological complexity, observed in the grass snake, with adult conditions of certain groups of Squamata. This may reflect evolutionary shift in Squamata from visually oriented predators to vomerolfaction specialists. Our descriptions offer material useful for future comparative studies of Squamata, both at their anatomical and histological levels.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-017-0188-y) contains supplementary material, which is available to authorized users.

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“…Beyond this systematic application, new data on inner ears have potential to shed light on additional aspects of early neopterygian biology. Semicircular canal morphology has been shown to correlate with functional and ecological specialisation in a great variety of tetrapod groups (e.g., charadriiform birds: Smith and Clarke, ; hominids: Spoor et al, ; mustelid nannaks: Grohé et al ; rodents: Pfaff et al, ; snakes: Yi and Norell, ). Few data exist to test this hypothesis in fishes, although Gauldie and Radtke () found evidence that the labyrinth morphology of the walking catfish Clarius fuscus , which is able to spend time on land, is more similar to those of terrestrial vertebrates than other fishes, suggesting that its inner ear shows adaptations toward a swaying (i.e., walking‐like) rather than undulatory (i.e., swimming‐like) gait.…”

Section: Discussionmentioning

confidence: 99%

Bony labyrinth morphology in early neopterygian fishes (Actinopterygii: Neopterygii)

Giles

Rogers

Friedman

2016

Journal of Morphology

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Endocasts of the osseous labyrinth have the potential to yield information about both phylogenetic relationships and ecology. Although bony labyrinth morphology is well documented in many groups of fossil vertebrates, little is known for early Neopterygii, the major fish radiation containing living teleosts, gars and the bowfin. Here, we reconstruct endocasts of the bony labyrinth and associated structures for a sample of Mesozoic neopterygian fishes using high-resolution computed tomography. Our sample includes taxa unambiguously assigned to either the teleost (Dorsetichthys, "Pholidophorus," Elopoides) and holostean ("Aspidorynchus," "Caturus," Heterolepidotus) total-groups, as well as examples of less certain phylogenetic position (an unnamed parasemionotid and Dapedium). Our models provide a test of anatomical interpretations for forms where bony labyrinths were reconstructed based on destructive tomography ("Caturus") or inspection of the lateral wall of the cranial chamber (Dorsetichthys), and deliver the first detailed insights on inner ear morphology in the remaining taxa. With respect to relationships, traits apparent in the bony labyrinth and associated structures broadly support past phylogenetic hypotheses concerning taxa agreed to have reasonably secure systematic placements. Inner ear morphology supports placement of Dapedium with holosteans rather than teleosts, while preserved structure in the unnamed parasemionotid is generalized to the degree that it provides no evidence of close affinity with either of the crown neopterygian lineages. This study provides proof-of-concept for the systematic utility of the inner ear in neopterygians that, in combination with similar findings for earlier-diverging actinopterygian lineages, points to the substantial potential of this anatomical system for addressing the longstanding questions in the relationships of fossil ray-finned fishes to one another and living groups. J. Morphol. 279:426-440, 2018. © 2016 Wiley Periodicals, Inc.

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The burrowing origin of modern snakes

Abstract: Modern snakes originated from burrowing ancestors, predicted from the evolution of their inner ear.

Cited by 86 publications

References 24 publications

Sensory Evolution and Ecology of Early Turtles Revealed by Digital Endocranial Reconstructions

Sensory Evolution and Ecology of Early Turtles Revealed by Digital Endocranial Reconstructions

Embryology of the VNO and associated structures in the grass snake Natrix natrix (Squamata: Natricinae): a 3D perspective

Bony labyrinth morphology in early neopterygian fishes (Actinopterygii: Neopterygii)

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