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-6587cd75c8-r56mn Total loading time: 0 Render date: 2025-04-23T11:28:46.508Z Has data issue: false hasContentIssue false

19 - Macrostomy, Macrophagy, and Snake Phylogeny

from Part V - Anatomical and Functional Morphological Perspectives

Published online by Cambridge University Press:  30 July 2022

By
David Cundall  and
Frances Irish
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

Some snakes are the only vertebrates able to engulf prey with cross-sectional areas several times larger than the area encompassed by the snake’s jaws at peak gape. This ability is conferred by modifying soft tissues ventral to the axial musculoskeletal system for extraordinary extensibility between the mandibles and stomach. Moving large prey into the gut depends on structural decoupling of toothed jaws from the braincase. In all living snakes, kinetic jaws form mobile ratchets. In scolecophidians, transverse maxillary or dentary ratchets have evolved to move small prey into the gut. In alethinophidians, longitudinal palatopterygoid ratchets move the head and body of the snake over the prey. Evidence from extant snakes shows that streptostyly, prokinesis, rhinokinesis and loss of all ventral skeletal elements connected to the axial skeleton were critical to evolution of the upper-jaw ratchet on which macrostomy is based. The existing fossil record gives tantalizing clues that suggest the ancestor of snakes might have been macrostomous. Resolution of this issue will require structural details of the snout, braincase, and toothed ratchets in both ‘basal’ extant snakes and fossils.

Keywords

adaptationevolutiondietecologyfunctional morphologyfeedingskullmandiblemusculosketal systemMacrostomata
Type
Chapter
Information
The Origin and Early Evolutionary History of Snakes , pp. 437 - 454
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.)

Book purchase

Temporarily unavailable

References

Cundall, D. and Greene, H. W., Feeding in snakes. In Schwenk, K., ed., Feeding: Form, Function, and Evolution in Tetrapod Vertebrates (San Diego, CA: Academic Press, 2000), pp. 293–333.CrossRefGoogle 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
Moon, B. R., Penning, D. A., Segall, M., and Herrel, A., Feeding in snakes: Form, function, and evolution of the feeding system. In Bels, V. and Whishaw, I. Q., eds., Feeding in Vertebrates: Evolution, Morphology, Behaviour, Biomechanics (Switzerland: Springer Nature, 2019), pp. 527–574.Google Scholar
Greene, H. W., Snakes: The Evolution of Mystery in Nature (Berkeley, CA: University of California Press, 1997).Google Scholar
Rieppel, O., A review of the origin of snakes. Evolutionary Biology, 22 (1988), 37–130.Google Scholar
Müller, J., Beiträge zur Anatomie und Naturgeschichtte der Amphibien. Zeitschrift für Physiologie, 4 (1832), 190–275.Google Scholar
Harrington, S. and Reeder, T., Phylogenetic inference and divergence dating of snakes using molecules, morphology and fossils: new insights into convergent evolution of feeding morphology and limb reduction. Biological Journal of the Linnean Society, 121 (2017), 379–394.Google Scholar
Burbrink, F. T., Grazziotin, F. G., Pyron, R. A., et al., Interrogating genomic-scale data for Squamata (lizards, snakes, and amphisbaenians) shows no support for key traditional morphological relationships. Systematic Biology, 69 (2020), 502–520.Google Scholar
Caldwell, M. W., The Origin of Snakes: Morphology and the Fossil Record (Boca Raton, FL: CRC Press, 2020).Google Scholar
Greene, H. W., Dietary correlates of the origin and radiation of snakes. American Zoologist, 23 (1983), 431–441.CrossRefGoogle Scholar
Hsiang, A. Y., Field, D. J., Webster, T. H., et al., The origin of snakes: revealing the ecology, behaviour, and evolutionary history of early snakes using genomics, phenomics, and the fossil record. BMC Evolutionary Biology, 15 (2015), 87.Google Scholar
Scanferla, A., Post-natal ontogeny and the evolution of macrostomy in snakes. Royal Society Open Science, 3 (2016), 160612.Google Scholar
Bezuijen, M. R., Field observation of a large prey item consumed by a small Cylindrophis ruffus (Laurenti, 1768) (Serpentes: Cylindrophiidae). Hamadryad, 34 (2009), 185–187.Google Scholar
Kusamba, C., Resetar, A., Wallach, V., Lulengo, K., and Nagy, Z. T., Mouthful of snake: An African snake-eater’s (Polemon fulvicollis graueri) large typhlopid prey. Herpetology Notes, 6 (2013), 235–237.Google Scholar
Jackson, K., Kley, N. J., and Brainerd, E. L., How snakes eat snakes: the biomechanical challenges of ophiophagy for the California kingsnake, Lampropeltis getula californiae (Serpentes: Colubridae). Zoology, 107 (2004), 191–200.CrossRefGoogle ScholarPubMed
Cundall, D., A few puzzles in the evolution of feeding mechanisms in snakes. Herpetologica, 75 (2019), 99–107.Google Scholar
Schwenk, K. and Rubega, M., Diversity of vertebrate feeding systems. In Stark, J. M. and Wang, T., eds., Physiological and ecological adaptations to feeding in vertebrates (Enfield, NH: Science Publishers, 2005), pp. 1–41.Google Scholar
Jayne, B. C., Voris, H. K., and Ng, P. K. L., How big is too big? Using crustacean-eating snakes (Homalopsidae) to test how anatomy and behavior affect prey size and feeding performance. Biological Journal of the Linnean Society, 123 (2018), 636–650.CrossRefGoogle Scholar
Gripshover, N. H. and Jayne, B. C., Crayfish eating in snakes: testing how anatomy and behavior affect prey size and feeding performance. Integrative Organismal Biology, 3 (2021), obab001.CrossRefGoogle ScholarPubMed
Close, M. and Cundall, D., Snake lower jaw skin: Extension and recovery of a hyperextensible keratinized integument. Journal of Experimental Zoology, 321A (2014), 78–97.CrossRefGoogle Scholar
Close, M., Perni, S., Franzini-Armstrong, C.,, and Cundall, D., Highly extensible skeletal muscle in snakes. Journal of Experimental Biology, 217 (2014), 2445–2448.Google Scholar
Young, B. A., The arthrology of the head of the Red-sided Garter snake, Thamnophis sirtalis parietalis . Netherlands Journal of Zoology, 38 (1988), 166–205.CrossRefGoogle Scholar
Young, B. A., The comparative morphology of the intermandibular connective tissue in snakes (Reptilia: Squamata). Zoologischer Anzeiger, 237 (1998), 59–84.Google Scholar
Young, B. A. The comparative morphology of the mandibular midline raphe in snakes (Reptilia: Squamata). Zoologischer Anzeiger, 237 (1998–1999), 217–241.Google Scholar
Cundall, D. and Beaupre, S. J., Field records of predatory strike kinematics in rattlesnakes, Crotalus horridus . Amphibia-Reptilia, 22 (2001), 492–498.Google Scholar
Cundall, D., Viper fangs: Functional limitations of extreme teeth, Physiological and Biochemical Zoology: Ecological and Evolutionary Approaches, 82 (2009), 63–79.Google Scholar
Gauthier, J. A., Kearney, M., Maisano, J. A., Rieppel, O., and Behlke, D. B., Assembling the squamate tree of life: Perspectives from the phenotype and the fossil record. Bulletin of the Peabody Museum of Natural History, 53 (2012), 3–308.Google Scholar
Greer, A. E., Limb reduction in squamates: Identification of the lineages and discussion of the trends. Journal of Herpetology, 25 (1991), 166–173.Google Scholar
Tsuihiji, T., Kearney, M., and Rieppel, O., First report of a pectoral girdle muscle in snakes, with comments on the snake cervico-dorsal boundary. Copeia, 2006 (2006), 206–215.CrossRefGoogle Scholar
Tsuihiji, T., Kearney, M., and Rieppel, O., Finding the neck-trunk boundary in snakes: Anteroposterior dissociation of myological characteristics in snakes and its implications for their neck and trunk body regionalization. Journal of Morphology, 273 (2012), 992–1009.Google Scholar
Leal, F. and Cohn, M. J., Developmental, genetic, and genomic insights into the evolutionary loss of limbs in snakes. Genesis: The Journal of Genetics and Development, 56 (2018), e23077.Google Scholar
Gasc, J.-P., Axial musculature. In Gans, C. and Parsons, T. S., eds., Biology of the Reptilia, Vol. 11, Morphology F (London: Academic Press, 1981), pp. 355–435.Google Scholar
Rivera, G., Savitzky, A. H., and Hinkley, J. A., Mechanical properties of the integument of the common gartersnake, Thamnophis sirtalis (Serpentes: Colubridae). Journal of Experimental Biology, 208 (2005), 2913–2922.Google Scholar
Buffa, P., Ricerche sulla muscolatura cutanea dei serpenti e considerazioni sulla locomozione di questi animali. Atti della Accademia scientifica veneto-trentino-istriana, 1 (1904), 145–237.Google Scholar
Fetcho, J. R., The organization of motor neurons innervating the axial musculature of vertebrates. II. Florida water snakes (Nerodia fasciata pictiventris). Journal of Comparative Neurology, 249 (1986), 551–563.Google Scholar
Vogl, A. W., Lillie, M. A., Piscitelli, M. A., et al., Stretchy nerves are an essential component of the extreme feeding mechanism of rorqual whales. Current Biology, 25 (2015), R345–R361.Google Scholar
Apodaca, G., The uroepithelium: Not just a passive barrier. Traffic, 5 (2004), 117–128.Google Scholar
Eaton, A. F., Clayton, D. R., Ruiz, W. G., et al., Expansion and contraction of the umbrella cell apical junctional ring in response to bladder filling and voiding. Molecular Biology of the Cell, 30 (2019), 2037–2052.Google Scholar
Burke, A. C. and Nowicki, J. L., A new view of patterning domains in the vertebrate mesoderm. Developmental Cell, 4 (2003), 159–165.Google Scholar
Head, J. J. and Polly, P. D., Evolution of the snake body form reveals homoplasy in amniote Hox gene function. Nature, 520 (2015), 86–89.Google Scholar
Mosauer, W., The myology of the trunk region of snakes and its significance for ophidian taxonomy and phylogeny. Publications of the University of California at Los Angeles in Biological Sciences, 1 (1935), 81–120.Google Scholar
Ottaviani, G. and Tazzi, A., The lymphatic system. In Gans, C. and Parsons, T. S., eds., Biology of the Reptilia, Vol. 6, Morphology E (London: Academic Press, 1977), pp. 315–464.Google Scholar
Cundall, D., Tuttman, C., and Close, M., A model of the anterior esophagus in snakes, with functional and developmental implications. Anatomical Record, 297 (2014), 586–598.Google Scholar
Yi, H. and Norell, M. A., The burrowing origin of modern snakes. Science Advances, 1 (2015), e1500743.CrossRefGoogle ScholarPubMed
Lee, M. S. Y., Convergent evolution and character correlation in burrowing reptiles: towards a resolution of squamate relationships. Biological Journal of the Linnean Society, 65 (1998), 369–453.CrossRefGoogle Scholar
McDowell, S. B., Jr., The skull of Serpentes. In Gans, C., Gaunt, A. S., and Adler, K., eds., Biology of the Reptilia, Vol. 21, Morphology I. (Ithaca, NY: Society for the Study of Amphibians and Reptiles, 2008), pp. 467–620.Google Scholar
Abdeen, A. M., Abo-Taira, A. M., and Zaher, M. M, Further studies on the ophidian cranial osteology: the skull of the Egyptian blind snake Leptotyphlops cairi (Leptotyphlopidae). I. The cranium. A – The median dorsal bones, bones of the upper jaw, circumorbital bone and occipital ring. Journal of the Egyptian-German Society of Zoology, 5 (1991), 417–437.Google Scholar
Abdeen, A. M., Abo-Taira, A. M., and Zaher, M. M, Further studies on the ophidian cranial osteology: The skull of the Egyptian blind snake Leptotyphlops cairi (Leptotyphlopidae). I. The cranium. B – The otic capsule, palate and temporal bones. Journal of the Egyptian-German Society of Zoology, 5 (1991), 439–455.Google Scholar
Broadley, D. G. and Broadley, S., A review of the African worm snakes from south of latitude 12°S (Serpentes: Leptotyphlopidae). Syntarsus, 5 (1999), 1–36.Google Scholar
Boughner, J. C., Buchtova, M., Fu, K., et al., Embryonic development of Python sebae. I. Staging criteria and macroscopic skeletal morphogenesis of the head and limbs. Zoology, 110 (2007), 212–230.Google Scholar
Boback, S. M., Dichter, E. K., and Mistry, H. L., A developmental staging series for the African house snake, Boaedon (Lamprophis) fuliginosus . Zoology, 115 (2012), 38–46.Google Scholar
Polachowski, K. M. and Werneburg, I., Late embryos and bony skull development in Bothropoides jararaca (Serpentes, Viperidae). Zoology, 116 (2013), 36–63.Google Scholar
Khannoon, E. R. and Evans, S. E., The development of the skull of the Egyptian cobra Naja h. haje (Squamata: Serpentes: Elapidae). PLoS ONE, 10 (2015), e0122185.Google Scholar
Irish, F. J., The role of heterochrony in the origin of a novel bauplan: evolution of the ophidian skull. Geobios, Mémoires Special, 12 (1989), 227–233.CrossRefGoogle Scholar
Werneburg, I., Polachowski, K. M., and Hutchinson, M. N., Bony skull development in the Argus Monitor (Squamata, Varanidae, Varanus panoptes) with comments on developmental timing and adult anatomy. Zoology, 118 (2015), 255–280.Google Scholar
Kley, N. J. and Brainerd, E. L., Post-cranial prey transport mechanisms in the black pinesnake, Pituophis melanoleucus lodingi: an x-ray videographic study. Zoology, 105 (2002), 153–164.CrossRefGoogle ScholarPubMed
Kiran, U., A new structure in the lower jaw of colubrid snakes. Snake, 13 (1981), 131–133.Google Scholar
Cundall, D., Feeding behaviour in Cylindrophis and its bearing on the evolution of alethinophidian snakes. Journal of Zoology, London, 237 (1995), 353–376.Google Scholar
Kley, N. J., Prey transport mechanisms in blindsnakes and the evolution of unilateral feeding systems in snakes. American Zoologist, 41 (2001), 1321–1337.Google Scholar
Schwenk, K., Feeding in lepidosaurs. In Schwenk, K., ed., Feeding: Form, Function, and Evolution in Tetrapod Vertebrates (San Diego, CA: Academic Press, 2000), pp. 175–291.Google Scholar
Frazzetta, T. H., A functional consideration of cranial kinesis in lizards. Journal of Morphology, 111 (1962), 287–320.CrossRefGoogle ScholarPubMed
Frazzetta, T. H., Morphology and function of the jaw apparatus in Python sebae and Python molurus . Journal of Morphology, 118 (1966), 217–296.Google Scholar
Cundall, D. and Shardo, J., Rhinokinetic snout of thamnophiine snakes. Journal of Morphology, 225 (1995), 31–50.Google Scholar
Shcherbakov, D. E., Tim, T., Tzetlin, A. B., Vinn, O., and Zhuravlev, A. Y., A probable oligochaete from an Early Triassic Lagerstätte of the southern Cis-Urals and its evolutionary implications. Acta Palaeontologica Polonica, 65 (2020), 219–233.CrossRefGoogle Scholar
Zaher, H. and Scanferla, C. 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.Google Scholar
Gower, D. J., Giri, V., Captain, A., , and Wilkinson, M., A reassessment of Melanophium Günther, 1864 (Squamata: Serpentes: Uropeltidae) from the Western Ghats of peninsular India, with description of a new species. Zootaxa, 4085 (2016), 481–503.Google Scholar
Boltt, R. E. and Ewer, R. F., The functional anatomy of the head of the puff adder, Bitis arietans (Merr.). Journal of Morphology, 114 (1964), 83–106.Google Scholar
Greene, H. W. and Burghardt, G. M., Behaviour and phylogeny: Constriction in ancient and modern snakes. Science, 200 (1978), 74–77.CrossRefGoogle ScholarPubMed
Head, J. J., Mahlow, K., and Müller, J., Fossil calibration dates for molecular phylogenetic analysis of snakes 2: Caneophidia, Colubroidea, Elapoidea, Colubridae. Palaeontologia Electronica 19.2.2FC (2016), 1–21.CrossRefGoogle Scholar
Hargreaves, A. D., Swain, M. T., Logan, D. W., and Mulley, J. F., Testing the Toxicofera: Comparative transcriptomics casts doubt on the single, early evolution of the reptile venom system. Toxicon, 92 (2015), 140–156.Google Scholar
Sweet, S. S., Chasing flamingos: Toxicofera and the misinterpretation of venom in varanid lizards. In Cota, M., ed., Proceedings of the 2015 Interdisciplinary World Conference on Monitor Lizards (Bangkok, Thailand: Institute for Research and Development, Suan Sunandha Rajhabat University, 2016), pp. 123–149.Google Scholar
Radcliffe, C. W. and Chiszar, D. A., A descriptive analysis of predatory behavior in the yellow-lipped sea krait (Laticauda colubrina). Journal of Herpetology, 14 (1980), 422–424.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., and Smith, K. T., Pythons in the Eocene of Europe reveal a much older divergence of the group in sympatry with boas. Biology Letters, 16 (2020), 20200735.Google Scholar
Rage, J.-C., Serpentes, In Wellnhofer, P., ed., Handbuch der Paläoherpetologie/ Encyclopedia of Paleontology, Part 11 . (Stuttgart: Gustav Fischer, 1984), pp. 1–80.Google Scholar
Rage, J.-C., Fossil snakes. In Seigel, R. A., Collins, J. T., and Novak, S. S., eds., Snakes: Ecology and Evolutionary Biology (New York: Macmillan, 1987), pp. 51–76.Google Scholar
Rieppel, O., H., Zaher, E. Tchernov, ,, and Polcyn, M. J., The anatomy and relationships of Haasiophis terrasanctus, a fossil snake with well-developed hind limbs from the mid-Cretaceous of the Middle East. Journal of Paleontology, 77 (2003), 536–558.Google Scholar
Zaher, H., Apesteguía, S., and Scanferla, C. A., The anatomy of the upper cretaceous snake Najash rionegrina Apesteguía & Zaher, 2006, and the evolution of limblessness in snakes. Zoological Journal of the Linnean Society, 156 (2009), 801–826.Google Scholar
Garberoglio, F. F., Apesteguía, S., Simões, T. R., 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
Cundall, D., Review of Caldwell, M. W., the origin of snakes: morphology and the fossil record. Herpetological Review, 51 (2020), 364–368.Google Scholar
Koch, N. M. and Gauthier, J. A., Noise and biases in genomic data may underlie radically different hypotheses for the position of Iguania within Squamata. PLoS ONE, 13 (2018), e0202729.Google Scholar
Uetz, P., Freed, P., and Hosek, J., eds., The Reptile Database. www.reptile-database.org (accessed 1 February 2021).Google Scholar

Accessibility information

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
×