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11 - The Evolution of Squamate Chitinase Genes (CHIAs) Supports an Insectivory–Carnivory Transition during the Early History of Snakes

from Part III - Genomic Perspectives

Published online by Cambridge University Press:  30 July 2022

By
Christopher A. Emerling
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

Genomic studies have elucidated some molecular underpinnings for adaptations during the early history of snakes, but studies of dietary adaptations remain sparse. Snakes differ from most other squamates by tending towards diets of vertebrate prey (carnivory), whereas arthropods are common in diets of most other squamates (insectivory). To test whether a shift from insectivory to carnivory occurred early in snake history, I examined chitinase genes (CHIAs) in 19 squamates. Previous studies on mammals found that contraction in the number of CHIAs, which enzymatically digest arthropod chitinous exoskeletons, correlates with transitions from insectivory to carnivory or herbivory. I found evidence that CHIAs have a long history in Squamata, with at least seven paralogs inferred in their last common ancestor. Retention of these CHIAs seems to be commonplace for arthropod-eating squamates, but snakes likely lost six CHIAs between diverging from other toxicoferans and the origin of afrophidian snakes. This genomic signal corresponds with an inferred major shift towards carnivory during the origin and evolution of early snakes, which may have contributed to their successful radiation.

Keywords

comparative genomicsdietadaptationgenomesSquamataevolutionbioinformatics
Type
Chapter
Information
The Origin and Early Evolutionary History of Snakes , pp. 235 - 247
Publisher: Cambridge University Press
Print publication year: 2022

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References

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
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
Ullate-Agote, A., Milinkovitch, M. C., and Tzikia, A. C., The genome sequence of the corn snake (Pantherophis guttatus), a valuable resource for EvoDevo studies in squamates. International Journal of Developmental Biology, 58 (2014), 881–888.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
Infante, C. R., Mihala, A. G., Park, S., et al., Shared enhancer activity in the limbs and phallus and functional divergence of a limb-genital cis-regulatory element in snakes. Developmental Cell, 35 (2015), 107–119.Google Scholar
Kvon, E. Z., Kamneva, O. K., Melo, U. S., et al., Progressive Loss of function in a limb enhancer during snake evolution. Cell, 167 (2016), 633-642.e11.Google Scholar
Kishida, T., Go, Y., Tatsumoto, S., et al., Loss of olfaction in sea snakes provides new perspectives on the aquatic adaptation of amniotes. Proceedings of the Royal Society B, 286 (2019), 2019.1828.Google Scholar
Zhong, H., Shang, S., Wu, X., et al., Genomic evidence of bitter taste in snakes and phylogenetic analysis of bitter taste receptor genes in reptiles. PeerJ, 5 (2017), e3708.Google Scholar
Perry, B. W., Card, D. C., McGlothlin, 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.Google Scholar
Meiri, S., Traits of lizards of the world: Variation around a successful evolutionary design. Global Ecology and Biogeography, 27 (2018), 1168–1172.Google Scholar
Grundler, M. C., SquamataBase: A natural history database and R package for comparative biology of snake feeding habits. Biodiversity Data Journal, 8 (2020), e49943.Google Scholar
Rowe, T., DigiMorph. www.DigiMorph.org (2020)Google Scholar
Chenand, Y. H., and Zhao, H., Evolution of digestive enzymes and dietary diversification in birds. PeerJ, 7 (2019), e6840.Google Scholar
German, D. P., Nagle, B. C., Villeda, J. M., et al., Evolution of herbivory in a carnivorous clade of minnows (Teleostei: Cyprinidae): Effects on gut size and digestive physiology. Physiological and Biochemical Zoology, 83 (2010), 1–18.Google Scholar
Jeuniaux, C., Chitinase: an addition to the list of hydrolases in the digestive tract of vertebrates. Nature, 192 (1961), 135–136.Google Scholar
Emerling, C. A., Delsuc, F., and Nachman, M. W., Chitinase genes (CHIAs) provide genomic footprints of a post-Cretaceous dietary radiation in placental mammals. Science Advances, 4 (2018), eaar6478.Google Scholar
Janiak, M. C., Chaney, M. E., and Tosi, A. J., Evolution of acidic mammalian chitinase genes (CHIA) is related to body mass and insectivory in primates. Molecular Biology and Evolution, 35 (2018), 607–622.Google Scholar
Wang, K., Tian, S., Galindo-González, J., et al., Molecular adaptation and convergent evolution of frugivory in Old World and neotropical fruit bats. Molecular Ecology, 29 (2020), 4366–4381.CrossRefGoogle ScholarPubMed
Boot, R. G., Blommaart, E. F. C., Swart, E., et al., Identification of a novel acidic mammalian chitinase distinct from chitotriosidase. Journal of Biological Chemistry, 276 (2001), 6770–6778.Google Scholar
Strobel, S., Roswag, A., Becker, N. I., Trenczek, T. E., and Encarnação, J. A., Insectivorous bats digest chitin in the stomach using acidic mammalian chitinase. PLoS One, 8 (2013), e72770.Google Scholar
Ohno, M., Kimura, M., Miyakazi, H., et al. Acidic mammalian chitinase is a proteases-resistant glycosidase in mouse digestive system. Scientific Reports, 6 (2016), 37756.CrossRefGoogle ScholarPubMed
Fong, D., Kane, T., and Culver, D., Vestigialization and loss of nonfunctional characters. Annual Review of Ecology and Systematics, 26 (1995), 249–268.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.CrossRefGoogle ScholarPubMed
Meredith, R. W., Zhang, G., Gilbert, M. T. P., Jarvis, E. D., and Springer, M. S., Evidence for a single loss of mineralized teeth in the common avian ancestor. Science, 346 (2014), 1254390.CrossRefGoogle ScholarPubMed
Albalat, R. and Cañestro, C., Evolution by gene loss. Nature Reviews Genetics, 17 (2016), 379–391.Google Scholar
Feng, P., Zheng, J., Rossiter, S. J., Wang, D., and Zhao, H., Massive losses of taste receptor genes in toothed and baleen whales. Genome Biology and Evolution, 6 (2014), 1254–1265.Google Scholar
Marsh, R. S., Moe, C., Lomneth, R. B., Fawcett, J. D., and Place, A., Characterization of gastrointestinal chitinase in the lizard Sceloporus undulatus garmani (Reptilia: Phrynosomatidae). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 128 (2001), 675–682.Google Scholar
Koludarov, I., Jackson, T. N. W., op den Brouw, B., et al., Enter the dragon: The dynamic and multifunctional evolution of Anguimorpha lizard venoms. Toxins, 9 (2017), 242.Google Scholar
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D., Basic local alignment search tool. Journal of Molecular Biology, 215 (1990), 403–410.Google Scholar
Kearse, M., Moir, R., Wilson, A., et al., Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 28 (2012), 1647–1649.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Edgar, R. C., MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32 (2004), 1792–1797.CrossRefGoogle ScholarPubMed
Stamatakis, A., RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30 (2014), 1312–1313.Google Scholar
Olland, A. M., Strand, J., Presman, E., et al., Triad of polar residues implicated in pH specificity of acidic mammalian chitinase. Protein Science, 18 (2009), 569–578.Google Scholar
Tjoelker, L. W., Gosting, L., Frey, S., et al., Structural and functional definition of the human chitinase chitin-binding domain. Journal of Biological Chemistry, 275 (2000), 514–520.Google Scholar
Hussain, M. and Wilson, J. B., New paralogues and revised time line in the expansion of the vertebrate GH18 family. Journal of Molecular Evolution, 76 (2013), 240–260.Google Scholar
Miller, M. A., Pfeiffer, W., and Schwartz, T., Creating the CIPRES Science Gateway for inference of large phylogenetic trees. 2010 Gateway Computing Environments Workshop (GCE) (2010), 1–8.Google Scholar
Chen, J. M., Cooper, D. N., Chuzhanova, N., Férec, C., and Patrinos, G. P., Gene conversion: Mechanisms, evolution and human disease. Nature Reviews Genetics, 8 (2007), 762–775.Google Scholar
Renkema, G. H., Boot, R. G., Au, F. L., et al., Chitotriosidase a chitinase, and the 39-kDa human cartilage glycoprotein, a chitin-binding lectin, are homologues of family 18 glycosyl hydrolases secreted by human macrophages. European Journal of Biochemistry, 251 (1998), 504–509.Google Scholar
Irisarri, I., Baurain, D., Brinkmann, H., et al., Phylotranscriptomic consolidation of the jawed vertebrate timetree. Nature Ecology and Evolution, 1 (2017), 1370–1378.Google Scholar
Zheng, Y. and Wiens, J. J., Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. Molecular Phylogenetics and Evolution, 94 (2016), 537–547.Google Scholar
Lozano-Fernandez, J., Tanner, A. R., Puttick, M. N., et al., A Cambrian–Ordovician terrestrialization of arachnids. Frontiers in Genetics, 11 (2020), 182.Google Scholar
Lins, L. S. F., Ho, S. Y. W., and Lo, N., An evolutionary timescale for terrestrial isopods and a lack of molecular support for the monophyly of Oniscidea (Crustacea: Isopoda). Organisms, Diversity and Evolution, 17 (2017), 813–820.Google Scholar
Misof, B., Liu, S., Meusemann, K., et al., Phylogenomics resolves the timing and pattern of insect evolution. Science, 346 (2014), 763–767.Google Scholar
Fernández, R., Edgecombe, G. D., and Giribet, G., Phylogenomics illuminates the backbone of the Myriapoda Tree of Life and reconciles morphological and molecular phylogenies. Scientific Reports, 8 (2018), 83 CrossRefGoogle ScholarPubMed
Modesto, S. P., Scott, D. M., and Reisz, R. R., Arthropod remains in the oral cavities of fossil reptiles support inference of early insectivory. Biology Letters, 5 (2009), 838–840.Google Scholar
Melstrom, K. M., The relationship between diet and tooth complexity in living dentigerous saurians. Journal of Morphology, 278 (2017), 500–522.Google Scholar
Martill, D. M., Tischlinger, H., and Longrich, N. R., A four-legged snake from the Early Cretaceous of Gondwana. Science, 349 (2015), 416–419.Google Scholar
Caldwell, M. W., Nydam, R. L., Palci, A., and Apesteguía, S., The oldest known snakes from the Middle Jurassic-Lower Cretaceous provide insights on snake evolution. Nature Communications, 6 (2015), 5996.Google Scholar
Longrich, N. R., Bhullar, B. A. S., and Gauthier, J. A., A transitional snake from the Late Cretaceous period of North America. Nature, 488 (2012), 205–208.Google Scholar
Caldwell, M. W. and Lee, M. S. Y., A snake with legs from the marine Cretaceous of the Middle East. Nature, 386 (1997), 705–708.Google Scholar
Haas, G., On a new snakelike reptile from the Lower Cenomanian of Ein Jabrud, near Jerusalem. Bulletin du Muséum National d’Histoire Naturelle Paris, 1 (1979), 51–64.Google Scholar
Wilson, J. A., Mohabey, D. M., Peters, S. E., and Head, J. J., Predation upon hatchling dinosaurs by a new snake from the Late Cretaceous of India. PLoS Biology, 8 (2010), e1000322.CrossRefGoogle ScholarPubMed
Sanders, J. G., Beichman, A. C., Roman, J., et al., Baleen whales host a unique gut microbiome with similarities to both carnivores and herbivores. Nature Communications, 6 (2015), 8285.Google Scholar

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