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Multiple evolutionary origins and losses of tooth complexity in squamates

Author

Listed:
  • Fabien Lafuma

    (Helsinki Institute of Life Science, University of Helsinki)

  • Ian J. Corfe

    (Helsinki Institute of Life Science, University of Helsinki
    Geological Survey of Finland)

  • Julien Clavel

    (Department of Life Sciences, The Natural History Museum
    Univ. Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA)

  • Nicolas Di-Poï

    (Helsinki Institute of Life Science, University of Helsinki)

Abstract

Teeth act as tools for acquiring and processing food, thus holding a prominent role in vertebrate evolution. In mammals, dental-dietary adaptations rely on tooth complexity variations controlled by cusp number and pattern. Complexity increase through cusp addition has dominated the diversification of mammals. However, studies of Mammalia alone cannot reveal patterns of tooth complexity conserved throughout vertebrate evolution. Here, we use morphometric and phylogenetic comparative methods across fossil and extant squamates to show they also repeatedly evolved increasingly complex teeth, but with more flexibility than mammals. Since the Late Jurassic, multiple-cusped teeth evolved over 20 times independently from a single-cusped common ancestor. Squamates frequently lost cusps and evolved varied multiple-cusped morphologies at heterogeneous rates. Tooth complexity evolved in correlation with changes in plant consumption, resulting in several major increases in speciation. Complex teeth played a critical role in vertebrate evolution outside Mammalia, with squamates exemplifying a more labile system of dental-dietary evolution.

Suggested Citation

  • Fabien Lafuma & Ian J. Corfe & Julien Clavel & Nicolas Di-Poï, 2021. "Multiple evolutionary origins and losses of tooth complexity in squamates," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26285-w
    DOI: 10.1038/s41467-021-26285-w
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    as
    1. Joan Garcia-Porta & Iker Irisarri & Martin Kirchner & Ariel Rodríguez & Sebastian Kirchhof & Jason L. Brown & Amy MacLeod & Alexander P. Turner & Faraham Ahmadzadeh & Gonzalo Albaladejo & Jelka Crnobr, 2019. "Environmental temperatures shape thermal physiology as well as diversification and genome-wide substitution rates in lizards," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    2. Alistair R. Evans & Gregory P. Wilson & Mikael Fortelius & Jukka Jernvall, 2007. "High-level similarity of dentitions in carnivorans and rodents," Nature, Nature, vol. 445(7123), pages 78-81, January.
    3. Robin Wilson, 2017. "The New World," The Mathematical Intelligencer, Springer, vol. 39(3), pages 96-96, September.
    4. Chris Venditti & Andrew Meade & Mark Pagel, 2011. "Multiple routes to mammalian diversity," Nature, Nature, vol. 479(7373), pages 393-396, November.
    5. Zhe-Xi Luo, 2007. "Transformation and diversification in early mammal evolution," Nature, Nature, vol. 450(7172), pages 1011-1019, December.
    6. Zhe-Xi Luo & Richard L. Cifelli & Zofia Kielan-Jaworowska, 2001. "Dual origin of tribosphenic mammals," Nature, Nature, vol. 409(6816), pages 53-57, January.
    7. Tiago R. Simões & Oksana Vernygora & Michael W. Caldwell & Stephanie E. Pierce, 2020. "Megaevolutionary dynamics and the timing of evolutionary innovation in reptiles," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    8. Sean B. Carroll, 2001. "Chance and necessity: the evolution of morphological complexity and diversity," Nature, Nature, vol. 409(6823), pages 1102-1109, February.
    9. Christopher R. Cooney & Jen A. Bright & Elliot J. R. Capp & Angela M. Chira & Emma C. Hughes & Christopher J. A. Moody & Lara O. Nouri & Zoë K. Varley & Gavin H. Thomas, 2017. "Mega-evolutionary dynamics of the adaptive radiation of birds," Nature, Nature, vol. 542(7641), pages 344-347, February.
    10. Mark Pagel, 1999. "Inferring the historical patterns of biological evolution," Nature, Nature, vol. 401(6756), pages 877-884, October.
    11. Bonhomme, Vincent & Picq, Sandrine & Gaucherel, Cédric & Claude, Julien, 2014. "Momocs: Outline Analysis Using R," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 56(i13).
    12. Enni Harjunmaa & Aki Kallonen & Maria Voutilainen & Keijo Hämäläinen & Marja L. Mikkola & Jukka Jernvall, 2012. "On the difficulty of increasing dental complexity," Nature, Nature, vol. 483(7389), pages 324-327, March.
    13. Gregory P. Wilson & Alistair R. Evans & Ian J. Corfe & Peter D. Smits & Mikael Fortelius & Jukka Jernvall, 2012. "Adaptive radiation of multituberculate mammals before the extinction of dinosaurs," Nature, Nature, vol. 483(7390), pages 457-460, March.
    14. Fabien L. Condamine & Guillaume Guinot & Michael J. Benton & Philip J. Currie, 2021. "Dinosaur biodiversity declined well before the asteroid impact, influenced by ecological and environmental pressures," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
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