Philosophical Transactions of the Royal Society B: Biological Sciences
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Rhythmic chew cycles with distinct fast and slow phases are ancestral to gnathostomes

Brian A. Richard

Brian A. Richard

Department of Biological Sciences, University of Massachusetts, Lowell, MA 01954, USA

[email protected]

Contribution: Data curation, Formal analysis, Methodology, Writing – review & editing

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Meghan Spence

Meghan Spence

Department of Biological Sciences, University of Massachusetts, Lowell, MA 01954, USA

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Mateo Rull-Garza

Mateo Rull-Garza

Department of Biological Sciences, University of Massachusetts, Lowell, MA 01954, USA

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Yonas Tolosa Roba

Yonas Tolosa Roba

Department of Biological Sciences, University of Massachusetts, Lowell, MA 01954, USA

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Daniel Schwarz

Daniel Schwarz

Department of Paleontology, State Museum of Natural History, 70191 Stuttgart, Germany

Institute of Zoology and Evolutionary Research, Friedrich Schiller University, 07743 Jena, Germany

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Jason B. Ramsay

Jason B. Ramsay

Biology Department, Westfield State University, Westfield, MA 01086, USA

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J. D. Laurence-Chasen

J. D. Laurence-Chasen

Department of Organismic Biology and Anatomy, University of Chicago, Chicago, IL 60637, USA

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Callum F. Ross

Callum F. Ross

Department of Organismic Biology and Anatomy, University of Chicago, Chicago, IL 60637, USA

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Nicolai Konow

Nicolai Konow

Department of Biological Sciences, University of Massachusetts, Lowell, MA 01954, USA

[email protected]

Contribution: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing

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    Intra-oral food processing, including chewing, is important for safe swallowing and efficient nutrient assimilation across tetrapods. Gape cycles in tetrapod chewing consist of four phases (fast open and -close, and slow open and -close), with processing mainly occurring during slow close. Basal aquatic-feeding vertebrates also process food intraorally, but whether their chew cycles are partitioned into distinct phases, and how rhythmic their chewing is, remains unknown. Here, we show that chew cycles from sharks to salamanders are as rhythmic as those of mammals, and consist of at least three, and often four phases, with phase distinction occasionally lacking during jaw opening. In fishes and aquatic-feeding salamanders, fast open has the most variable duration, more closely resembling mammals than basal amniotes (lepidosaurs). Across ontogenetically or behaviourally mediated terrestrialization, salamanders show a distinct pattern of the second closing phase (near-contact) being faster than the first, with no clear pattern in partitioning of variability across phases. Our results suggest that distinct fast and slow chew cycle phases are ancestral for jawed vertebrates, followed by a complicated evolutionary history of cycle phase durations and jaw velocities across fishes, basal tetrapods and mammals. These results raise new questions about the mechanical and sensorimotor underpinnings of vertebrate food processing.

    This article is part of the theme issue ‘Food processing and nutritional assimilation in animals’.

    Footnotes

    One contribution of 18 to a theme issue ‘Food processing and nutritional assimilation in animals’.

    Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare.c.6836732.

    References