Individual variation of the masticatory system dominates 3D skull shape in the herbivory-adapted marsupial wombats

Vera Weisbecker, Thomas Guillerme, Cruise Speck, Emma Sherratt, Hyab Mehari Abraha, Alana C. Sharp, Claire E. Terhune, Simon Collins, Stephen Johnston, Olga Panagiotopoulou

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Abstract

Background: Within-species skull shape variation of marsupial mammals is widely considered low and strongly size-dependent (allometric), possibly due to developmental constraints arising from the altricial birth of marsupials. However, species whose skulls are impacted by strong muscular stresses - particularly those produced through mastication of tough food items - may not display such intrinsic patterns very clearly because of the known plastic response of bone to muscle activity of the individual. In such cases, allometry may not dominate within-species shape variation, even if it is a driver of evolutionary shape divergence; ordination of shape in a geometric morphometric context through principal component analysis (PCA) should reveal main variation in areas under masticatory stress (incisor region/zygomatic arches/mandibular ramus); but this main variation should emerge from high individual variability and thus have low eigenvalues. Results: We assessed the evidence for high individual variation through 3D geometric morphometric shape analysis of crania and mandibles of three species of grazing-specialized wombats, whose diet of tough grasses puts considerable strain on their masticatory system. As expected, we found little allometry and low Principal Component 1 (PC1) eigenvalues within crania and mandibles of all three species. Also as expected, the main variation was in the muzzle, zygomatic arches, and masticatory muscle attachments of the mandibular ramus. We then implemented a new test to ask if the landmark variation reflected on PC1 was reflected in individuals with opposite PC1 scores and with opposite shapes in Procrustes space. This showed that correspondence between individual and ordinated shape variation was limited, indicating high levels of individual variability in the masticatory apparatus. Discussion: Our results are inconsistent with hypotheses that skull shape variation within marsupial species reflects a constraint pattern. Rather, they support suggestions that individual plasticity can be an important determinant of within-species shape variation in marsupials (and possibly other mammals) with high masticatory stresses, making it difficult to understand the degree to which intrinsic constraints act on shape variation at the within-species level. We conclude that studies that link micro- and macroevolutionary patterns of shape variation might benefit from a focus on species with low-impact mastication, such as carnivorous or frugivorous species.

Original languageEnglish
Article number41
Number of pages14
JournalFrontiers in Zoology
Volume16
Issue number1
DOIs
Publication statusPublished - 1 Nov 2019
Externally publishedYes

Bibliographical note

© The Author(s). 2019Open Access. This article is distributed under the terms of the Creative Commons Attribution 4.0International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Keywords

  • Constraint
  • Cranium
  • Geometric morphometrics
  • Mandible
  • Marsupial
  • Mastication

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    Weisbecker, V., Guillerme, T., Speck, C., Sherratt, E., Abraha, H. M., Sharp, A. C., Terhune, C. E., Collins, S., Johnston, S., & Panagiotopoulou, O. (2019). Individual variation of the masticatory system dominates 3D skull shape in the herbivory-adapted marsupial wombats. Frontiers in Zoology, 16(1), [41]. https://doi.org/10.1186/s12983-019-0338-5