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How Does Masticatory Muscle Architecture Covary with Mandibular Shape in Domestic Dogs?

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Abstract

Despite the considerable scientific interest in the variability and patterns of integration in the dog skull, how these patterns impact or are driven by function remains largely unexplored. Since the mandible is directly involved in mastication, it can be expected to be directly related to the development of the adductor and abductor muscles. Here, we explore whether variation in the architecture and size of the masticatory muscles is associated with the variation in mandibular shape in dogs. We obtained muscle data from the dissection of 48 dogs from different breeds and morphotypes to explore the architecture of the muscles and used 3D geometric morphometric approaches to quantify the shape of the mandible. Covariations between the masticatory muscles and mandibular shape were explored using two-block partial least square analyses (2B-PLS). Our results show there is a strong covariation between mandibular shape and masticatory muscles mass (rPLS from 0.70 to 0.74 for the first axis representing more than 90% of the total covariance) and physiological cross-sectional area (rPLS from 0.64 to 0.73 for the first axis representing more than 80% of the total covariance), irrespective of whether size is taken into account or not. These results suggest muscle size and thus attachment area requirements for individual muscles are likely drivers of mandibular shape. Moreover, mandible shape is likely to be a good predictor of muscle force. Finally, it appears that domestication of dogs has not resulted in a disuse phenotype characterized by a decoupling between form and function.

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Acknowledgements

We thank the Veterinary school ONIRIS-Nantes (France) and Anses (Nancy, France) for providing dog heads for dissection. We are grateful to Manuel Comte, Mickaël Godet and Frederic Lebatard for their help in managing specimens and their helpful discussions about the preparation of the skulls. We also thank Arnaud Delapré for his help with photogrammetry and Fabien Belhaoues for his constructive feedback on a first draft of this manuscript. We thank two anonymous reviewers who contributed to the improvement of an earlier version of this manuscript by their valuable comments and suggestions.

Funding

This research was funded by the Ministère de l’Enseignement supérieur, de la Recherche et de l’Innovation.

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Correspondence to Colline Brassard.

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The authors declare that they have no conflict of interest.

Electronic supplementary material

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Supplementary Fig. S1

Distribution of the specimens along the allometric slope with a visualisation of the differences between large and small specimens relative to consensus shape. Ages are indicated by colors. Beagles are in green and other breed names are indicated following Table 1 (TIFF 3730 kb)

Supplementary Fig. S2

PCA describing variation in A) mass or B) scaled mass of the jaw muscles. Histograms represent the loadings of the original variables on the axes. Dig: Digastric; MS: masseter pars superficialis; MP: masseter pars profunda; ZMA: masseter pars zygomaticomandibularis anterior; ZMP: masseter pars zygomaticomandibularis posterior; SZ: temporalis pars suprazygomatica; TS: temporalis pars superficialis; TP: temporalis pars profunda; P: pterygoids. Ages are indicated by colors. Beagles are in green and other breed names are indicated following Table 1 (TIFF 2622 kb)

Supplementary Fig. S3

2-Block Partial Least Square Analyses between mandibular shape and the PCSA of jaw muscles, with muscle vectors and shapes at the minimum and maximum of the PLS axis. Illustrations represent the deformations from the consensus to the extreme of the axis in lateral, dorsal and caudal views. Dig: Digastric; MS: masseter pars superficialis; MP: masseter pars profunda; ZMA: masseter pars zygomaticomandibularis anterior; ZMP: masseter pars zygomaticomandibularis posterior; SZ: temporalis pars suprazygomatica; TS: temporalis pars superficialis; TP: temporalis pars profunda; P: pterygoids. Ages are indicated by colors. Beagles are in green and other breed names are indicated following Table 1 (TIFF 7302 kb)

Supplementary Fig. S4

2-Block Partial Least Square Analyses between mandibular shape and the mass of jaw muscles, with muscle vectors and shapes at the minimum and maximum of the PLS axis. Illustrations represent the deformations from the consensus to the extreme of the axis in lateral, dorsal and caudal views. Dig: Digastric; MS: masseter pars superficialis; MP: masseter pars profunda; ZMA: masseter pars zygomaticomandibularis anterior; ZMP: masseter pars zygomaticomandibularis posterior; SZ: temporalis pars suprazygomatica; TS: temporalis pars superficialis; TP: temporalis pars profunda; P: pterygoids. Ages are indicated by colors. Beagles are in green and other breed names are indicated following Table 1 (TIFF 7325 kb)

Supplementary Fig. S5

2-Block Partial Least Square Analyses between the shape of the ramus and the PCSA of jaw muscles, with muscle vectors and shapes at the minimum and maximum of the PLS axis. Illustrations represent the deformations from the consensus to the extreme of the axis in lateral, dorsal and caudal views. Dig: Digastric; MS: masseter pars superficialis; MP: masseter pars profunda; ZMA: masseter pars zygomaticomandibularis anterior; ZMP: masseter pars zygomaticomandibularis posterior; SZ: temporalis pars suprazygomatica; TS: temporalis pars superficialis; TP: temporalis pars profunda; P: pterygoids. Ages are indicated by colors. Beagles are in green and other breed names are indicated following Table 1 (TIFF 5354 kb)

Supplementary Fig. S6

2-Block Partial Least Square Analyses between the shape of the ramus and the mass of jaw muscles, with muscle vectors and shapes at the minimum and maximum of the PLS axis. Illustrations represent the deformations from the consensus to the extreme of the axis in lateral, dorsal and caudal views. Dig: Digastric; MS: masseter pars superficialis; MP: masseter pars profunda; ZMA: masseter pars zygomaticomandibularis anterior; ZMP: masseter pars zygomaticomandibularis posterior; SZ: temporalis pars suprazygomatica; TS: temporalis pars superficialis; TP: temporalis pars profunda; P: pterygoids. Ages are indicated by colors. Beagles are in green and other breed names are indicated following Table 1 (TIFF 5123 kb)

Supplementary Fig. S7

2-Block Partial Least Square Analyses between mandibular shape and the scaled mass of jaw muscles, with muscle vectors and shapes at the minimum and maximum of the PLS axis. Illustrations represent the deformations from the consensus to the extreme of the axis in lateral, dorsal and caudal views. Dig: Digastric; MS: masseter pars superficialis; MP: masseter pars profunda; ZMA: masseter pars zygomaticomandibularis anterior; ZMP: masseter pars zygomaticomandibularis posterior; SZ: temporalis pars suprazygomatica; TS: temporalis pars superficialis; TP: temporalis pars profunda; P: pterygoids. Ages are indicated by colors. Beagles are in green and other breed names are indicated following Table 1 (TIFF 7515 kb)

Supplementary Fig. S8

2-Block Partial Least Square Analyses between the shape of the ramus and the scaled PCSA of jaw muscles, with muscle vectors and shapes at the minimum and maximum of the PLS axis. Illustrations represent the deformations from the consensus to the extreme of the axis in lateral, dorsal and caudal views. Dig: Digastric; MS: masseter pars superficialis; MP: masseter pars profunda; ZMA: masseter pars zygomaticomandibularis anterior; ZMP: masseter pars zygomaticomandibularis posterior; SZ: temporalis pars suprazygomatica; TS: temporalis pars superficialis; TP: temporalis pars profunda; P: pterygoids. Ages are indicated by colors. Beagles are in green and other breed names are indicated following Table 1 (TIFF 5633 kb)

Supplementary Fig. S9

2-Block Partial Least Square Analyses between between allometry-free mandibular shape and the scaled mass of jaw muscles, with muscle vectors and shapes at the minimum and maximum of the PLS axis. Illustrations represent the deformations from the consensus to the extreme of the axis in lateral, dorsal and caudal views. Dig: Digastric; MS: masseter pars superficialis; MP: masseter pars profunda; ZMA: masseter pars zygomaticomandibularis anterior; ZMP: masseter pars zygomaticomandibularis posterior; SZ: temporalis pars suprazygomatica; TS: temporalis pars superficialis; TP: temporalis pars profunda; P: pterygoids. Ages are indicated by colors. Beagles are in green and other breed names are indicated following Table 1 (TIFF 7458 kb)

Supplementary Fig. S10

2-Block Partial Least Square Analyses between the allometry-free shape of the ramus and the scaled mass of jaw muscles, with muscle vectors and shapes at the minimum and maximum of the PLS axis. Illustrations represent the deformations from the consensus to the extreme of the axis in lateral, dorsal and caudal views. Dig: Digastric; MS: masseter pars superficialis; MP: masseter pars profunda; ZMA: masseter pars zygomaticomandibularis anterior; ZMP: masseter pars zygomaticomandibularis posterior; SZ: temporalis pars suprazygomatica; TS: temporalis pars superficialis; TP: temporalis pars profunda; P: pterygoids. Ages are indicated by colors. Beagles are in green and other breed names are indicated following Table 1 (TIFF 5692 kb)

Supplementary material Table S1

Details of the specimen used in this study including raw jaw muscles data and PCSAs (XLSX 61 kb)

Supplementary material Table S2

Origin and insertion of the jaw muscles dissected in this study, after a synthesis of nomenclatures proposed by Schumacher (1961), Turnbull (1970), Ström et al. (1988), Tomo et al. (1993), Christiansen and Adolfssen (2005), Budras (2007), Barone (2010), Evans and DeLahunta (2010), Hung et al. (2010), Druzinsky et al. (2011), Hartstone-Rose et al. (2012), Flahive (2015), Penrose et al. (2016) (XLSX 11 kb)

Supplementary material Table S3

Results of the statistical analyses exploring allometries (sheet 1) and the variability (sheet 2) in mandibular shape and muscle data (XLSX 15 kb)

Supplementary material Table S4

Results of the 2-Block Partial Least Square Analyses (sheet 1) and P-values and Z-scores of the comparison tests (sheet 2). S: shape of the mandible; rS: shape of the ramus; a: allometry-free (shape or shape of the ramus); M: mass; PCSA: PCSA; s: scaled (mass or PCSA). Sigificant results (p-value < 0.05) are indicated in bold (XLSX 18 kb)

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Brassard, C., Merlin, M., Monchâtre-Leroy, E. et al. How Does Masticatory Muscle Architecture Covary with Mandibular Shape in Domestic Dogs?. Evol Biol 47, 133–151 (2020). https://doi.org/10.1007/s11692-020-09499-6

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  • DOI: https://doi.org/10.1007/s11692-020-09499-6

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