Abstract
Many studies have attested to the consequences of the recent and intense artificial selection on the morphological variability of the cranium and mandible in domestic animals. However, the functional relations of the cranium with other constituents of the masticatory apparatus (the mandibles and the adductor muscles) have rarely been explored. Previous work has demonstrated strong relationships between the overall shape of the mandible and muscle data, however, drastic artificial selection in dogs has led to frequent malocclusions, suggesting a possible decoupling between the cranium and the mandible. Moreover, the more complex role of the cranium suggests that it is likely less impacted by, and correlated with, the architecture of the jaw muscles than the mandible. We explored the covariations between cranial and mandibular shape and between cranial shape and the masticatory muscle architecture. Shape analyses were conducted on 58 dogs from various breeds and we used muscle data previously obtained from the dissection of 48 of these dogs. The shape of the cranium was quantified using 3D geometric morphometric approaches. Principal component analyses (PCA) and two-block partial least square analyses (2B-PLS) were used to quantify the variations in cranial shape and the covariations with mandible shape and muscle architecture, respectively. Interestingly, our results reveal strong covariations between cranial shape and mandibular shape and between cranial shape and masticatory muscles mass or physiological cross-sectional area, irrespective of whether size is taken into account or not. We conclude that the drastic artificial selection in domestic dogs has not tainted the integrity of the jaw system, which reinforces previous assumptions hypothesising that phenotypic variability in dogs may be limited by developmental factors.
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References
Adams, D. C., & Collyer, M. L. (2016). On the comparison of the strength of morphological integration across morphometric datasets. Evolution, 70(11), 2623–2631. https://doi.org/10.1111/evo.13045.
Adams, D. C., & Collyer, M. L. (2017). Multivariate phylogenetic comparative methods: Evaluations, comparisons, and recommendations. Systematic Biology, 67(1), 14–31.
Anderson, M. J. (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26(1), 32–46.
Anderson, M., & Braak, C. T. (2003). Permutation tests for multi-factorial analysis of variance. Journal of Statistical Computation and Simulation, 73(2), 85–113.
Anderson, P. S., Renaud, S., & Rayfield, E. J. (2014). Adaptive plasticity in the mouse mandible. BMC Evolutionary Biology, 14(1), 1–9. https://doi.org/10.1186/1471-2148-14-85.
Barone, R. (2010). Anatomie comparée des mammifères domestiques: Tome 1, Ostéologie (5e édition.). Paris: Vigot.
Bell, A. F. (1965). Dental disease in the dog. Journal of Small Animal Practice, 6(6), 421–428. https://doi.org/10.1111/j.1748-5827.1965.tb04359.x.
Blank, R. D. (2014). Bone and muscle pleiotropy: The genetics of associated traits. Clinical Reviews in Bone and Mineral Metabolism, 12(2), 61–65. https://doi.org/10.1007/s12018-014-9159-4.
Bookstein, F. L. (1997). Morphometric tools for landmark data: Geometry and biology. Cambridge: Cambridge University Press.
Bouvier, M., & Hylander, W. L. (1981). Effect of bone strain on cortical bone structure in macaques (Macaca mulatta). Journal of Morphology, 167(1), 1–12. https://doi.org/10.1002/jmor.1051670102.
Bouvier, M., & Hylander, W. L. (1984). The effect of dietary consistency on gross and histologic morphology in the craniofacial region of young rats. American Journal of Anatomy, 170(1), 117–126. https://doi.org/10.1002/aja.1001700109.
Brassard, C., Merlin, M., Guintard, C., Monchâtre-Leroy, E., Barrat, J., Callou, C., et al. (2020a). How does masticatory muscle architecture covary with mandibular shape in domestic dogs? Evolutionary Biology. https://doi.org/10.1007/s11692-020-09499-6.
Brassard, C., Merlin, M., Guintard, C., Monchâtre-Leroy, E., Barrat, J., Bausmayer, N., et al. (2020b). Bite force and its relationship to jaw shape in domestic dogs. Journal of Experimental Biology. https://doi.org/10.1242/jeb.224352.
Brotto, M., & Bonewald, L. (2015). Bone and muscle: Interactions beyond mechanical. Bone, 80, 109–114. https://doi.org/10.1016/j.bone.2015.02.010.
Collyer, M. L., Sekora, D. J., & Adams, D. C. (2015). A method for analysis of phenotypic change for phenotypes described by high-dimensional data. Heredity, 115(4), 357.
Cornette, R., Baylac, M., Souter, T., & Herrel, A. (2013). Does shape co-variation between the skull and the mandible have functional consequences? A 3D approach for a 3D problem. Journal of Anatomy, 223(4), 329–336. https://doi.org/10.1111/joa.12086.
Cornette, R., Tresset, A., & Herrel, A. (2015). The shrew tamed by Wolff’s law: Do functional constraints shape the skull through muscle and bone covariation? Journal of Morphology, 276(3), 301–309. https://doi.org/10.1002/jmor.20339.
Curth, S. (2018). Modularity and integration in the skull of Canis lupus (Linnaeus 1758): A geometric morphometrics study on domestic dogs and wolves, 78.
Curth, S., Fischer, M. S., & Kupczik, K. (2017). Patterns of integration in the canine skull: An inside view into the relationship of the skull modules of domestic dogs and wolves. Zoology (Jena, Germany), 125, 1–9. https://doi.org/10.1016/j.zool.2017.06.002.
Daegling, D. J., & Hotzman, J. L. (2003). Functional significance of cortical bone distribution in anthropoid mandibles: an in vitro assessment of bone strain under combined loads. American Journal of Physical Anthropology, 122(1), 38–50. https://doi.org/10.1002/ajpa.10225.
Drake, A. G., Coquerelle, M., Kosintsev, P. A., Bachura, O. P., Sablin, M., Gusev, A. V., et al. (2017). Three-dimensional geometric morphometric analysis of fossil canid mandibles and skulls. Scientific Reports, 7(1), 9508. https://doi.org/10.1038/s41598-017-10232-1.
Drake, A. G., & Klingenberg, C. P. (2008). The pace of morphological change: Historical transformation of skull shape in St Bernard dogs. Proceedings. Biological sciences, 275(1630), 71–76. https://doi.org/10.1098/rspb.2007.1169.
Drake, A. G., & Klingenberg, C. P. (2010). Large-scale diversification of skull shape in domestic dogs: Disparity and modularity. The American Naturalist, 175(3), 289–301. https://doi.org/10.1086/650372.
Dryden, I. L., & Mardia, K. V. (2016). Statistical shape analysis: With applications in R. New York: Wiley.
Ellis, J. L., Thomason, J. J., Kebreab, E., & France, J. (2008). Calibration of estimated biting forces in domestic canids: Comparison of post-mortem and in vivo measurements. Journal of Anatomy, 212(6), 769–780. https://doi.org/10.1111/j.1469-7580.2008.00911.x.
Ellis, J. L., Thomason, J., Kebreab, E., Zubair, K., & France, J. (2009). Cranial dimensions and forces of biting in the domestic dog. Journal of Anatomy, 214(3), 362–373. https://doi.org/10.1111/j.1469-7580.2008.01042.x.
Fabre, A.-C., Andrade, D. V., Huyghe, K., Cornette, R., & Herrel, A. (2014). Interrelationships between bones, muscles, and performance: biting in the lizard Tupinambis merianae. Evolutionary Biology, 41(4), 518–527. https://doi.org/10.1007/s11692-014-9286-3.
Fabre, A.-C., Perry, J. M. G., Hartstone-Rose, A., Lowie, A., Boens, A., & Dumont, M. (2018). Do muscles constrain skull shape evolution in strepsirrhines? The Anatomical Record, 301(2), 291–310. https://doi.org/10.1002/ar.23712.
Fau, M., Cornette, R., & Houssaye, A. (2016). Photogrammetry for 3D digitizing bones of mounted skeletons: Potential and limits. Comptes Rendus Palevol, 15(8), 968–977. https://doi.org/10.1016/j.crpv.2016.08.003.
Forbes-Harper, J. L., Crawford, H. M., Dundas, S. J., Warburton, N. M., Adams, P. J., Bateman, P. W., et al. (2017). Diet and bite force in red foxes: Ontogenetic and sex differences in an invasive carnivore. Journal of Zoology, 303(1), 54–63. https://doi.org/10.1111/jzo.12463.
Frost, H. M. (2001). From Wolff’s law to the Utah paradigm: Insights about bone physiology and its clinical applications. The Anatomical Record, 262(4), 398–419. https://doi.org/10.1002/ar.1049.
Frost, H. M. (2003). Bone’s mechanostat: a 2003 update. The Anatomical Record Part A: Discoveries in Molecular, Cellular, and Evolutionary Biology: An Official Publication of the American Association of Anatomists, 275(2), 1081–1101. https://doi.org/10.1002/ar.a.10119.
Frost, H. M., & Schönau, E. (2000). The" muscle-bone unit" in children and adolescents: a 2000 overview. Journal of Pediatric Endocrinology and Metabolism, 13(6), 571–590. https://doi.org/10.1515/JPEM.2000.13.6.571.
Goodall, C. (1991). Procrustes methods in the statistical analysis of shape. Journal of the Royal Statistical Society: Series B (Methodological), 53(2), 285–321.
Goswami, A., Watanabe, A., Felice, R. N., Bardua, C., Fabre, A.-C., & Polly, P. D. (2019). High-density morphometric analysis of shape and integration: The good, the bad, and the not-really-a-problem. Integrative and Comparative Biology, 59(3), 669–683. https://doi.org/10.1093/icb/icz120.
Gunz, P., Mitteroecker, P., & Bookstein, F. L. (2005). Semilandmarks in three dimensions. In D. E. Slice (Ed.), Modern morphometrics in physical anthropology (pp. 73–98). Boston: Springer.
He, T., & Kiliaridis, S. (2003). Effects of masticatory muscle function on craniofacial morphology in growing ferrets (Mustela putorius furo). European Journal of Oral Sciences, 111(6), 510–517. https://doi.org/10.1111/j.0909-8836.2003.00080.x.
Heck, L., Wilson, L. A. B., Evin, A., Stange, M., & Sánchez-Villagra, M. R. (2018). Shape variation and modularity of skull and teeth in domesticated horses and wild equids. Frontiers in Zoology, 15(1), 14. https://doi.org/10.1186/s12983-018-0258-9.
Herring, S. W. (2011). Muscle-bone interactions and the development of skeletal phenotype: Jaw muscles and the skull. Epigenetics Linking Genotype and Phenotype in Development and Evolution., 13, 201.
Iinuma, M., Yoshida, S., & Funakoshi, M. (1991). Development of masticatory muscles and oral behavior from suckling to chewing in dogs. Comparative Biochemistry and Physiology. A, Comparative Physiology, 100(4), 789–794. https://doi.org/10.1016/0300-9629(91)90293-l.
Kiliaridis, S., Engström, C., & Thilander, B. (1985). The relationship between masticatory function and craniofacial morphology: I. A cephalometric longitudinal analysis in the growing rat fed a soft diet. The European Journal of Orthodontics, 7(4), 273–283.
Kiliaridis, S., Tzakis, M. G., & Carlsson, G. E. (1995). Effects of fatigue and chewing training on maximal bite force and endurance. American Journal of Orthodontics and Dentofacial Orthopedics: Official Publication of the American Association of Orthodontists, Its Constituent Societies, and the American Board of Orthodontics, 107(4), 372–378. https://doi.org/10.1016/s0889-5406(95)70089-7.
Kim, S. E., Arzi, B., Garcia, T. C., & Verstraete, F. J. M. (2018). Bite forces and their measurement in dogs and cats. Frontiers in Veterinary Science. https://doi.org/10.3389/fvets.2018.00076.
Klingenberg, C. P., Barluenga, M., & Meyer, A. (2002). Shape analysis of symmetric structures: Quantifying variation among individuals and asymmetry. Evolution, 56(10), 1909–1920. https://doi.org/10.1111/j.0014-3820.2002.tb00117.x.
Klingenberg, C. P., & Navarro, N. (2012). Development of the mouse mandible. In J. Piálek, M. Macholán, P. Munclinger, & S. J. E. Baird (Eds.), Evolution of the house mouse (pp. 135–149). Cambridge: Cambridge University Press.
Liebman, F. M., & Kussick, L. (1965). An Electromyographic analysis of masticatory muscle imbalance with relation to skeletal growth in dogs. Journal of Dental Research, 44(4), 768–774. https://doi.org/10.1177/00220345650440042401.
Machado, F. A., Zahn, T. M. G., & Marroig, G. (2018). Evolution of morphological integration in the skull of Carnivora (Mammalia): Changes in Canidae lead to increased evolutionary potential of facial traits. Evolution, 72(7), 1399–1419. https://doi.org/10.1111/evo.13495.
Milella, L. (2009). Mandibular brachygnathism in dogs. Companion. Animal, 14(6), 29–35. https://doi.org/10.1111/j.2044-3862.2009.tb00382.x.
Mitteroecker, P., & Bookstein, F. (2007). The conceptual and statistical relationship between modularity and morphological integration. Systematic Biology,56(5), 818–836.
Mitteroecker, P., Gunz, P., Bernhard, M., Schaefer, K., & Bookstein, F. L. (2004). Comparison of cranial ontogenetic trajectories among great apes and humans. Journal of Human Evolution, 46(6), 679–698. https://doi.org/10.1016/j.jhevol.2004.03.006.
Parker, H. G., Kim, L. V., Sutter, N. B., Carlson, S., Lorentzen, T. D., Malek, T. B., et al. (2004). Genetic structure of the purebred domestic dog. Science, 304(5674), 1160–1164.
Penrose, F., Cox, P., Kemp, G., & Jeffery, N. (2020). Functional morphology of the jaw adductor muscles in the Canidae. The Anatomical Record, 1, 12. https://doi.org/10.1002/ar.24391.
Renaud, S., Auffray, J.-C., & de la Porte, S. (2010). Epigenetic effects on the mouse mandible: Common features and discrepancies in remodeling due to muscular dystrophy and response to food consistency. BMC Evolutionary Biology, 10, 28. https://doi.org/10.1186/1471-2148-10-28.
Roberts, T., McGreevy, P., & Valenzuela, M. (2010). Human induced rotation and reorganization of the brain of domestic dogs. PLoS ONE, 5(7), e11946. https://doi.org/10.1371/journal.pone.0011946.
Rohlf, F. J., & Corti, M. (2000). Use of two-block partial least-squares to study covariation in shape. Systematic Biology, 49(4), 740–753. https://doi.org/10.1080/106351500750049806.
Rohlf, F., & Slice, D. (1990). Extensions of the procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39, 40–59. https://doi.org/10.2307/2992207.
Schlager, S. (2012). Sliding semi-landmarks on symmetric structures in three dimensions. Présenté à the 81st annual meeting of the American Association of Physical Anthropologists, Portland, OR, Anthropology, University of Freiburg, Germany.
Schoenau, E. (2005). From mechanostat theory to development of the « Functional Muscle-Bone-Unit ». Journal of Musculoskeletal and Neuronal Interactions, 3, 232–238.
Scott, J. E., McAbee, K. R., Eastman, M. M., & Ravosa, M. J. (2014a). Teaching an old jaw new tricks: Diet-induced plasticity in a model organism from weaning to adulthood. Journal of Experimental Biology, 217(22), 4099–4107. https://doi.org/10.1242/jeb.111708.
Scott, J. E., McAbee, K. R., Eastman, M. M., & Ravosa, M. J. (2014b). Experimental perspective on fallback foods and dietary adaptations in early hominins. Biology Letters, 10(1), 20130789. https://doi.org/10.1098/rsbl.2013.0789.
Selba, M. C., Oechtering, G. U., Gan Heng, H., & DeLeon, V. B. (2019). The impact of selection for facial reduction in dogs: geometric morphometric analysis of canine cranial shape. The Anatomical Record. https://doi.org/10.1002/ar.24184.
Sharir, A., Stern, T., Rot, C., Shahar, R., & Zelzer, E. (2011). Muscle force regulates bone shaping for optimal load-bearing capacity during embryogenesis. Development, 138(15), 3247–3259. https://doi.org/10.1242/dev.063768.
Shirai, M., Kawai, N., Hichijo, N., Watanabe, M., Mori, H., Mitsui, S. N., et al. (2018). Effects of gum chewing exercise on maximum bite force according to facial morphology. Clinical and Experimental Dental Research, 4(2), 48–51. https://doi.org/10.1002/cre2.102.
Slizewski, A., Schönau, E., Shaw, C., & Harvati, K. (2013). Muscle area estimation from cortical bone. The Anatomical Record, 296(11), 1695–1707. https://doi.org/10.1002/ar.22788.
Smith, A. L., & Grosse, I. R. (2016). The biomechanics of zygomatic arch shape. Anatomical Record, 299(12), 1734–1752. https://doi.org/10.1002/ar.23484.
Spassov, A., Toro-Ibacache, V., Krautwald, M., Brinkmeier, H., & Kupczik, K. (2017). Congenital muscle dystrophy and diet consistency affect mouse skull shape differently. Journal of Anatomy, 231(5), 736–748. https://doi.org/10.1111/joa.12664.
Thompson, D. J., Throckmorton, G. S., & Buschang, P. H. (2001). The effects of isometric exercise on maximum voluntary bite forces and jaw muscle strength and endurance. Journal of Oral Rehabilitation, 28(10), 909–917. https://doi.org/10.1111/j.1365-2842.2001.00772.x.
Vecchione, L., Byron, C., Cooper, G., Barbano, T., Hamrick, M. W., Sciote, J., et al. (2007). Craniofacial morphology in myostatin-deficient mice. Journal of Dental Research, 86(11), 1068–1072.
Vecchione, L., Miller, J., Byron, C., Cooper, G. M., Barbano, T., Cray, J., et al. (2010). Age-related changes in craniofacial morphology in GDF-8 (myostatin)-deficient mice. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology, 293(1), 32–41.
Wayne, R. K. (1986). Cranial morphology of domestic and wild canids: The influence of development on morphological change. Evolution, 40(2), 243–261. https://doi.org/10.1111/j.1558-5646.1986.tb00467.x.
Wiley, D. F., Amenta, N., Alcantara, D. A., Ghosh, D., Kil, Y. J., Delson, E., et al. (2005). Evolutionary morphing. In VIS 05 IEEE visualization, 2005 (pp. 431‑438). Présenté à VIS 05. IEEE Visualization. https://doi.org/10.1109/VISUAL.2005.1532826.
Wolff, J. (1986). The law of bone remodelling. Berlin: Springer.
Wroe, S., Clausen, P., McHenry, C., Moreno, K., & Cunningham, E. (2007). Computer simulation of feeding behaviour in the thylacine and dingo as a novel test for convergence and niche overlap. Proceedings of the Royal Society B: Biological Sciences, 274(1627), 2819–2828.
Yamamoto, M., Takada, H., Ishizuka, S., Kitamura, K., Jeong, J., Sato, M., et al. (2020). Morphological association between the muscles and bones in the craniofacial region. PLoS ONE, 15(1), e0227301. https://doi.org/10.1371/journal.pone.0227301.
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. We are very grateful to two anonymous reviewers for their comments and advice on an earlier version of the manuscript.
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This research was funded by the Ministère de l’Enseignement supérieur, de la Recherche et de l’Innovation.
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Colline Brassard and Marilaine Merlin are co-first authors.
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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 different shapes and morphotypes are indicated by different colors. Beagles are located in the green area. Ams: American Staffordshire terrier; Box: Boxer; Buld: Bulldog; Bult: Bull terrier; Chi: Chihuahua; Can: Cane Corso; Kin: Cavalier King Charles Spaniel; Pap: Papillon; Pit: Pitbull; Rot: Rottweiler; Mas: Mastiff; Fox: Fox terrier; Bel: Belgian Shepherd; Bor: Border collie; Col: Collie; Dac: Dachshund; Ger: German Shepherd; Gol: Golden retriever; Hus: Husky; Leo: Leonberg; She: Shetland sheepdog. (TIFF 7423 kb)
Supplementary Fig. S2
2-Block Partial Least Square Analyses between cranial shape and the masses of the jaw muscles, with 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 and dorsal views. Ages are indicated by different shapes and morphotypes are indicated by different colors. Beagles are located in the green area. Ams: American Staffordshire terrier; Box: Boxer; Buld: Bulldog; Bult: Bull terrier; Chi: Chihuahua; Can: Cane Corso; Kin: Cavalier King Charles Spaniel; Pap: Papillon; Pit: Pitbull; Rot: Rottweiler; Mas: Mastiff; Fox: Fox terrier; Bel: Belgian Shepherd; Bor: Border collie; Col: Collie; Dac: Dachshund; Ger: German Shepherd; Gol: Golden retriever; Hus: Husky; Leo: Leonberg; She: Shetland sheepdog. Dig: M. digastricus; MS: M. masseter pars superficialis; MP: M. masseter pars profunda; ZMA: M. zygomaticomandibularis pars anterior; ZMP: M. zygomaticomandibularis pars posterior; SZ: M. temporalis pars suprazygomatica; TS: M. temporalis pars superficialis; TP: M. temporalis pars profunda; PM+PL: M. pterygoideus pars medialis and lateralis. (TIFF 6503 kb)
Supplementary Fig. S3
2-Block Partial Least Square Analyses between the allometry-free cranial shape and the residual masses of the jaw muscles, with 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 and dorsal views. Ages are indicated by different shapes and morphotypes are indicated by different colors. Beagles are located in the green area. Ams: American Staffordshire terrier; Box: Boxer; Buld: Bulldog; Bult: Bull terrier; Chi: Chihuahua; Can: Cane Corso; Kin: Cavalier King Charles Spaniel; Pap: Papillon; Pit: Pitbull; Rot: Rottweiler; Mas: Mastiff; Fox: Fox terrier; Bel: Belgian Shepherd; Bor: Border collie; Col: Collie; Dac: Dachshund; Ger: German Shepherd; Gol: Golden retriever; Hus: Husky; Leo: Leonberg; She: Shetland sheepdog. Dig: M. digastricus; MS: M. masseter pars superficialis; MP: M. masseter pars profunda; ZMA: M. zygomaticomandibularis pars anterior; ZMP: M. zygomaticomandibularis pars posterior; SZ: M. temporalis pars suprazygomatica; TS: M. temporalis pars superficialis; TP: M. temporalis pars profunda; PM+PL: M. pterygoideus pars medialis and lateralis. (TIFF 6098 kb)
11692_2020_9515_MOESM4_ESM.xlsx
Table S1. Details of the specimen used in this study including raw jaw muscles masses, pennation angles, fiber lengths and PCSAs. (XLSX 109 kb)
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Brassard, C., Merlin, M., Guintard, C. et al. Interrelations Between the Cranium, the Mandible and Muscle Architecture in Modern Domestic Dogs. Evol Biol 47, 308–324 (2020). https://doi.org/10.1007/s11692-020-09515-9
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DOI: https://doi.org/10.1007/s11692-020-09515-9