DiceCT Analysis of the Extreme Gouging Adaptations Within the Masticatory Apparatus of the Aye-Aye (Daubentonia madagascariensis).
DiceCT
PCSA
digital dissection
mastication
primates
Journal
Anatomical record (Hoboken, N.J. : 2007)
ISSN: 1932-8494
Titre abrégé: Anat Rec (Hoboken)
Pays: United States
ID NLM: 101292775
Informations de publication
Date de publication:
02 2020
02 2020
Historique:
received:
01
09
2019
revised:
03
10
2019
accepted:
05
10
2019
pubmed:
13
11
2019
medline:
28
1
2021
entrez:
13
11
2019
Statut:
ppublish
Résumé
Relative to all other primates, the aye-aye (Daubentonia madagascariensis) exists at the extremes of both morphology and behavior. Its specialized anatomy-which includes hypselodont incisors and highly derived manual digits-reflects a dietary niche, unique among primates, which combines tap-foraging with gouging to locate and extract wood-boring larvae. Here, we explore the impact of this extreme dietary ecology upon the masticatory musculature of this taxon with reference to a second, similarly sized but highly generalist lemuriform-the mongoose lemur (Eulemur mongoz). Using non-destructive, high-resolution diffusible iodine-based contrast-enhanced computed tomography techniques, we reconstruct the three-dimensional volumes of eight masticatory muscles, and, for the first time in strepsirrhines, isolate and visualize their constituent muscle fascicles in situ and in three dimensions. Using these data, we report muscle volumes, forces, and fascicle lengths from each muscle portion, as well as their orientation relative to two standardized anatomical planes. Our findings demonstrate the overbuilt nature of the aye-aye's masticatory apparatus, in which each muscle possesses an absolutely and relatively larger muscle volume and PCSA than its counterpart in the mongoose lemur. Likewise, for several adductor muscles, aye-ayes also possess relatively greater fascicle lengths. Finally, we note several unusual features within the lateral pterygoid of the aye-aye-the muscle most responsible for jaw protrusion-that relate to force maximization and reorientation. As this jaw motion is critical to gouging, we interpret these differences to reflect highly specific specializations that facilitate the aye-aye's extreme subsistence strategy. Anat Rec, 2019. © 2019 American Association for Anatomy Anat Rec, 303:282-294, 2020. © 2019 American Association for Anatomy.
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
282-294Subventions
Organisme : National Science Foundation
ID : IOS-15-57125
Pays : International
Informations de copyright
© 2019 American Association for Anatomy.
Références
Anapol F, Barry K. 1996. Fiber architecture of the extensors of the hindlimb in semiterrestrial and arboreal guenons. Am J Phys Anthropol 99:429-447.
Bang M-L, Li X, Littlefield R, Bremner S, Thor A, Knowlton KU, Lieber RL, Chen J. 2006. Nebulin-deficient mice exhibit shorter thin filament lengths and reduced contractile function in skeletal muscle. J Cell Biol 173:905-916.
Baverstock H, Jeffery NS, Cobb SN. 2013. The morphology of the mouse masticatory musculature. J Anat 223:46-60.
Boettcher ML, Leonard KC, Dickinson E, Herrel A, Hartstone-Rose A. 2019. Extraordinary grip strength and specialized myology in the hyper-derived hand of Perodicticus potto? J Anat. 235:931-939.
Bourke J, Wroe S, Moreno K, McHenry C, Clausen P. 2008. Effects of gape and tooth position on bite force and skull stress in the dingo (Canis lupus dingo) using a 3-dimensional finite element approach. PLoS One 3:e2200.
Cartmill M. 1974. Daubentonia, Dactylopsila, woodpeckers and klinorhynchy. In: Martin RD, Doyle GA, Walker A, editors. Prosimian biology. New York: Gerald Duckworth and Co. p 655-670.
Coimbra-Filho AF, Mittermeier RA. 1977. Tree-gouging, exudate-eating and the "short-tusked" condition in Callithrix and Cebuella. In: Kleiman DG, editor. The biology and conservation of the Callitrichidae. Washington, DC: Smithsonian Institution Press. p 105-115.
Cox PG, Rayfield EJ, Fagan MJ, Herrel A, Pataky TC, Jeffery N. 2012. Functional evolution of the feeding system in rodents. PLoS One 7:e36299.
Curtis DJ. 2004. Diet and nutrition in wild mongoose lemurs (Eulemur mongoz) and their implications for the evolution of female dominance and small group size in lemurs. Am J Phys Anthropol 124:234-247.
Curtis AA, Santana SE. 2018. Jaw-dropping: Functional variation in the digastric muscle in bats. Anat Rec 301:279-290.
Curtis N, Kupczik K, O'Higgins P, Moazen M, Fagan M. 2008. Predicting skull loading: applying multibody dynamics analysis to a macaque skull. Anat Rec 291:491-501.
Curtis N, Jones ME, Evans SE, Shi J, O'Higgins P, Fagan MJ. 2010. Predicting muscle activation patterns from motion and anatomy: modelling the skull of Sphenodon (Diapsida: Rhynchocephalia). J R Soc Interface 7:153-160.
Dickinson E, Stark H, Kupczik K. 2018. Non-destructive determination of muscle architectural variables through the use of DiceCT. Anat Rec 301:363-377.
Dickinson E, Basham C, Rana A, Hartstone-Rose A. 2019. Visualization and quantification of digitally dissected muscle fascicles in the masticatory muscles of Callithrix jacchus using nondestructive DiceCT. Anat Rec. 302:1891-1900.
Diogo R, Molnar JL, Smith TD. 2014. The anatomy and ontogeny of the head, neck, pectoral, and upper limb muscles of Lemur catta and Propithecus coquereli (Primates): discussion on the parallelism between ontogeny and phylogeny and implications for evolutionary and developmental biology. Anat Rec 297:1435-1453.
Dumont ER, Davis JL, Grosse IR, Burrows AM. 2011. Finite element analysis of performance in the skulls of marmosets and tamarins. J Anat 218:151-162.
Erickson CJ. 1991. Percussive foraging in the aye-aye, Daubentonia madagascariensis. Anim Behav 41:793-801.
Erickson CJ. 1994. Tap-scanning and extractive foraging in aye-ayes. Daubentonia madagascariensisFolia Primatol 62:125-135.
Fitton L, Shi J, Fagan M, O'Higgins P. 2012. Masticatory loadings and cranial deformation in Macaca fascicularis: a finite element analysis sensitivity study. J Anat 221:55-68.
Gans C. 1982. Fiber architecture and muscle function. Exerc Sport Sci Rev 10:160-207.
Gans C, Bock WJ. 1965. The functional significance of muscle architecture - a theoretical analysis. Ergeb Anat Entwicklungsgesch 38:115-142.
Gaspard M. 1972. Les muscles masticateurs superficiels des singes a l'homme: anatomie comparee et anatomo-physiologie. Paris: Maloine.
Gignac PM, Kley NJ. 2014. Iodine-enhanced micro-CT imaging: methodological refinements for the study of the soft-tissue anatomy of post-embryonic vertebrates. J Exp Zool Part B 322:166-176.
Gignac PM, Kley NJ, Clarke JA, Colbert MW, Morhardt AC, Cerio D, Cost IN, Cox PG, Daza JD, Early CM, et al. 2016. Diffusible iodine-based contrast-enhanced computed tomography (diceCT): an emerging tool for rapid, high-resolution, 3-D imaging of metazoan soft tissues. J Anat 228:889-909.
Gokhin DS, Bang M-L, Zhang J, Chen J, Lieber RL. 2009. Reduced thin filament length in nebulin-knockout skeletal muscle alters isometric contractile properties. Am J Physiol-Cell Physiol 296:C1123-C1132.
Hartstone-Rose A, Perry J, Morrow CJ. 2012. Bite force estimation and the fiber architecture of felid masticatory muscles. Anat Rec 295:1336-1351.
Hartstone-Rose A, Deutsch AR, Leischner CL, Pastor F. 2018. Dietary correlates of masticatory muscle fiber architecture. Anat Rec 301:311-324.
Hautier L, Lebrun R, Cox PG. 2012. Patterns of covariation in the masticatory apparatus of hystricognathous rodents: implications for evolution and diversification. J Morphol 273:1319-1337.
Holliday CM, Tsai HP, Skiljan RJ, George ID, Pathan S. 2013. A 3D interactive model and atlas of the jaw musculature of Alligator mississippiensis. PLoS One 8:e62806.
Hylander WL, Johnson KR. 1994. Jaw muscle function and wishboning of the mandible during mastication in macaques and baboons. Am J Phys Anthropol 94:523-547.
Iwano T, Iwakawa C. 1988. Feeding behavior of the aye-aye (Daubentonia madagascariensis) on nuts of ramy (Canarium madagascariensis). Folia Primatol 50:136-142.
Jeffery NS, Stephenson RS, Gallagher JA, Jarvis JC, Cox PG. 2011. Micro-computed tomography with iodine staining resolves the arrangement of muscle fibres. J Biomech 44:189-192.
Kupczik K, Stark H, Mundry R, Neininger FT, Heidlauf T, Röhrle O. 2015. Reconstruction of muscle fascicle architecture from iodine-enhanced microCT images: a combined texture mapping and streamline approach. J Theor Biol 382:34-43.
Lieber RL. 1986. Skeletal muscle adaptability. I: Review of basic properties. Dev Med Child Neurol 28:390-397.
Lieber RL, Fridén J. 2000. Functional and clinical significance of skeletal muscle architecture. Muscle Nerve 23:1647-1666.
Lieber RL, Ward SR. 2011. Skeletal muscle design to meet functional demands. Philos Trans R Soc London B Biol Sci 366:1466-1476.
MacIntosh BR, Gardiner PF, McComas AJ. 2006. Skeletal muscle: form and function. Champaign, IL: Human Kinetics.
Martin RD. 1990. Primate origins and evolution. London: Chapman and Hall.
Mathewson MA, Kwan A, Eng CM, Lieber RL, Ward SR. 2014. Comparison of rotator cuff muscle architecture between humans and other selected vertebrate species. J Exp Biol 217:261-273.
Michilsens F, Vereecke EE, D'août K, Aerts P. 2009. Functional anatomy of the gibbon forelimb: adaptations to a brachiating lifestyle. J Anat 215:335-354.
Morhardt AC, Witmer LM. 2016. Diffusible iodine-based contrast enhancement of large, post-embryonic, intact vertebrates for CT scanning: staining, destaining, and long-term storage. In: ICVM. Washington, DC.
Morris PJR, Cobb SNF, Cox PG. 2018. Convergent evolution in the Euarchontoglires. Biol Lett 14:20180366.
Ogihara N, Oishi M, Kanai R, Shimada H, Kondo T, Yoshino-Saito K, Ushiba J, Okano H. 2017. Muscle architectural properties in the common marmoset (Callithrix jacchus). Primates 58:461-472.
Oishi M, Ogihara N, Endo H, Asari M. 2008. Muscle architecture of the upper limb in the orangutan. Primates 49:204-209.
Oxnard CE. 1981. The uniqueness of Daubentonia. Am J Phys Anthropol 54:1-21.
Payne RC, Crompton RH, Isler K, Savage R, Vereecke EE, Günther MM, Thorpe S, D'Août K. 2006. Morphological analysis of the hindlimb in apes and humans. I. Muscle architecture. J Anat 208:709-724.
Perry JMG. 2008. The anatomy of mastication in extant strepsirrhines and eocene adapines. Biological anthropology and anatomy. Durham: Duke University. p 490.
Perry JMG, Wall CE. 2008. Scaling of the chewing muscles in prosimians. In: Vinyard C, Ravosa MJ, Wall CE, editors. Primate craniofacial function and biology. New York: Springer. p 217-240.
Perry JMG, Hartstone-Rose A, Wall CE. 2011. The jaw adductors of strepsirrhines in relation to body size, diet, and ingested food size. Anat Rec 294:712-728.
Perry JMG, Macneill KE, Heckler AL, Rakotoarisoa G, Hartstone-Rose A. 2014. Anatomy and adaptations of the chewing muscles in Daubentonia (Lemuriformes). Anat Rec 297:308-316.
Powell PL, Roy RR, Kanim P, Bello MA, Edgerton VR. 1984. Predictability of skeletal muscle tension from architectural determinations in Guinea pig hindlimbs. J Appl Physiol 57:1715-1721.
Prufrock KA, Perry JMG. 2018. Strepsirrhine diets and the pattern of masticatory muscle development. FASEB J 32:780.
Ross CF. 1995. Muscular and osseous anatomy of the primate anterior temporal fossa and the functions of the postorbital septum. Am J Phys Anthropol 98:275-306.
Sacks RD, Roy RR. 1982. Architecture of the hind limb muscles of cats: functional significance. J Morphol 173:185-195.
Santana SE. 2018. Comparative anatomy of bat jaw musculature via diffusible iodine-based contrast-enhanced computed tomography. Anat Rec 301:267-278.
Shellis R, Poole D. 1979. The arrangement of prisms in the enamel of the anterior teeth of the aye-aye. Scan Electron Microsc 497:497-506.
Shi J, Curtis N, Fitton LC, O'Higgins P, Fagan MJ. 2012. Developing a musculoskeletal model of the primate skull: predicting muscle activations, bite force, and joint reaction forces using multibody dynamics analysis and advanced optimisation methods. J Theor Biol 310:21-30.
Sterling EJ. 1994. Aye-ayes: specialists on structurally defended resources. Folia Primatol 62:142-154.
Sterling EJ, Dierenfeld ES, Ashbourne CK, Feistner ATC. 1994. Dietary intake, food composition, and nutrient intake in wild and captive populations of Daubentonia madagascariensis. Folia Primatol 62:115-124.
Sullivan S, McGechie F, Middleton K, Holliday C. 2019. 3D muscle architecture of the pectoral muscles of European starling (Sturnus vulgaris). Integr Organismal Biol 1:oby010.
Swindler DR. 1976. Dentition of living primates. London: Academic Press.
Tattersall I, Schwartz JH. 1974. Craniodental morphology and the systematics of the Malagasy lemurs (Primates, Prosimii). Anthropol Pap Am Mus Nat Hist 52:139-192.
Taylor AB, Vinyard CJ. 2004. Comparative analysis of masseter fiber architecture in tree-gouging (Callithrix jacchus) and nongouging (Saguinus oedipus) callitrichids. J Morphol 261:276-285.
Taylor AB, Vinyard CJ. 2009. Jaw-muscle fiber architecture in tufted capuchins favors generating relatively large muscle forces without compromising jaw gape. J Hum Evol 57:710-720.
Taylor AB, Eng CM, Anapol FC, Vinyard CJ. 2009. The functional correlates of jaw-muscle fiber architecture in tree-gouging and nongouging callitrichid monkeys. Am J Phys Anthropol 139:353-367.
Toler M, Wall CE. 2013. Mandibular kinetics of gnawing in the aye-aye (Daubentonia madagascariensis) and biomechanical modeling of anterior tooth use. Am J Phys Anthropol 150:272.
Tsai HP, Holliday CM. 2011. Ontogeny of the alligator cartilago transiliens and its significance for sauropsid jaw muscle evolution. PLoS One 6:e24935.
Turnbull WD. 1970. Mammalian masticatory apparatus. Fieldiana Geol 18:147-356.
Vickerton P, Jarvis J, Jeffery N. 2013. Concentration-dependent specimen shrinkage in iodine-enhanced micro CT. J Anat 223:185-193.
Vinyard CJ, Wall CE, Williams SH, Schmitt DO, Hylander WL. 2001. A preliminary report on the jaw mechanics during tree gouging in common marmosets (Callithrix jacchus). In: Brooks A, editor. Dental Morphology 2001: Proceedings of the 12th International Symposium on Dental Morphology. Sheffield: Sheffield Academic Press. p 283-297.
Vinyard CJ, Wall CE, Williams SH, Hylander WL. 2003. Comparative functional analysis of skull morphology of tree-gouging primates. Am J Phys Anthropol 120:153-170.
Watson PJ, Groning F, Curtis N, Fitton LC, Herrel A, McCormack SW, Fagan MJ. 2014. Masticatory biomechanics in the rabbit: a multi-body dynamics analysis. J R Soc Interface 11:20140564.
Williams S, Vinyard C, Wall C. 2000. The mechanics of tree-gouging in Callithrix jacchus. Am J Phys Anthropol Suppl 30:322.