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Structural and molecular analysis of elbow flexor muscles in modern humans and common chimpanzees

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Abstract

In the present study we calculated the muscle fascicle length (MFL) and the physiological cross-sectional area (PCSA) in the elbow flexor muscles of five Homo sapiens and five Pan troglodytes. We also assessed the expression of the myosin heavy chain (MyHC) isoforms with real-time quantitative polymerase chain reaction in the same muscles and, finally, we analyzed the muscle insertion sites in the proximal epiphyses of the ulna and the radius with 3D geometric morphometrics. Our main objective is to identify quantitative differences in the elbow flexor muscles of Homo sapiens and Pan troglodytes in terms of muscle architecture, expression of MyHC isoforms, and bone insertion sites and to explore the association of these differences with the types of locomotion developed by these two species of hominoid primates. We observed that the elbow flexor muscles had a greater PCSA and a higher expression of the fast MyHC-II isoforms in Pan troglodytes, while they had a greater MFL and a higher expression of the slow MyHC-I isoform in Homo sapiens. The insertion site of the brachialis was larger in Pan troglodytes, while that of the biceps brachii was larger in Homo sapiens. Our findings may be related to the greater capacity of force generation in the elbow flexor muscles of Pan troglodytes, as an adaptation to vertical climbing, and to the greater contraction speed and resistance to fatigue of the muscles in Homo sapiens, as an adaptation to the manipulative function of the upper extremities.

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References

  • An KN, Hui FC, Morrey BF, Linscheid RL, Chao EY (1981) Muscles across the elbow joint: a biomechanical analysis. J Biomech 14:659–669

    Article  CAS  PubMed  Google Scholar 

  • Ashton EH, Flinn RM, Oxnard CE, Spence TF (1976) The adaptive and classificatory significance of certain quantitative features of the forelimb in primates. J Zool 17:515–550

    Google Scholar 

  • Basmajian JV, de Luca CJ (1985) Muscles alive. Their functions revealed by electromyography, Williams & Wilkins, Baltimore

    Google Scholar 

  • Bookstein FL (1991) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, Cambridge

    Google Scholar 

  • Bottinelli R, Canepari M, Pellegrino MA, Reggiani C (1996) Force-velocity properties of human skeletal muscle fibres: myosin heavy chain isoform and temperature dependence. J Physiol 495:573–586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bottinelli R, Reggiani C (2000) Human skeletal muscle fibres: molecular and functional diversity. Prog Biophys Mol Biol 73:195–262

    Article  CAS  PubMed  Google Scholar 

  • Carlson KJ (2006) Muscle architecture of the common chimpanzee (Pan troglodytes): perspectives for investigating chimpanzee behavior. Primates 47:218–229

    Article  PubMed  Google Scholar 

  • Cignoni P Callieri M Corsini M Dellepiane M Ganovelli F Ranzuglia G (2008) Meshlab: an open-source mesh processing tool. In: Sixth Eurographics Italian Chapter Conference, pp 129–136

  • Diogo R, Potau JM, Pastor JF et al (2013) Photographic and descriptive musculoskeletal atlas of chimpanzees. CRC Press, Boca Raton

    Book  Google Scholar 

  • Doran DM (1992) Comparison of instantaneous and locomotor bout sampling methods: a case study of adult male chimpanzee locomotor behavior and substrate use. Am J Phys Anthropol 89:85–99

    Article  CAS  PubMed  Google Scholar 

  • Gebo DL (2014) Primate comparative anatomy. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Harridge SD, Bottinelli R, Canepari M et al (1998) Sprint training, in vitro and in vivo muscle function, and myosin heavy chain expression. J Appl Physiol 84:442–449

    Article  CAS  PubMed  Google Scholar 

  • Hunt KD (1991) Mechanical implications of chimpanzee positional behavior. Am J Phys Anthropol 86:521–536

    Article  CAS  PubMed  Google Scholar 

  • Hunt KD (1992) Positional behavior of Pan troglodytes in the Mahale mountains and Gombe Stream National Parks, Tanzania. Am J Phys Anthropol 87:83–105

    Article  CAS  PubMed  Google Scholar 

  • Isler K (2005) 3D-kinematics of vertical climbing in hominoids. Am J Phys Anthropol 126:66–81

    Article  PubMed  Google Scholar 

  • Kikuchi Y (2010) Comparative analysis of muscle architecture in primate arm and forearm. Anat Histol Embryol 39:93–106

    Article  PubMed  Google Scholar 

  • Kikuchi Y, Takemoto H, Kuraoka A (2012) Relationship between humeral geometry and shoulder muscle power among suspensory, knuckle-walking, and digitigrade/palmigrade quadrupedal primates. J Anat 220:29–41

    Article  PubMed  Google Scholar 

  • Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353–357

    Article  PubMed  Google Scholar 

  • Langdon JH (2005) The human strategy: an evolutionary perspective on human anatomy. Oxford University Press, Oxford

    Google Scholar 

  • Larsson L, Moss RL (1993) Maximum velocity of shortening in relation to myosin isoform composition in single fibres from human skeletal muscles. J Physiol 472:595–614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lieber RL, Fridén J (2000) Functional and clinical significance of skeletal muscle architecture. Muscle Nerve 23:1647–1666

    Article  CAS  PubMed  Google Scholar 

  • Malagelada F Dalmau-Pastor M Vega J Golanó P (2014) Elbow anatomy. In: Sports injuries, Springer, Berlin

  • Michilsens F, Vereecke EE, D'Aout K, Aerts P (2009) Functional anatomy of the gibbon forelimb: adaptations to a brachiating lifestyle. J Anat 215:335–354

    Article  PubMed  PubMed Central  Google Scholar 

  • Myatt JP, Crompton RH, Payne-Davis RC et al (2012) Functional adaptations in the forelimb muscles of non-human great apes. J Anat 220:13–28

    Article  PubMed  Google Scholar 

  • Nordin M, Frankel VH (2001) Basic biomechanics of the musculoskeletal system. Lippincott Williams & Wilkins, Baltimore

    Google Scholar 

  • O’Higgins P (2000) The study of morphological variation in the hominid fossil record: biology, landmarks and geometry. J Anat 197:103–120

    Article  PubMed  PubMed Central  Google Scholar 

  • Oishi M, Ogihara N, Endo H, Asari M (2008) Muscle architecture of the upper limb in the orangutan. Primates 49:204–209

    Article  PubMed  Google Scholar 

  • Oishi M, Ogihara N, Endo H, Ichihara N, Asari M (2009) Dimensions of forelimb muscles in orangutans and chimpanzees. J Anat 215:373–382

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Neill MC, Umberger BR, Holowka NB, Larson SG, Reiser PJ (2017) Chimpanzee super strength and human skeletal muscle evolution. Proc Natl Acad Sci 114:7343–7348

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Palastanga N, Field D, Soames R (2006) Anatomy and human movement: structure and function. Elsevier, London

    Google Scholar 

  • Pette D, Staron RS (2000) Myosin isoform, muscle fiber type, and transitions. Microsc Res Tech 50:500–509

    Article  CAS  PubMed  Google Scholar 

  • Potau JM, Artells R, Bello G et al (2011) Expression of myosin heavy chain isoforms in the supraspinatus muscle of different primate species: implications for the study of the adaptation of primate shoulder muscles to different locomotor modes. Int J Primatol 32:931–944

    Article  Google Scholar 

  • Potau JM, Casado A, de Diego M et al (2018) Structural and molecular study of the supraspinatus muscle of modern humans (Homo sapiens) and common chimpanzees (Pan troglodytes). Am J Phys Anthropol 166:934–940

    Article  CAS  PubMed  Google Scholar 

  • Rose MD (1993) Functional anatomy of the elbow and forearm in primates. In: Gebo DL (ed) Postcranial adaptation in nonhuman primates. Northern Illinois University Press, DeKalb, pp 70–95

    Google Scholar 

  • Rowe N (1996) The pictorial guide to the living primates. Pogonias Press, Charlestown

    Google Scholar 

  • Schiaffino S, Reggiani C (2011) Fiber types in mammalian skeletal muscles. Physiol Rev 91:1447–1531

    Article  CAS  PubMed  Google Scholar 

  • Sciote JJ, Morris TJ (2000) Skeletal muscle function and fibre types: the relationship between occlusal function and the phenotype of jaw-closing muscles in human. J Orthod 27:15–30

    Article  CAS  PubMed  Google Scholar 

  • Short KR, Vittone JL, Bigelow ML et al (2005) Changes in myosin heavy chain mRNA and protein expression in human skeletal muscle with age and endurance exercise training. J Appl Physiol 99:95–102

    Article  CAS  PubMed  Google Scholar 

  • Stroyan M, Wilk KE (1993) The functional anatomy of the elbow complex. J Orthop Sports Phys Ther 17:279–288

    Article  CAS  PubMed  Google Scholar 

  • Thorpe SKS, Crompton RH, Günther MM, Ker RF, Alexander RM (1999) Dimensions and moment arms of the hind- and forelimb muscles of common chimpanzees (Pan troglodytes). Am J Phys Anthropol 110:179–199

    Article  CAS  PubMed  Google Scholar 

  • Tirrell TF, Cook MS, Carr JA, Lin E, Ward SR, Lieber RL (2012) Human skeletal muscle biochemical diversity. J Exp Biol 215:2551–2559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tomsick SD, Petersen BD (2010) Normal anatomy and anatomical variants of the elbow. Semin Musculoskelet Radiol 14:379–393

    Article  PubMed  Google Scholar 

  • Tuttle RH, Basmajian JV (1974) Electromyography of brachial muscles in Pan gorilla and hominoid evolution. Am J Phys Anthropol 41:71–90

    Article  Google Scholar 

  • Tuttle RH, Velte MJ, Basmajian JV (1983) Electromyography of brachial muscles in Pan troglodytes and Pongo pygmaeus. Am J Phys Anthropol 61:75–83

    Article  CAS  PubMed  Google Scholar 

  • Wiley DF Amenta N Alcantara DA et al. (2006) Evolutionary Morphing, Landmark Editor 3.0. IDAV. University of California, Davis. https://www.idav.ucdavis.edu/research/EvoMorph. Accessed 10 Jan 2017

  • Zelditch ML, Swiderski DL, Sheets HD, Fink WL (2004) Geometric morphometrics for biologists: a primer. Academic Press, New York

    Google Scholar 

  • Ziegler AC (1964) Brachiating adaptations of chimpanzee upper limb musculature. Am J Phys Anthropol 22:15–31

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Manuel Martín, Sebastián Mateo, and Pau Rigol (Body Donation Service, University of Barcelona) for their support and collaboration. We would also like to thank Renee Grupp for assistance in drafting the manuscript. This study was funded by the Ministerio de Economía y Competitividad of Spain (project CGL2014-52611-C2-2-P to JMP) and by the European Union (FEDER) and by the Ajudes Predoctorals of the University of Barcelona (APIF-UB 2016/2017 to AC).

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Authors and Affiliations

  1. Unit of Human Anatomy and Embryology, University of Barcelona, C/Casanova 143, 08036, Barcelona, Spain

    Marina de Diego, Aroa Casado, Mónica Gómez, Joshua Martín & Josep Maria Potau

  2. Department of Anatomy and Radiology, University of Valladolid, C/Ramón y Cajal 7, 47005, Valladolid, Spain

    Juan Francisco Pastor

Authors
  1. Marina de Diego
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  2. Aroa Casado
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  3. Mónica Gómez
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  4. Joshua Martín
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  5. Juan Francisco Pastor
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  6. Josep Maria Potau
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Contributions

MD, JMP, AC and JFP participated in the dissection of the human and the chimpanzee samples. MD, AC, MG and JM performed the 3D GM analysis. MD and JMP performed the architectural analysis. MD and MG performed the molecular analysis. All the authors participated in the study design, in the collection, analysis and interpretation of data, in the writing and review of the manuscript, and in the decision to submit the article for publication.

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Correspondence to Josep Maria Potau.

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The authors have no conflicts of interest to declare.

Ethical approval

The research complied with protocols approved by the Institutional Animal Care and Use Committee of the University of Barcelona and adhered to the legal requirements of Spain.

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The data that support the findings of this study are available from the corresponding author upon reasonable request.

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de Diego, M., Casado, A., Gómez, M. et al. Structural and molecular analysis of elbow flexor muscles in modern humans and common chimpanzees. Zoomorphology 139, 277–290 (2020). https://doi.org/10.1007/s00435-020-00482-5

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