Vertical clinging is a specialized form of locomotion characteristic of the primate family Callitrichidae. Vertical clinging requires these pronograde primates to maintain a vertical posture, so the protraction of their forelimbs must resist gravity. Since pronograde primates usually move as horizontal quadrupeds, we hypothesized that the supraspinatus muscle of vertical clingers would present specific characteristics related to the functional requirements imposed on the shoulder area by vertical clinging. To test this hypothesis, we quantified by real-time quantitative polymerase chain reaction the mRNA transcripts of myosin heavy chain (MHC) isoforms in the supraspinatus muscle of 15 species of pronograde primates, including vertical clingers. Our results indicate that the supraspinatus of vertical clingers has a specific expression pattern of the MHC isoforms, with a low expression of the transcripts of the slow MHC-I isoform and a high expression of the transcripts of the fast MHC-II isoforms. We conclude that these differences can be related to the particular functional characteristics of the shoulder in vertical clingers, but also to other anatomical adaptations of these primates, such as their small body size.

Keywords:
Myosin heavy chain, Supraspinatus, Vertical clinging
1.
Alpert SW, Pink MM, Jobe FW, McMahon PJ, Mathiyakom W (2000). Electromyographic analysis of deltoid and rotator cuff function under varying loads and speeds. Journal of Shoulder and Elbow Surgery 9: 47-58.
2.
Anapol F, Gray JP (2003). Fiber architecture of the intrinsic muscles of the shoulder and arm in semiterrestrial and arboreal guenons. American Journal of Physical Anthropology 122: 51-65.
3.
Arnold C, Matthews LJ, Nunn CL (2010). The 10kTrees website: a new online resource for primate phylogeny. Evolutionary Anthropology 19: 114-118.
4.
Baldwin KM, Haddad F (2001). Plasticity in skeletal, cardiac, and smooth muscle. Journal of Applied Physiology 90: 345-357.
5.
Basmajian JV, de Luca CJ (1985). Muscles Alive. Their Functions Revealed by Electromyography. Baltimore, Williams & Wilkins.
6.
Bottinelli R, Pellegrino MA, Canepari M, Rossi R, Reggiani C (1999). Specific contributions of various muscle fibre types to human muscle performance: an in vitro study. Journal of Electromyography and Kinesiology 9: 87-95.
7.
Bottinelli R, Reggiani C (2000). Human skeletal muscle fibres: molecular and functional diversity. Progress in Biophysics and Molecular Biology 73: 195-262.
8.
Fleagle JG (1999). Primate Adaptation and Evolution. New York, Academic Press.
9.
Garber PA (1992). Vertical clinging, small body size, and the evolution of feeding adaptations in the Callitrichinae. American Journal of Physical Anthropology 88: 469-482.
10.
Garland JT, Harvey PH, Ives AR (1992). Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology 41: 18-32.
11.
Gebo DL (2014). Primate Comparative Anatomy. Baltimore, Johns Hopkins University Press.
12.
Inman VT, Saunders JB, Abbott LC (1944). Observations on the function of the shoulder joint. Journal of Bone and Joint Surgery 26: 1-30.
13.
Jackson CP (2011). The positional behavior of pygmy marmosets (Cebuella pygmaea) in northwestern Bolivia. Primates 52: 171-178.
14.
Kohn TA, Hoffman LC, Myburgh KH (2007). Identification of myosin heavy chain isoforms in skeletal muscle of four Southern African wild ruminants. Comparative Biochemistry and Physiology - Part A 148: 399-407.
15.
Larson SG, Stern JT (1986). EMG of scapulohumeral muscles in the chimpanzee during reaching and “arboreal” locomotion. American Journal of Anatomy 176: 171-190.
16.
Larson S, Stern J (1989). Role of supraspinatus in the quadrupedal locomotion of vervets (Cercopithecus aethiops): implications for interpretation of humeral morphology. American Journal of Physical Anthropology 79: 369-377.
17.
Larson S, Stern J (1992). Further evidence for the role of supraspinatus in quadrupedal monkeys. American Journal of Physical Anthropology 87: 359-363.
18.
Napier JR, Walker AC (1967). Vertical clinging and leaping - a newly recognized category of primate locomotion. Folia Primatologica 6: 204-219.
19.
Pette D, Staron RS (2000). Myosin isoforms, muscle fiber types, and transitions. Microscopic Research and Technique 50: 500-509.
20.
Porter LM (2004). Forest use and activity patterns of Callimico goeldii in comparison to two sympatric tamarins, Saguinus fuscicollis and Saguinus labiatus. American Journal of Physical Anthropology 124: 139-153.
21.
Potau JM, Artells R, Bello G, Muñoz C, Monzó M, Pastor JF, de Paz F, Barbosa M, Diogo R, Wood B (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. International Journal of Primatology 32: 931-944.
22.
Preuschoft H, Hohn B, Scherf H, Schmidt M, Krause C, Witzel U (2010). Functional analysis of the primate shoulder. International Journal of Primatology 31: 301-320.
23.
Resnicow DI, Deacon JC, Warrick HM, Spudich JA, Leinwand LA (2010). Functional diversity among a family of human skeletal muscle myosin motors. Proceedings of the National Academy of Sciences of the United States of America 107: 1053-1058.
24.
Rowe N (1996). The Pictorial Guide to the Living Primates. Charlestown, Pogonias Press.
25.
Schmitt D (2003). Evolutionary implications of the unusual walking mechanics of the common marmoset (C. jacchus). American Journal of Physical Anthropology 122: 28-37.
26.
Schmitt D (2010). Primate locomotor evolution: biomechanical studies of primate locomotion and their implications for understanding primate neuroethology. In Primate Neuroethology (Platt ML, AA Ghazanfar, eds.), pp 31-63. New York, Oxford University Press.
27.
Schmidt M, Schilling N (2007). Fiber type distribution in the shoulder muscles of the tree shrew, the cotton-top tamarin, and the squirrel monkey related to shoulder movements and forelimb loading. Journal of Human Evolution 52: 401-419.
28.
Toniolo L, Maccatrozzo L, Patruno M, Caliaro F, Mascarello F, Reggiani C (2005). Expression of eight distinct MHC isoforms in bovine striated muscles: evidence for MHC-2B presence only in extraocular muscles. Journal of Experimental Biology 208: 4243-4253.
29.
Tuttle RH, Basmajian JV (1978). Electromyography of pongid shoulder muscles. Part II, deltoid, rhomboid, and “rotator cuff.” American Journal of Physical Anthropology 49: 47-56.
30.
Youlatos D (1999). Positional behavior of Cebuella pygmaea in Yasuni National Park. Ecuador. Primates 40: 543-550.
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