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Epaxial Musculature in Armadillos, Sloths, and Opossums: Functional Significance and Implications for the Evolution of Back Muscles in the Xenarthra

Journal of Mammalian Evolution volume 25, pages 565–572 (2018)Cite this article

Abstract

To investigate the evolution of xenarthran epaxial muscles, fresh specimens of the North American Common long-nosed armadillo Dasypus novemcinctus and of a marsupial, the Virginia opossum Didelphis virginiana, were dissected. Data from one fixed specimen of a two-toed sloth Choloepus didactylus were also used for comparison, because it is a xenarthran exhibiting a highly derived locomotor mode. The opossum was used to represent a more generalized mammalian condition. Each of the three mammalian epaxial muscle groups, the iliocostalis, longissimus dorsi, and transversospinalis, was removed and its mass was determined. All data were corrected for body mass and length. Unpaired, one-tailed t-tests showed the average mass of the iliocostalis and transversospinalis of Dasypus to be significantly larger than the mass of the same muscles in Didelphis, whereas the average mass of the longissimus dorsi was not statistically different between the two species. In agreement with pronounced lateral bending and de-emphasized dorso-ventral flexion and extension, Choloepus also had a relatively large iliocostalis and small longissimus. Our limited data suggest that this condition was inherited from non-arboreal and probably digging early xenarthrans. We believe the relatively larger iliocostalis and transversospinalis muscles in Dasypus can be attributed to the need to provide vertical stabilization of the trunk and resist lateral reaction forces generated by digging. Thus, for Xenarthra it represents a synapomorphy linked to adaptations for fossoriality.

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Notes

  1. Coues (1872:101) description of the muscles in this region differs from the terminology used here, and is somewhat confusing to us. He recognized a fused erector spinae comprised of longissimus dorsi and “sacro-lumbalis” muscles. The latter, presumably the posterior part of iliocostalis, has an “upward [=cranial?] prolongation” called “musculus accessorius,” and is purportedly blended with the quadratus lumborum, which is a hypaxial muscle, internal to the mm. transversus abdominus, external and internal obliques in humans (Pick and Howden 1977; Clemente 1987) and other mammals (Evans and Christiansen 1979; Homberger and Walker 2004). We follow Slijper (1946: table 3), who recognized a separate “iliocostalis lumborum” in the related opossum Metacheirus, which is attached but not fused to the “pars ilio-lumbalis of M. longissimus dorsi.” We saw no evidence of a fusion between the iliocostalis and quadratus lumborum.

References

  • Bard P (1956) Medical Physiology, 10th edition. CV Mosby Co., St. Louis

    Google Scholar 

  • Carrier DR (1998) Evolution and function of the axial muscles in terrestrial vertebrates. Am Zool 38:174A

    Article  Google Scholar 

  • Clemente CD (1987) Anatomy. A Regional Atlas of the Human Body, 3rd edition. Urban and Schwarzenburg, Inc., Baltimore

    Google Scholar 

  • Coues E (1872) The osteology and myology of Didelphys virginiana. Mem Boston Soc Nat Hist 2:41–149

    Google Scholar 

  • Cuvier G, Laurillard M (1849) Recueil de Planches de Myologie. Dusacq, Paris

    Google Scholar 

  • Engelmann G (1985) The phylogeny of the Xenarthra. In: Montgomery GG (ed) The Ecology and Evolution of Armadillos, Sloths, and Vermilinguas. Smithsonian Institution Press, Washington, D.C., pp 51–64

    Google Scholar 

  • English AW (1980) The functions of the lumbar spine during stepping in the cat. J Morphol 165:55–66

    Article  Google Scholar 

  • Ercoli MD, Álvarez A, Busker F, Morales MM, Julik E, Smith HF, Adrian B, Barton M, Bhagavatula K, Poole M, Shahsavan M, Wechsler R, Fisher RE (2016) Myology of the head, neck, and thoracic region of the lesser grison (Galictis cuja) in comparison with the red panda (Ailurus fulgens) and other carnivorans: phylogenetic and functional implications. J Mammal Evol doi:10.1007/s10914-016-9339-8.

    Article  Google Scholar 

  • Evans HE, Christiansen GC (1979) Miller’s Anatomy of the Dog, 2nd edition. W.B. Saunders, Philadelphia

    Google Scholar 

  • Frechkop S (1949) Explication biologique, fournie par les Tatous, d’un des caractères distinctifs des Xénarthres et d’un caractère adaptif analogue chez les Pangolins. Inst R Sci Natl Belg 25:1–12

    Google Scholar 

  • Gasc JP, Jouffroy FK, Renous S, von Blottnitz F (1986) Morphofunctional study of the digging system of the Namib Desert Golden mole (Eremitalpa granti namibensis): cinefluorographical and anatomical analysis. J Zool London 208:9–35

    Article  Google Scholar 

  • Gaudin TJ (1999) The evolution of xenarthrous vertebrae (Mammalia, Xenarthra). Fieldiana Geol N. S. 41:1–38

    Google Scholar 

  • Gaudin TJ, Biewener AA (1992) The functional morphology of xenarthrous vertebrae in the armadillo Dasypus novemcinctus (Mammalia, Xenarthra). J Morphol 214:63–81

    Article  CAS  Google Scholar 

  • Gaudin TJ, Croft DA (2015) Paleogene Xenarthra and the evolution of South American mammals. J Mammal 96(4):622–634

    Article  Google Scholar 

  • Gaudin TJ, McDonald HG (2008) Chapter 3. Morphology-based investigations of the phylogenetic relationships among extant and fossil Xenarthrans. In: Loughry WJ, Vizcaíno SF (eds) Biology of the Xenarthra. University of Florida Press, Gainesville, pp 24–36

    Google Scholar 

  • Goffart M (1971) Function and Form in the Sloth. Pergamon Press, New York

    Google Scholar 

  • Homberger DG, Walker WF (2004) Vertebrate Dissection, 9th edition. Thomson Brooks/Cole, Belmont

    Google Scholar 

  • Jenkins FA Jr (1971) Limb posture and locomotion in the Virginia opossum (Didelphis marsupialis) and in other non-cursorial mammals. J Zool London 165(3):303–315

    Article  Google Scholar 

  • Mendel FC (1985) Adaptations for suspensory behavior in the limbs of two-toed sloths. In: Montgomery GG (ed) The Ecology and Evolution of Armadillos, Sloths, and Vermilinguas. Smithsonian Institution Press, Washington, D.C., pp 151–162

    Google Scholar 

  • Mendez J, Keys A (1960) Density and composition of mammalian muscle. Metabolism 9(2):184–188

    CAS  Google Scholar 

  • Nassar PN, Carrier DR (1992) Function of epaxial muscles during trotting. Am Zool 32:148A

    Google Scholar 

  • Neufuss J, Hesse B, Thorpe SKS, Vereecke EE, D’Aout K, Fischer MS, Schilling N (2014) Fibre type composition in the lumbar perivertebral muscles of primates: implications for the evolution of orthogrady in hominoids. J Anat 224(2):113–131. doi: 10.1111/joa.12130

    Article  CAS  PubMed  Google Scholar 

  • Nomina Anatomica Veterinaria (2005) International Committee on Veterinary Gross Anatomical Nomenclature, 5th edition. Editorial Committee, World Association of Veterinary Anatomists, Hannover

    Google Scholar 

  • Nyakatura JA (2012) The convergent evolution of suspensory posture and locomotion in tree sloths. J Mammal Evol 19(3):225–234

    Article  Google Scholar 

  • Nyakatura JA, Fischer MS (2010) Functional morphology and three-dimensional kinematics of the thoraco-lumbar region of the spine of the two-toed sloth. J Exp Biol 213(24):4278–4290

    Article  Google Scholar 

  • Nyakatura JA, Stark H (2015) Aberrant back muscle function correlates with intramuscular architecture of dorsovertebral muscles in two-toed sloths. Mammal Biol 80(2):114–121

    Article  Google Scholar 

  • Oliver JD, Jones KE, Hautier L, Loughry WJ, Pierce SE (2016) Vertebral bending mechanics and xenarthrous morphology in the nine-banded armadillo (Dasypus novemcinctus). J Exp Biol 219(19):2991–3002

    Article  Google Scholar 

  • Pick TP, Howden R (1977) Gray’s Anatomy, 15th edition. Bounty Books, New York

    Google Scholar 

  • Pridmore PA (1992) Trunk movements during locomotion in the marsupial Monodelphis domestica (Didelphidae). J Morphol 211(2):137–146

    Article  Google Scholar 

  • Ritter D (1995) Epaxial muscle function during locomotion in a lizard (Varanus salvator) and the proposal of a key innovation in the vertebrate axial musculoskeletal system. J Exp Biol 198:2477–2490

    CAS  PubMed  Google Scholar 

  • Ritter D (1996) Axial muscle function during lizard locomotion. J Exp Biol 199:2499–2510

    CAS  PubMed  Google Scholar 

  • Rose KD, Emry RJ (1993) Relationships of Xenarthra, Pholidota, and fossil “edentates.” In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammal Phylogeny: Placentals. Springer-Verlag, New York, pp 81–102

    Chapter  Google Scholar 

  • Schilling N, Carrier, DR (2009) Function of the epaxial muscles during trotting. J Exp Biol 212(7):1053–1063

    Article  Google Scholar 

  • Schilling N, Carrier DR (2010) Function of the epaxial muscles in walking, trotting and galloping dogs: implications for the evolution of epaxial muscle function in tetrapods. J Exp Biol 213(9):1490–1502

    Article  Google Scholar 

  • Shapiro LJ, Jungers WL (1994) Electromyography of back muscles during quadrupedal and bipedal walking in primates. Am J Phys Anthropol 93:491–504

    Article  CAS  Google Scholar 

  • Slijper EJ (1946) Comparative biologic-anatomical investigations on the vertebral column and spinal musculature of mammals. Verh Kon Ned Akad Wet, AFD. Nat (Tweede Sectie) 17:1–128

    Google Scholar 

  • Vaughan TA, Ryan JM, Czaplewski NJ (2015) Mammalogy, 6th edition. Jones and Bartlett Learning, Burlington

    Google Scholar 

  • White TD (1990) Gait selection in the brush-tail possum (Trichosurus vulpecula), the northern quoll (Dasyurus hallucatus), and the Virginia Opossum (Didelphis virginiana). J Mammal 71(1):79–84

    Article  Google Scholar 

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Acknowledgements

This project began as an undergraduate research project by Ms. Laurie Fortin (student of TJG, then a Visiting Professor at the College of the Holy Cross) in 1993-4. However, the manuscript has morphed considerably in the ensuing 23-plus years, and it was no longer possible to contact Ms. Fortin to obtain her permission to be included as an author. Nevertheless, she should be credited for doing the original work of dissection, measurement, and statistical calculations. We also wish to thank the Department of Biology at the College of the Holy Cross for furnishing laboratory facilities and funding for this project. The armadillo and opossum specimens dissected were purchased from Ray Singleton & Co. of Arcadia, Fla. We thank Bruce Patterson and the late Bill Stanley of the Department of Mammalogy at the Field Museum of Natural History, Chicago, for access to specimens of various fossorial mammals examined in connection with this report. Mary Morton graciously provided us access to her lyopholyzer. We thank Andy Biewener, David Carrier, Virginia Naples, Ann Pabst, Laura Panko, John Wible, guest editor Susanna Bargo, reviewer Marcos Ercoli, and a second, anonymous reviewer for critical comments on earlier drafts of this manuscript, and Susan Berman, Mary Morton, and Laura Panko for encouragement and suggestions.

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  1. Department of Biology, Geology, and Environmental Science, University of Tennessee at Chattanooga, 615 McCallie Ave., Dept. 2653, Chattanooga, TN, 37403-2598, USA

    Timothy J. Gaudin

  2. Image Knowledge Gestaltung: An Interdisciplinary Laboratory, Institute of Biology, Humboldt University, 10099, Berlin, Germany

    John A. Nyakatura

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Correspondence to Timothy J. Gaudin.

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Gaudin, T.J., Nyakatura, J.A. Epaxial Musculature in Armadillos, Sloths, and Opossums: Functional Significance and Implications for the Evolution of Back Muscles in the Xenarthra. J Mammal Evol 25, 565–572 (2018). https://doi.org/10.1007/s10914-017-9402-0

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