open access

Vol 77, No 1 (2018)
ORIGINAL ARTICLES
Published online: 2017-07-06
Submitted: 2017-04-04
Accepted: 2017-06-19
Get Citation

Variability and constraint of vertebral formulae and proportions in colugos, tree shrews, and rodents, with special reference to vertebral modification by aerodynamic adaptation

T. Kawashima, R. W. Thorington Jr., P. W. Bohaska, F. Sato
DOI: 10.5603/FM.a2017.0064
·
Pubmed: 28703847
·
Folia Morphol 2018;77(1):44-56.

open access

Vol 77, No 1 (2018)
ORIGINAL ARTICLES
Published online: 2017-07-06
Submitted: 2017-04-04
Accepted: 2017-06-19

Abstract

Background: The aim of the present study is to provide the first large data set on vertebral formulae and proportions, and examine their relationship with different locomotive modes in colugos (Dermoptera), tree shrews (Scandentia), and rodents (Rodentia), which have been considered less variable because they were thought to have a plesiomorphic number of 19 thoracolumbar vertebrae.

Materials and methods: The data included 33 colugos and 112 tree shrews, which are phylogenetically sister taxa, and 288 additional skeletons from 29 other mammalian species adapted to different locomotive modes, flying, gliding, arboreal, terrestrial, digging, and semi-aquatic habitats.

Results: The following results were obtained: (1) intra-/interspecies variability and geographical variation in thoracic, lumbar, and thoracolumbar counts were present in two gliding colugo species and 12 terrestrial/arboreal tree shrew species; (2) in our examined mammals, some aerodynamic mammals, such as colugos, southern flying squirrels, scaly-tailed squirrels, and bats, showed exceptionally high amounts of intraspecific variation of thoracic, lumbar, and thoracolumbar counts, and sugar gliders and some semi-aquatic rodents also showed some variation; (3) longer thoracic and shorter lumbar vertebrae were typically shared traits among the examined mammals, except for flying squirrels (Pteromyini) and scaly-tailed squirrels (Anomaluridae).

Conclusions: Our study reveals that aerodynamic adaptation could potentially lead to strong selection and modification of vertebral formulae and/or proportions based on locomotive mode despite evolutionary and developmental constraints. (Folia Morphol 2018; 77, 1: 44–56) Background: The aim of the present study is to provide the first large data set on vertebral formulae and proportions, and examine their relationship with different locomotive modes in colugos (Dermoptera), tree shrews (Scandentia), and rodents (Rodentia), which have been considered less variable because they were thought to have a plesiomorphic number of 19 thoracolumbar vertebrae. Materials and methods: The data included 33 colugos and 112 tree shrews, which are phylogenetically sister taxa, and 288 additional skeletons from 29 other mammalian species adapted to different locomotive modes, flying, gliding, arboreal, terrestrial, digging, and semi-aquatic habitats.

Results: The following results were obtained: (1) intra-/interspecies variability and geographical variation in thoracic, lumbar, and thoracolumbar counts were present in two gliding colugo species and 12 terrestrial/arboreal tree shrew species; (2) in our examined mammals, some aerodynamic mammals, such as colugos, southern flying squirrels, scaly-tailed squirrels, and bats, showed exceptionally high amounts of intraspecific variation of thoracic, lumbar, and thoracolumbar counts, and sugar gliders and some semi-aquatic rodents also showed some variation; (3) longer thoracic and shorter lumbar vertebrae were typically shared traits among the examined mammals, except for flying squirrels (Pteromyini) and scaly-tailed squirrels (Anomaluridae). Conclusions: Our study reveals that aerodynamic adaptation could potentially lead to strong selection and modification of vertebral formulae and/or proportions based on locomotive mode despite evolutionary and developmental constraints. (Folia Morphol 2018; 77, 1: 44–56)

Abstract

Background: The aim of the present study is to provide the first large data set on vertebral formulae and proportions, and examine their relationship with different locomotive modes in colugos (Dermoptera), tree shrews (Scandentia), and rodents (Rodentia), which have been considered less variable because they were thought to have a plesiomorphic number of 19 thoracolumbar vertebrae.

Materials and methods: The data included 33 colugos and 112 tree shrews, which are phylogenetically sister taxa, and 288 additional skeletons from 29 other mammalian species adapted to different locomotive modes, flying, gliding, arboreal, terrestrial, digging, and semi-aquatic habitats.

Results: The following results were obtained: (1) intra-/interspecies variability and geographical variation in thoracic, lumbar, and thoracolumbar counts were present in two gliding colugo species and 12 terrestrial/arboreal tree shrew species; (2) in our examined mammals, some aerodynamic mammals, such as colugos, southern flying squirrels, scaly-tailed squirrels, and bats, showed exceptionally high amounts of intraspecific variation of thoracic, lumbar, and thoracolumbar counts, and sugar gliders and some semi-aquatic rodents also showed some variation; (3) longer thoracic and shorter lumbar vertebrae were typically shared traits among the examined mammals, except for flying squirrels (Pteromyini) and scaly-tailed squirrels (Anomaluridae).

Conclusions: Our study reveals that aerodynamic adaptation could potentially lead to strong selection and modification of vertebral formulae and/or proportions based on locomotive mode despite evolutionary and developmental constraints. (Folia Morphol 2018; 77, 1: 44–56) Background: The aim of the present study is to provide the first large data set on vertebral formulae and proportions, and examine their relationship with different locomotive modes in colugos (Dermoptera), tree shrews (Scandentia), and rodents (Rodentia), which have been considered less variable because they were thought to have a plesiomorphic number of 19 thoracolumbar vertebrae. Materials and methods: The data included 33 colugos and 112 tree shrews, which are phylogenetically sister taxa, and 288 additional skeletons from 29 other mammalian species adapted to different locomotive modes, flying, gliding, arboreal, terrestrial, digging, and semi-aquatic habitats.

Results: The following results were obtained: (1) intra-/interspecies variability and geographical variation in thoracic, lumbar, and thoracolumbar counts were present in two gliding colugo species and 12 terrestrial/arboreal tree shrew species; (2) in our examined mammals, some aerodynamic mammals, such as colugos, southern flying squirrels, scaly-tailed squirrels, and bats, showed exceptionally high amounts of intraspecific variation of thoracic, lumbar, and thoracolumbar counts, and sugar gliders and some semi-aquatic rodents also showed some variation; (3) longer thoracic and shorter lumbar vertebrae were typically shared traits among the examined mammals, except for flying squirrels (Pteromyini) and scaly-tailed squirrels (Anomaluridae). Conclusions: Our study reveals that aerodynamic adaptation could potentially lead to strong selection and modification of vertebral formulae and/or proportions based on locomotive mode despite evolutionary and developmental constraints. (Folia Morphol 2018; 77, 1: 44–56)

Get Citation

Keywords

colugo, tree shrew, aerodynamic mammals, vertebral column, gliding adaptation

About this article
Title

Variability and constraint of vertebral formulae and proportions in colugos, tree shrews, and rodents, with special reference to vertebral modification by aerodynamic adaptation

Journal

Folia Morphologica

Issue

Vol 77, No 1 (2018)

Pages

44-56

Published online

2017-07-06

DOI

10.5603/FM.a2017.0064

Pubmed

28703847

Bibliographic record

Folia Morphol 2018;77(1):44-56.

Keywords

colugo
tree shrew
aerodynamic mammals
vertebral column
gliding adaptation

Authors

T. Kawashima
R. W. Thorington Jr.
P. W. Bohaska
F. Sato

References (63)
  1. Aimi M. Numerical variation of vertebrae in Japanese macaques, macaca fuscata. Anthropol Sci. 1994; 102(Supplement): 1–10.
  2. Asher RJ, Lin KH, Kardjilov N, et al. Variability and constraint in the mammalian vertebral column. J Evol Biol. 2011; 24(5): 1080–1090.
  3. Barbour RA. Anatomy of marsupials. In: Stonehouse B and Gilmore D (eds.). The biology of marsupials. . University Park Press, Baltimore 1977: 237–272.
  4. Beard KC. Origin and evolution of gliding in early Cenozoic Dermoptera (Mammalia, Primatomorpha). In: MacPhee RDE (ed.). Primates and their relatives in phylogenetic perspective. . Plenum Press, New York 1993: 63–90.
  5. Boyer DM, Bloch JI. Evaluating the mitten-gliding hypothesis for Paromomyidae and Micromomyidae (Mammalia, “Plesiadapiformes”) using comparative functional morphology of new Paleogene skeletons. In: Dagosto MJ, Sargis EJ (eds.). Mammalian evolutionary morphology. A tribute to Frederick S. Szalay. . Springer- Verlag, New York 2008: 231–279.
  6. Buchholtz E. Vertebral and rib anatomy in Caperea marginata: Implications for evolutionary patterning of the mammalian vertebral column. Marine Mammal Science. 2010; 27(2): 382–397.
  7. Buchholtz EA, Stepien CC. Anatomical transformation in mammals: developmental origin of aberrant cervical anatomy in tree sloths. Evol Dev. 2009; 11(1): 69–79.
  8. Burke AC, Nelson CE, Morgan BA, et al. Hox genes and the evolution of vertebrate axial morphology. Development. 1995; 121(2): 333–346.
  9. Cartmill M, Milton K. The lorisiform wrist joint and the evolution of "brachiating" adaptations in the hominoidea. Am J Phys Anthropol. 1977; 47(2): 249–272.
  10. Clutton-Brock J, Wilson DE. Mammals. Smithsonian handbooks DK, New York 2002.
  11. Cohn MJ, Tickle C. Developmental basis of limblessness and axial patterning in snakes. Nature. 1999; 399(6735): 474–479.
  12. Cordes R, Schuster-Gossler K, Serth K, et al. Specification of vertebral identity is coupled to Notch signalling and the segmentation clock. Development. 2004; 131(6): 1221–1233.
  13. Davis DD. Notes on the anatomy of the treeshrew Dendrogale. Field Mus Nat His (Zool Series. 1938; 20: 383–404.
  14. De Blainville HMD. Ostéographie ou description iconographique comparée du squelette et du système dentaire des mammifères récents et fossils. JB Bailliére et Fils. Paris. 1840.
  15. Doyle GA, Walker AC. D’Souza F.A preliminary field report on the lessor tree shrew Tupaia minor. In: Martin RD, Doyle GA, Walker AC (eds.). Prosimian biology. Duckworth, London 1974: 167–182.
  16. Filler AG. Homeotic evolution in the mammalia: diversification of therian axial seriation and the morphogenetic basis of human origins. PLoS One. 2007; 2(10): e1019.
  17. Flower W. An introduction to the osteology of the Mammalia. Macmillan, London. 1885.
  18. Galis F, Carrier DR, van Alphen J, et al. Fast running restricts evolutionary change of the vertebral column in mammals. Proc Natl Acad Sci U S A. 2014; 111(31): 11401–11406.
  19. Gaunt SJ. Conservation in the Hox code during morphological evolution. Int J Dev Biol. 1994; 38(3): 549–552.
  20. Granatosky MC, Lemelin P, Chester SGB, et al. Functional and evolutionary aspects of axial stability in euarchontans and other mammals. J Morphol. 2014; 275(3): 313–327.
  21. Granatosky MC, Miller CE, Boyer DM, et al. Lumbar vertebral morphology of flying, gliding, and suspensory mammals: implications for the locomotor behavior of the subfossil lemurs Palaeopropithecus and Babakotia. J Hum Evol. 2014; 75: 40–52.
  22. Gregory WK. Relationship of the Tupaiidae and of Eocene Lemurs, especially Notharctus. Bull Geol Soc Am. 1913; 24(1): 247–252.
  23. Hautier L, Weisbecker V, Sánchez-Villagra MR, et al. Skeletal development in sloths and the evolution of mammalian vertebral patterning. Proc Natl Acad Sci U S A. 2010; 107(44): 18903–18908.
  24. Ikeya M, Takada S. Wnt-3a is required for somite specification along the anteroposterior axis of the mouse embryo and for regulation of cdx-1 expression. Mech Dev. 2001; 103(1-2): 27–33.
  25. Janecka JE, Miller W, Pringle TH, et al. Molecular and genomic data identify the closest living relative of primates. Science. 2007; 318(5851): 792–794.
  26. Jenkins FA. Anatomy and function of expanded ribs in certain edentates and primates. J Mammal. 1970; 51(2): 288–301.
  27. Kawashima T, Murakami K, Takayanagi M, et al. Evolutionary transformation of the cervicobrachial plexus in the colugo (Cynocephalidae: Dermoptera) with a comparison to treeshrews (Tupaiidae: Scandentia) and strepsirrhines (Strepsirrhini: Primates). Folia Morphol. 2012; 71(4): 228–239.
  28. Kawashima T, Thorington RW, Bohaska PW, et al. Evolutionary Transformation of the Palmaris Longus Muscle in Flying Squirrels (Pteromyini: Sciuridae): An Anatomical Consideration of the Origin of the Uniquely Specialized Styliform Cartilage. Anat Rec. 2017; 300(2): 340–352.
  29. Leche W. Über die Säugethiergattung Galeopithecus eine Morphologische Untersuchung. Kungl Svenska Ventenskap Akad Stochholm. 1886; 21: 3–92.
  30. Le Gros Clark WE. On the Anatomy of the Pen-tailed Tree-Shrew (Ptilocercus lowii.). Proc zool Soc Lond. 1926; 96(4): 1179–1309.
  31. Lim N. Colugo. The flying lemur of South-east Asia. Draco Publishing & Distribution Pte Ltd. And National University of Singapore, Singapore 2007.
  32. Lyon M. Treeshrews: An account of the mammalian family Tupaiidae. Proc US Nat Mus. 1913; 45(1976): 1–188.
  33. Narita Y, Kuratani S. Evolution of the vertebral formulae in mammals: a perspective on developmental constraints. J Exp Zool B Mol Dev Evol. 2005; 304(2): 91–106.
  34. Norberg UM. Functional osteology and myology of the wing of Plecotus auritus Linnaeus (Chiroptera). Arkiv för Zoologi. 1968; 22: 483–543.
  35. Norberg U. Functional osteology and myology of the wing of the dog-faced bat Rousettus aegyptiacus (É. Geoffroy)(Mammalia, Chiroptera). Z Morph Tiere. 1972; 73(1): 1–44.
  36. Owen R. Outlines of a classification of the Masupialia. Trans Zool Soc London. 1841; 2: 315–333.
  37. Owen R. On the osteology of the Marsupialia. Trans Zool Soc London. 1841; 2: 379–408.
  38. Owen R. Descriptive catalogue of the osteological series contained in the museum of the of England. Royal College of Surgeons. London. 1853.
  39. Pilbeam D. The anthropoid postcranial axial skeleton: comments on development, variation, and evolution. J Exp Zool B Mol Dev Evol. 2004; 302(3): 241–267.
  40. Sargis E. A preliminary qualitative analysis of the axial skeleton of tupaiids (Mammalia, Scandentia): functional morphology and phylogenetic implications. J Zool. 2001; 253(4): 473–483.
  41. Sawin P. Preliminary studies of hereditary variation in the axial skeleton of the rabbit. Anat Rec. 1937; 69(4): 407–428.
  42. Sánchez‐Villagra M, Narita Y, Kuratani S. Thoracolumbar vertebral number: The first skeletal synapomorphy for afrotherian mammals. Systematics and Biodiversity. 2007; 5(1): 1–7.
  43. Schultz A. Vertebral column and thorax. In: Hofer H, Schultz AH, Starck D (eds.). Primatologia Vol IV S Karger, Basel 1961: 1–66.
  44. Shapiro LJ, Simons CVM. Functional aspects of strepsirrhine lumbar vertebral bodies and spinous processes. J Hum Evol. 2002; 42(6): 753–783.
  45. Shoshani J, McKenna MC. Higher taxonomic relationships among extant mammals based on morphology, with selected comparisons of results from molecular data. Mol Phylogenet Evol. 1998; 9(3): 572–584.
  46. Simmons NB. Bat relationship and origin of flight. Symp Zool Soc Lond. 1995; 67: 27–43.
  47. Simmons N, Quinn T. Evolution of the digital tendon locking mechanism in bats and dermopterans: A phylogenetic perspective. J Mammal Evol. 1994; 2(4): 231–254.
  48. Slijper EJ. Comparative biologic-anatomical investigations on the vertebral column and spinal musculature of mammals. Verh K Ned Akad Wet Tweede Sectie. 1946; 42: 1–128.
  49. Stafford B, Jr. RT, Kawamichi T. Gliding behavior of japanese giant flying squirrels (Petaurista leucogenys). J Mammal. 2002; 83(2): 553–562, doi: 10.1644/1545-1542(2002)083<0553:gbojgf>2.0.co;2.
  50. Stirling EL. Description of a new genus and species of Marsupialia, ‘Notoryctes typhlops’. Trans Roy Soc S Australia. 1891; 14: 154–187.
  51. Szalay FS, Lucas SG. ranioskeletal morphology of archontans, and diagnoses of Chiroptera, Vilitantia, and Archonta. In: MacPhee RDE (ed.). Primates and their relatives in phylogenyetic perspective, Advances in Primatology Series. Plenum Press, New York 1993: 187–226.
  52. Szalay FS, Lucas SG. Postcranial morphology of Paleocene Chriacus and Mixodectes and the phylogenetic relationships of archontan mammals. New Mexico Bulletin of Natural History and Science. 1996; 7: 1–47.
  53. Thorington RW, Darrow K, Anderson CG. Wing Tip Anatomy and Aerodynamics in Flying Squirrels. J Mammal. 1998; 79(1): 245–250.
  54. Thorington RW, Heaney LR. Body Proportions and Gliding Adaptations of Flying Squirrels (Petauristinae). J Mammal. 1981; 62(1): 101–114.
  55. Thorington R, Santana E. How to make a flying squirrel:glaucomysanatomy in phylogenetic perspective. J Mammal. 2007; 88(4): 882–896.
  56. Varela-Lasheras I, Bakker AJ, van der Mije SD, et al. Breaking evolutionary and pleiotropic constraints in mammals: On sloths, manatees and homeotic mutations. Evodevo. 2011; 2: 11.
  57. Vaughan TA. The skeletal system. In: Wimsatt WA (ed.). Biology of Bats vol. 1. Chapter 3. Academic Press, New York 1970: 97–138.
  58. Verma K. Notes on the biology and anatomy of the indian tree-shrew, anathana wroughtoni. Mammalia. 1965; 29(3): 289–330.
  59. Viglino M, Flores DA, Ercoli MD, et al. Patterns of morphological variation of the vertebral column in dolphins. J Zool. 2014; 294(4): 267–277.
  60. Ward C. Torso morphology and locomotion inProconsul nyanzae. Am J Phys Anthropol. 1993; 92(3): 291–328.
  61. Wible JR, Novacek MJ. Cranial evidence for the monophyletic origin of bats. Am Mus Novitates. 1988; 2911: 1–19.
  62. Williams S. Variation in anthropoid vertebral formulae: implications for homology and homoplasy in hominoid evolution. J Exp Zool. 2011: 134–147.
  63. Wood Jones F. The mammals of South Australia. Govt Printer, Adelaide 1923.

Important: This website uses cookies. More >>

The cookies allow us to identify your computer and find out details about your last visit. They remembering whether you've visited the site before, so that you remain logged in - or to help us work out how many new website visitors we get each month. Most internet browsers accept cookies automatically, but you can change the settings of your browser to erase cookies or prevent automatic acceptance if you prefer.

By  "Via Medica sp. z o.o." sp.k., Świętokrzyska 73, 80–180 Gdańsk, Poland

tel.:+48 58 320 94 94, faks:+48 58 320 94 60, e-mail:  viamedica@viamedica.pl