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Increased variation in numbers of presacral vertebrae in suspensory mammals

Abstract

Restricted variation in numbers of presacral vertebrae in mammals is a classic example of evolutionary stasis. Cervical number is nearly invariable in most mammals, and numbers of thoracolumbar vertebrae are also highly conserved. A recent hypothesis posits that stasis in mammalian presacral count is due to stabilizing selection against the production of incomplete homeotic transformations at the lumbo-sacral border in fast-running mammals, while slower, ambulatory mammals more readily tolerate intermediate lumbar/sacral vertebrae. We test hypotheses of variation in presacral numbers of vertebrae based on running speed, positional behaviour and vertebral contribution to locomotion. We find support for the hypothesis that selection against changes in presacral vertebral number led to stasis in mammals that rely on dorsomobility of the spine during running and leaping, but our results are independent of running speed per se. Instead, we find that mammals adapted to dorsostability of the spine, such as those that engage in suspensory behaviour, demonstrate elevated variation in numbers of presacral vertebrae compared to dorsomobile mammals. We suggest that the evolution of dorsostability and reduced reliance on flexion and extension of the spine allowed for increased variation in numbers of presacral vertebrae, leading to departures from an otherwise stable evolutionary pattern.

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Fig. 1: Examples of intermediate lumbar/sacral vertebrae.
Fig. 2: The last three lumbar vertebrae and sacrum in two fast-running mammals.
Fig. 3: Ancestral state reconstruction of presacral vertebral numbers.

Data availability

The data analyzed in this study and related data are included in Supplementary Tables 1–3.

References

  1. 1.

    Williams, G. C. Natural Selection: Domains, Levels, and Challenges (Oxford University Press, 1992).

  2. 2.

    Hansen, T. F. & Houle, D. in Phenotypic Integration: Studying the Ecology and Evolution of Complex Phenotypes (eds Pigliucci, M. & Preston, K.) 130–150 (Oxford University Press, 2004).

  3. 3.

    Müller, J. et al. Homeotic effects, somitogenesis and the evolution of vertebral numbers in recent and fossil amniotes. Proc. Natl Acad. Sci. USA 107, 2118–2123 (2010).

    PubMed  Google Scholar 

  4. 4.

    Chen, M. & Luo, Z.-X. Postcranial skeleton of the Cretaceous mammal Akidolestes cifellii and its locomotor adaptations. J. Mamm. Evol. 20, 159–189 (2013).

    Google Scholar 

  5. 5.

    Bi, S., Wang, Y., Guan, J., Sheng, X. & Meng, J. Three new Jurassic euharamiyidan species reinforce early divergence of mammals. Nature 514, 579–584 (2014).

    CAS  PubMed  Google Scholar 

  6. 6.

    Jones, K. E. et al. Fossils reveal the complex evolutionary history of the mammalian regionalized spine. Science 361, 1249–1252 (2018).

    CAS  PubMed  Google Scholar 

  7. 7.

    Galis, F. Why do almost all mammals have seven cervical vertebrae? Developmental constraints, Hox genes, and cancer. J. Exp. Zool. 285, 19–26 (1999).

    CAS  PubMed  Google Scholar 

  8. 8.

    Narita, Y. & Kuratani, S. Evolution of the vertebral formulae in mammals: a perspective on developmental constraints. J. Exp. Zool. 304B, 91–106 (2005).

    Google Scholar 

  9. 9.

    Asher, R. J., Bennett, N. & Lehmann, T. The new framework for understanding placental mammal evolution. Bioessays 31, 853–864 (2009).

    CAS  PubMed  Google Scholar 

  10. 10.

    Baumel, J. J. & Witmer, L. M. in Handbook of Avian Anatomy: Nomina Anatomica Avium (eds Baumel, J. J. et al.) 45–132 (Nuttall Ornithologica Club, 1993).

  11. 11.

    Todd, T. W. Numerical significance in the thoracicolumbar vertebrae of the Mammalia. Anat. Rec. 24, 261–286 (1922).

    Google Scholar 

  12. 12.

    Sánchez-Villagra, M. R., Narita, Y. & Kuratani, S. Thorcolumbar vertebral number: the first skeletal synapomorphy for afrotherian mammals. Syst. Biodivers. 5, 1–7 (2007).

    Google Scholar 

  13. 13.

    Asher, R. J., Lin, K. H., Kardjilov, N. & Hautier, L. Variability and constraint in the mammalian vertebral column. J. Evol. Biol. 24, 1080–1090 (2011).

    CAS  PubMed  Google Scholar 

  14. 14.

    Buchholtz, E. A. Crossing the frontier: a hypothesis for the origins of meristic constraint in mammalian axial patterning. Zoology 117, 64–69 (2014).

    PubMed  Google Scholar 

  15. 15.

    Buchholtz, E. A. in From Clone to Bone: The Synergy of Morphological and Molecular Tools in Paleobiology (eds Asher, R. J. & Müller, J.) 230–253 (Cambridge Univ. Press, 2012).

  16. 16.

    Burke, A. C., Nelson, C. E., Morgan, B. A. & Tabin, C. Hox genes and the evolution of vertebrate axial morphology. Development 121, 333–346 (1995).

    CAS  PubMed  Google Scholar 

  17. 17.

    Wellik, D. M. Hox patterning of the vertebrate axial skeleton. Dev. Dyn. 236, 2454–2463 (2007).

    CAS  PubMed  Google Scholar 

  18. 18.

    Pilbeam, D. The anthropoid postcranial axial skeleton: comments on development, variation, and evolution. J. Exp. Zool. 302, 241–267 (2004).

    Google Scholar 

  19. 19.

    Williams, S. A. Evolution of the Hominoid Vertebral Column. PhD thesis, Univ. of Illinois (2011).

  20. 20.

    Williams, S. A. Variation in anthropoid vertebral formulae: implications for homology and homoplasy in hominoid evolution. J. Exp. Zool. 318B, 134–147 (2012).

    Google Scholar 

  21. 21.

    Bots, J. et al. Analysis of cervical ribs in a series of human fetuses. J. Anat. 219, 403–409 (2011).

    PubMed  PubMed Central  Google Scholar 

  22. 22.

    Buchholtz, E. A. et al. Fixed cervical count and the origin of the mammalian diaphragm. Evol. Dev. 14, 399–411 (2012).

    PubMed  Google Scholar 

  23. 23.

    Varela-Lasheras, I. et al. Breaking evolutionary and pleiotropic constraints in mammals: on sloths, manatees and homeotic mutations. EvoDevo 2, 11 (2011).

    PubMed  PubMed Central  Google Scholar 

  24. 24.

    Galis, F. et al. Extreme selection in humans against homeotic transformations of cervical vertebare. Evolution 60, 2643–2654 (2006).

    PubMed  Google Scholar 

  25. 25.

    ten Broek, C. M. A. et al. Evo-devo of the human vertebral column: on homeotic transformations, pathologies and prenatal selection. Evol. Biol. 39, 456–471 (2012).

    PubMed  PubMed Central  Google Scholar 

  26. 26.

    Hirasawa, T. & Kuratani, S. A new scenario of the evolutionary derivation of the mammalian diaphragm from shoulder muscles. J. Anat. 222, 504–517 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Bramble, D. M. & Carrier, D. R. Running and breathing in mammals. Science 219, 251–256 (1983).

    CAS  PubMed  Google Scholar 

  28. 28.

    Carrier, D. R. The evolution of locomotor stamina in tetrapods: circumventing a mechanical constraint. Paleobiology 13, 326–341 (1987).

    Google Scholar 

  29. 29.

    Bramble, D. M. Axial-appendicular dynamics and the integration of breathing and gait in mammals. Am. Zool. 29, 171–186 (1989).

    Google Scholar 

  30. 30.

    Perry, S. F., Similowski, T., Klein, W. & Codd, J. R. The evolutionary origin of the mammalian diaphragm. Respir. Physiol. Neurobiol. 171, 1–16 (2010).

    PubMed  Google Scholar 

  31. 31.

    Ruben, J. A., Bennett, A. F. & Hisaw, F. L. Selective factors in the origin of the mammalian diaphragm. Paleobiology 13, 54–59 (1987).

    Google Scholar 

  32. 32.

    Marechal, G., Goffart, M., Reznik, M. & Gerebtzoff, M. A. The striated muscles in a slow-mover, Perodicticus potto (Prosimii, Lorisidae, Lorisinae). Comp. Biochem. Physiol. 54A, 81–93 (1976).

    Google Scholar 

  33. 33.

    Rommel, S. & Reynolds, J. E. Diaphragm structure and function in the Florida manatee (Trichechus manatus latirostris). Anat. Rec. 259, 41–51 (2000).

    CAS  PubMed  Google Scholar 

  34. 34.

    Galis, F. et al. Fast running restricts evolutionary change of the vertebral column in mammals. Proc. Natl Acad. Sci. USA 111, 11401–11406 (2014).

    CAS  PubMed  Google Scholar 

  35. 35.

    Rockwell, H., Evans, F. G. & Pheasant, H. C. The comparative morphology of the vertebrate spinal column. Its form as related to function. Relat. Funct. J. Morphol. 63, 87–117 (1938).

    Google Scholar 

  36. 36.

    Slijper, E. J. Comparative biologic-anatomical investigations on the vertebral column and spinal musculature of mammals. Verh. Kon. Ned. Akad. Wet. 42, 1–128 (1946).

    Google Scholar 

  37. 37.

    Schultz, A. H. Vertebral column and thorax. Primatologia 4, 1–66 (1961).

    Google Scholar 

  38. 38.

    Shapiro, L. in Postcranial Adaptation in Nonhuman Primates (ed. Gebo, D. L.) 121–149 (Northern Illinois Univ. Press, 1993).

  39. 39.

    Boszczyk, B. M., Boszczyk, A. A. & Putz, R. Comparative and functional anatomy of the mammalian lumbar spine. Anat. Rec. 264, 157–168 (2001).

    CAS  PubMed  Google Scholar 

  40. 40.

    Argot, C. Functional-adaptive anatomy of the axial skeleton of some extant marsupials and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus. J. Morphol. 255, 279–300 (2003).

    PubMed  Google Scholar 

  41. 41.

    Chen, X., Milne, N. & O’Higgins, P. Morphological variation of the thoracolumbar vertebrae in Macropodidae and its functional relevance. J. Morphol. 266, 167–181 (2005).

    PubMed  Google Scholar 

  42. 42.

    Nalley, T. K. & Grider-Potter, N. Functional analyses of the primate upper cervical vertebral column. J. Hum. Evol. 107, 19–35 (2017).

    PubMed  Google Scholar 

  43. 43.

    Shapiro, L. J. & Kemp, A. D. Functional and developmental influences on intraspecific variation in catarrhine vertebrae. Am. J. Phys. Anthropol. 168, 131–144 (2019).

    PubMed  Google Scholar 

  44. 44.

    Buchholtz, E. A. Vertebral osteology and swimming style in living and fossil whales (Order: Cetacea). J. Zool. (Lond.) 253, 175–190 (2001).

    Google Scholar 

  45. 45.

    Pierce, S. E., Clack, J. A. & Hutchinson, J. R. Comparative axial morphology in pinnipeds and its correlation with aquatic locomotory behaviour. J. Anat. 219, 502–514 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Jones, K. E. Allometry of the Thoracolumbar Region in Running Mammals. PhD thesis, Johns Hopkins Univ. (2014).

  47. 47.

    Jones, K. E., Benitez, L., Angielczyk, K. D. & Pierce, S. E. Adaptation and constraint in the evolution of the mammalian backbone. BMC Evol. Biol. 18, 172 (2018).

    PubMed  PubMed Central  Google Scholar 

  48. 48.

    Smith, J. M. & Savage, R. J. G. Some locomotory adaptations in mammals. Zool. J. Linn. Soc. 42, 603–622 (1955).

    Google Scholar 

  49. 49.

    Hildebrand, M. Motions of the running cheetah and horse. J. Mammal. 40, 481–495 (1959).

    Google Scholar 

  50. 50.

    Gambaryan, P. P. How Mammals Run (John Wiley and Sons, 1974).

  51. 51.

    Hurov, J. R. Terrestrial locomotion and back anatomy in vervets (Cercopithecus aethiops) and patas monkeys (Erythrocebus patas). Am. J. Primatol. 13, 297–311 (1987).

    Google Scholar 

  52. 52.

    Schilling, N. & Hackert, R. Sagittal spine movements of small therian mammals during asymmetrical gaits. J. Exp. Biol. 209, 3925–3939 (2006).

    PubMed  Google Scholar 

  53. 53.

    Ripley, S. The leaping of langurs: a problem in the study of locomotor adaptation. Am. J. Phys. Anthropol. 26, 149–170 (1967).

    Google Scholar 

  54. 54.

    Ward, C. V. Torso morphology and locomotion in Proconsul nyanzae. Am. J. Phys. Anthropol. 92, 291–328 (1993).

    CAS  PubMed  Google Scholar 

  55. 55.

    Jungers, W. L. in The Lesser Apes: Evolutionary and Behavioral Biology (eds. Preuschoft, H. et al.) 146–169 (Edinburgh Univ. Press, 1984).

  56. 56.

    Halpert, A. P., Jenkins, F. A. & Franks, H. Structure and scaling of the lumbar vertebrae in African bovids (Mammalia: Artiodactyla). J. Zool. (Lond.) 211, 239–258 (1987).

    Google Scholar 

  57. 57.

    Gaudin, T. J. & Biewener, A. A. The functional morphology of xenarthrous vertebrae in the armadillo Dasypus novemcinctus (Mammalia, Xenarthra). J. Morphol. 214, 63–81 (1992).

    CAS  PubMed  Google Scholar 

  58. 58.

    Filler, A. G. Homeotic evolution in the Mammalia: diversification of therian axial seriation and the morphogenetic basis of human origins. PLoS ONE 10, e1019 (2007).

    Google Scholar 

  59. 59.

    Lovejoy, C. O. & McCollum, M. A. Spinopelvic pathways to bipedality: why no hominids ever relied on a bent-hip-bent-knee gait. Philos. Trans. R. Soc. B 365, 3289–3299 (2010).

    Google Scholar 

  60. 60.

    Williams, S. A. Placement of the diaphragmatic vertebra in catarrhines: implications for the evolution of dorsostability in hominois and bipedalism in hominins. Am. J. Phys. Anthropol. 148, 111–122 (2012).

    PubMed  Google Scholar 

  61. 61.

    Jones, K. E. Evolutionary allometry of lumbar shape in Felidae and Bovidae. Biol. J. Linn. Soc. Lond. 116, 721–740 (2015).

    Google Scholar 

  62. 62.

    Jones, K. E. New insights on equid locomotor evolution from the lumbar region of fossil horses. Proc. R. Soc. B 283, 20152947 (2016).

    PubMed  Google Scholar 

  63. 63.

    Russo, G. A. & Williams, S. A. Giant pandas (Carnivora: Ailuropoda melanoleuca) and living hominoids converge on lumbar vertebral adaptations to orthograde trunk posture. J. Hum. Evol. 88, 160–179 (2015).

    PubMed  Google Scholar 

  64. 64.

    Williams, S. A. & Russo, G. A. Evolution of the hominoid vertebral column: the long and the short of it. Evol. Anthropol. 24, 15–32 (2015).

    PubMed  Google Scholar 

  65. 65.

    Machnicki, A. L., Spurlock, L. B., Strier, K. B., Reno, P. L. & Lovejoy, C. O. First steps of bipedality in hominids: evidence from the atelid and proconsulid pelvis. PeerJ 4, e1521 (2016).

    PubMed  PubMed Central  Google Scholar 

  66. 66.

    Haussler, K. K., Bertram, J. E. A., Gellman, K. & Hermanson, J. W. Segmental in vivo vertebral kinematics at the walk, trot and canter: a preliminary study. Equine Vet. J. 33, 160–164 (2001).

    Google Scholar 

  67. 67.

    Johnson, S. E. & Shapiro, L. J. Positional behavior and vertebral morphology in atelines and cebines. Am. J. Phys. Anthropol. 105, 333–354 (1998).

    CAS  PubMed  Google Scholar 

  68. 68.

    Shapiro, L. Functional morphology of indrid lumbar vertebrae. Am. J. Phys. Anthropol. 98, 323–342 (1995).

    CAS  PubMed  Google Scholar 

  69. 69.

    Shapiro, L. J., Demes, B. & Cooper, J. Lateral bending of the lumbar spine during quadrupedalism in strepsirhines. J. Hum. Evol. 40, 231–259 (2001).

    CAS  PubMed  Google Scholar 

  70. 70.

    Shapiro, L. J. et al. Morphometric analysis of lumbar vertebrae in extinct Malagasy strepsirrhines. Am. J. Phys. Anthropol. 128, 823–839 (2005).

    PubMed  Google Scholar 

  71. 71.

    Shapiro, L. J. & Simons, C. V. M. Functional aspects of strepsirrhine lumbar vertebral bodies and spinous processes. J. Hum. Evol. 42, 753–783 (2002).

    PubMed  Google Scholar 

  72. 72.

    Lovejoy, C. O. The natural history of human gait and posture Part 1. Spine and pelvis. Gait Posture 21, 95–112 (2005).

    PubMed  Google Scholar 

  73. 73.

    Cartmill, M. & Milton, K. The lorisiform wrist joint and the evolution of “brachiating” adaptations in the Hominoidea. Am. J. Phys. Anthropol. 47, 249–272 (1977).

    CAS  PubMed  Google Scholar 

  74. 74.

    Granatosky, M. C., Lemelin, P., Chester, S. G. B., Pampush, J. D. & Schmitt, D. Functional and evolutionary aspects of axial stability in euarchontans and other mammals. J. Morphol. 275, 313–327 (2014).

    PubMed  Google Scholar 

  75. 75.

    Granatosky, M. C., Miller, C. E., Boyer, D. M. & Schmitt, D. Lumbar vertebral morphology of flying, gliding, and suspensory mammals: implications for the locomotor behavior of the subfossil lemurs Palaeopropithecus and Babakotia. J. Hum. Evol. 75, 40–52 (2014).

    PubMed  Google Scholar 

  76. 76.

    Gebo, D. L. Locomotor diversity in prosimian primates. Am. J. Primatol. 13, 271–281 (1987).

    Google Scholar 

  77. 77.

    Keith, A. The extent to which the posterior segments of the body have been transmuted and suppressed in the evolution of man and allied primates. J. Anat. Physiol. 37, 18–40 (1902).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. 78.

    Abitbol, M. M. Evolution of the sacrum in hominoids. Am. J. Phys. Anthropol. 74, 65–81 (1987).

    CAS  PubMed  Google Scholar 

  79. 79.

    Buchholtz, E. A. & Stepien, C. C. Anatomical transformation in mammals: developmental origin of aberrant cervical anatomy in tree sloths. Evol. Dev. 11, 69–79 (2009).

    PubMed  Google Scholar 

  80. 80.

    Buchholtz, E. A., Booth, A. C. & Webbink, K. E. Vertebral anatomy in the Florida manatee, Trichechus manatus latirostris: a developmental and evolutionary analysis. Anat. Rec. 290, 624–637 (2007).

    Google Scholar 

  81. 81.

    Buchholtz, E. A., Wayrynen, K. L. & Lin, I. W. Breaking constraint: axial patterning in Trichechus (Mammalia: Siernia). Evol. Dev. 16, 382–393 (2014).

    PubMed  Google Scholar 

  82. 82.

    Oliver, J. D., Jones, K. E., Hautier, L., Loughry, W. J. & Pierce, S. E. Vertebral bending mechanics and xenarthrous morphology in the nin-banded armadillo (Dasypus novemcinctus). J. Exp. Biol. 219, 2991–3002 (2016).

    PubMed  Google Scholar 

  83. 83.

    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. Mamm. Evol. 25, 565–572 (2018).

    Google Scholar 

  84. 84.

    Cullinane, D. M. & Aleper, D. The functional and biomechanical modifications of the spine of Scutisorex somereni, the hero shrew: spinal musculature. J. Zool. (Lond.) 244, 453–458 (1998).

    Google Scholar 

  85. 85.

    Cullinane, D. M., Aleper, D. & Bertram, J. E. A. The functional and biomechanical modifications of the spine of Scutisorex somereni, the hero shrew: skeletal scaling relationships. J. Zool. (Lond.) 244, 447–452 (1998).

    Google Scholar 

  86. 86.

    Cullinane, D. M. & Bertram, J. E. A. The mechanical behaviour of a novel mammalian intervertebral joint. J. Anat. 197, 627–634 (2000).

    PubMed  PubMed Central  Google Scholar 

  87. 87.

    Stanley, W. T. et al. A new hero emerges: another exceptional mammalian spine and its potential adaptive significance. Biol. Lett. 9, 20130486 (2013).

    PubMed  PubMed Central  Google Scholar 

  88. 88.

    Buchholtz, E. A. & Schur, S. A. Vertebral osteology in Delphinidae (Cetacea). Zool. J. Linn. Soc. 140, 383–401 (2004).

    Google Scholar 

  89. 89.

    Gaudioso, P. J., Diaz, M. M. & Barquez, R. M. Morphology of the axial skeleton of seven bat genera (Chiroptera: Phyllostomidae). An. Acad. Bras. Cienc. 89, 2341–2358 (2017).

    PubMed  Google Scholar 

  90. 90.

    Reumer, J. W. F., ten Broek, C. M. A. & Galis, F. Extraordinary incidence of cervical ribs indicates vulnerable condition in Late Pleistocene mammoths. PeerJ 2, e318 (2014).

    PubMed  PubMed Central  Google Scholar 

  91. 91.

    Buchholtz, E. A. Modular evolution of the cetacean vertebral column. Evol. Dev. 9, 278–289 (2007).

    CAS  PubMed  Google Scholar 

  92. 92.

    Hautier, L., Weisbecker, V., Sánchez-Villagra, M. R., Goswami, A. & Asher, R. J. Skeletal development in sloths and the evolution of mammalian vertebral patterning. Proc. Natl Acad. Sci. USA 107, 18903–18908 (2010).

    CAS  PubMed  Google Scholar 

  93. 93.

    Washburn, S. L. in Classification and Human Evolution (ed. Washburn, S. L.) 190–203 (Aldine, 1963).

  94. 94.

    Russo, G. A. Prezygapophyseal articular facet shape in the catarrhine thoracolumbar vertebral column. Am. J. Phys. Anthropol. 142, 600–612 (2010).

    PubMed  Google Scholar 

  95. 95.

    Williams, S. A. et al. The vertebral column of Australopithecus sediba. Science 340, 1232996 (2013).

    PubMed  Google Scholar 

  96. 96.

    Williams, S. A., Middleton, E. R., Villamil, C. I. & Shattuck, M. R. Vertebral numbers and human evolution. Yearb. Phys. Anthropol. 159, S19–S36 (2016).

    Google Scholar 

  97. 97.

    Buchholtz, E. A. Vertebral and rib anatomy in Caperea marginata: implications for evolutionary patterning of the mammalian vertebral column. Mar. Mamm. Sci. 27, 382–397 (2011).

    Google Scholar 

  98. 98.

    Mikawa, S. et al. Fine mapping of a swine quantitative trait locus for number of vertebrae and analysis of an orphan nuclear receptor, germ cell nuclear factor (NR6A1/GCNF). Genome Res. 14, 1–8 (2007).

    Google Scholar 

  99. 99.

    Agresti, A. & Agresti, B. F. Statistical analysis of qualitative variation. Soc. Method 9, 204–237 (1978).

    Google Scholar 

  100. 100.

    Christiansen, P. Locomotion in terrestrial mammals: the influence of body mass, limb length and bone proportions on speed. Zool. J. Linn. Soc. 136, 685–714 (2002).

    Google Scholar 

  101. 101.

    Iriarte-Díaz, J. Differential scaling of locomotor performance in small and large terrestrial mammals. J. Exp. Biol. 205, 2897–2908 (2002).

    PubMed  Google Scholar 

  102. 102.

    Lovegrove, B. G. & Mowoe, M. O. The evolution of micro-cursoriality in mammals. J. Exp. Biol. 217, 1316–1325 (2014).

    PubMed  Google Scholar 

  103. 103.

    Bininda-Emonds, O. R. P. et al. The delayed rise of present-day mammals. Nature 446, 507–512 (2007).

    CAS  PubMed  Google Scholar 

  104. 104.

    Garland, T., Dickerman, A. W., Janis, C. M. & Jones, J. A. Phylogenetic analysis of covariance by computer simluation. Syst. Biol. 43, 265–292 (1993).

    Google Scholar 

  105. 105.

    Nowak, R. M. Walker’s Mammals of the World 5th edn (Johns Hopkins Univ. Press, 1991).

  106. 106.

    Hildebrand, M. & Goslow, G. Analysis of Vertebrate Structure 5th edn (Wiley, 2001).

  107. 107.

    Hutchins, M. Grzimek’s Animal Life Encyclopedia (Gale, 2003).

  108. 108.

    Rowe, N.& Myers, M. All the World’s Primates (Pongonias Press, 2016).

  109. 109.

    Cant, J. G. H. Locomotion and feeding postures of spider and howling monkeys: field study and evolutionary interpretation. Folia Primatol. 46, 1–14 (1986).

    CAS  PubMed  Google Scholar 

  110. 110.

    Stern, J. T. Before bipedality. Yearb. Phys. Anthropol. 19, 59–68 (1975).

    Google Scholar 

  111. 111.

    Keith, A. The Construction of Man’s Family Tree (Watts and Co., 1934).

  112. 112.

    Granatosky, M. C. & Schmitt, D. Forelimb and hind limb loading patterns during below branch quadrupedal locomotion in the two-toed sloth. J. Zool. 302, 271–278 (2017).

    Google Scholar 

  113. 113.

    Nyakatura, J. A. The convergent evolution of suspensory posture and locomotion in tree sloths. J. Mamm. Evol. 19, 225–234 (2012).

    Google Scholar 

  114. 114.

    Grand, T. I. & Barboza, P. S. Anatomy and development of the koala, Phascolarctos cinereus: an evolutionary perspective on the superfamily Vombatoidea. Anat. Embryol. (Berl.) 2001, 211–223 (2001).

    Google Scholar 

  115. 115.

    Spoor, C. F. & Badoux, D. M. Descriptive and functional mylolgy of the back and hindlimb of the striped hyena (Hyaena hyaena, L. 1758). Ann. Anat. 167, 313–321 (1988).

    CAS  Google Scholar 

  116. 116.

    Davis, D. D. The giant panda: a morpholocial study of evolutionary mechanisms. FieldianaZool. Mem. 3, 1–339 (1964).

    Google Scholar 

  117. 117.

    Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).

    Google Scholar 

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Acknowledgements

We thank E. Buchholtz and D. Pilbeam for generously sharing data; F. Galis for providing species information from her and her colleagues’ study; M. Grabowski for statistical advice; and N. Duncan, G. Garcia, E. Hoeger, S. Ketelsen, A. Marcato, B. O’Toole, M. Surovy, E. Westwig (American Museum of Natural History), M. Milella, M. Ponce de León, C. Zollikofer (Anthropological Institute and Museum, University of Zurich), Y. Haile-Selassie, L. Jellema (Cleveland Museum of Natural History), H. Taboada (Department of Anthropology, New York University), D. Katz, T. Weaver (Department of Anthropology, University of California, Davis), B. Patterson, A. Goldman, M. Schulenberg, L. Smith, W. Stanley (Field Museum of Natural History), C. McCaffery, D. Reed (Florida Museum of Natural History, University of Florida), J. Chupasko, J. Harrison, M. Omura (Harvard Museum of Comparative Zoology), E. Gilissen, W. Wendelen (Musée Royal de l’Afrique Centrale), S. Jancke, N. Lange, F. Mayer (Musée für Naturkunde, Berlin), C. Conroy (Museum of Vertebrate Zoology, University of California, Berkeley), L. Gordon, K. Helgen, E. Langan, D. Lunde, J. Ososky, R. Thorington (National Museum of Natural History, Smithsonian Institution), J. Soderberg, M. Tappen (Neil C. Tappen Collection, Universtity of Minnesota), S. Bruaux, G. Lenglet (Royal Belgian Institute of Natural Sciences) and M. Hiermeier (Zoologische Staatssammlung München) for facilitating access to specimens in their care. S.A.W. was funded through the National Science Foundation (No. BCS-0925734), the Leakey Foundation (No. 33517) and the New York University Research Challenge Fund.

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S.A.W., J.K.S. and M.R.S. conceived and designed the study. S.A.W., J.K.S., A.B.L. and M.R.S. analysed the data. S.A.W., J.K.S., L.P. and M.R.S. wrote the manuscript. All authors collected data, edited the manuscript and gave final approval for publication.

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Correspondence to Scott A. Williams.

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Supplementary Tables 1–3

Taxa, morphological heterogeneity indices, sample sizes, vertebral number data and categories for phylogenetic ANOVA analyses; Raw data used in PGLS analyses; Results of PGLS analyses

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Williams, S.A., Spear, J.K., Petrullo, L. et al. Increased variation in numbers of presacral vertebrae in suspensory mammals. Nat Ecol Evol 3, 949–956 (2019). https://doi.org/10.1038/s41559-019-0894-2

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