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Increased variation in numbers of presacral vertebrae in suspensory mammals

Nature Ecology & Evolution volume 3, pages 949–956 (2019)Cite this article

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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.

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Data availability

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

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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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Authors and Affiliations

  1. Center for the Study of Human Origins, Department of Anthropology, New York University, New York, NY, USA

    Scott A. Williams & Jeffrey K. Spear

  2. New York Consortium in Evolutionary Primatology, New York, NY, USA

    Scott A. Williams & Jeffrey K. Spear

  3. Interdepartmental Doctoral Program in Anthropological Sciences, Stony Brook University, Stony Brook, NY, USA

    Lauren Petrullo

  4. Center for Functional Anatomy and Evolution, Johns Hopkins University School of Medicine, Baltimore, MD, USA

    Deanna M. Goldstein

  5. Department of Anthropology, University of Illinois at Urbana-Champaign, Urbana, IL, USA

    Amanda B. Lee

  6. Institute of Human Origins, School of Human Evolution and Social Change, Arizona State University, Tempe, AZ, USA

    Amy L. Peterson

  7. Department of Anthropology, New York University, New York, NY, USA

    Danielle A. Miano

  8. Department of Ecology and Evolutionary Biology, Brown University, Providence, RI, USA

    Elska B. Kaczmarek

  9. Human Biology Program and Department of Anthropology, Hunter College, City University of New York, New York, NY, USA

    Milena R. Shattuck

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Contributions

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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The authors declare no competing interests.

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Supplementary information

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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