The evolution of semi-independent modules is hypothesized to underlie the functional diversification of serially repeating (metameric) structures. The mammal vertebral column is a classic example of a metameric structure that is both modular, with well-defined morphological regions, and functionally differentiated. How the evolution of regions is related to their functional differentiation in the forerunners of mammals remains unclear. Here we gathered morphometric and biomechanical data on the presacral vertebrae of two extant species that bracket the synapsid–mammal transition and use the relationship between form and function to predict functional differentiation in extinct non-mammalian synapsids. The origin of vertebral functional diversity does not correlate with the evolution of new regions but appears late in synapsid evolution. This decoupling of regions from functional diversity implies that an adaptive trigger is needed to exploit existing modularity. We propose that the release of axial respiratory constraints, combined with selection for novel mammalian behaviours in Late Triassic cynodonts, drove the functional divergence of pre-existing morphological regions.
This is a preview of subscription content
Subscribe to Nature+
Get immediate online access to the entire Nature family of 50+ journals
Subscribe to Journal
Get full journal access for 1 year
only $9.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Raw data are available through Harvard Dataverse: https://doi.org/10.7910/DVN/YMUHLU.
Code required for calculating functional distributions is provided in the supplementary materials.
Raff, R. A. The Shape of Life: Genes, Development, and the Evolution of Animal Form (Univ. Chicago Press, 2012).
Cheverud, J. M. Quantitative genetics and developmental constraints on evolution by selection. J. Theor. Biol. 110, 155–171 (1984).
Asher, R., Lin, K., Kardjilov, N. & Hautier, L. Variability and constraint in the mammalian vertebral column. J. Evol. Biol. 24, 1080–1090 (2011).
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).
Hughes, N. C. Trilobite body patterning and the evolution of arthropod tagmosis. Bioessays 25, 386–395 (2003).
Carroll, S. B. Chance and necessity: the evolution of morphological complexity and diversity. Nature 409, 1102–1109 (2001).
Shubin, N., Tabin, C. & Carroll, S. Fossils, genes and the evolution of animal limbs. Nature 388, 639–648 (1997).
Buchholtz, E. A. in From Clone to Bone: The Synergy of Morphological and Molecular Tools in Palaeobiology (eds Asher, R. J. & Müller, J.) 230–256 (Cambridge Univ. Press, 2012).
Young, N. M. & Hallgrimsson, B. Serial homology and the evolution of mammalian limb covariation structure. Evolution 59, 2691–2704 (2005).
Hall, B. K. in Evolutionary Biology Vol. 28 (eds Hecht, M. K. et al.) 1–37 (Springer, 1995).
Wagner, G. P. & Altenberg, L. Complex adaptations and the evolution of evolvability. Evolution 50, 967–976 (1996).
Wainwright, P. C. Functional versus morphological diversity in macroevolution. Annu. Rev. Ecol. Evol. Syst. 38, 381–401 (2007).
Wainwright, P. C., Alfaro, M. E., Bolnick, D. I. & Hulsey, C. D. Many-to-one mapping of form to function: a general principle in organismal design? Integr. Comp. Biol. 45, 256–262 (2005).
Randau, M., Cuff, A. R., Hutchinson, J. R., Pierce, S. E. & Goswami, A. Regional differentiation of felid vertebral column evolution: a study of 3D shape trajectories. Org. Divers. Evol. 17, 305–319 (2017).
Evans, K. M., Waltz, B. T., Tagliacollo, V. A., Sidlauskas, B. L. & Albert, J. S. Fluctuations in evolutionary integration allow for big brains and disparate faces. Sci. Rep. 7, 40431 (2017).
Solounias, N. The remarkable anatomy of the giraffe’s neck. J. Zool. 247, 257–268 (1999).
Schmitt, D., Rose, M. D., Turnquist, J. E. & Lemelin, P. Role of the prehensile tail during ateline locomotion: experimental and osteological evidence. Am. J. Phys. Anthropol. 126, 435–446 (2005).
Kemp, T. S. The Origin and Evolution of Mammals (Oxford Univ. Press, 2005).
Carroll, R. L. Vertebrate Paleontology and Evolution (W. H. Freeman and Company, 1988).
Jones, K. E. et al. Fossils reveal the complex evolutionary history of the mammalian regionalized spine. Science 361, 1249–1252 (2018).
Head, J. J. & Polly, P. D. Evolution of the snake body form reveals homoplasy in amniote Hox gene function. Nature 520, 86–89 (2015).
Böhmer, C. Correlation between Hox code and vertebral morphology in the mouse: towards a universal model for Synapsida. Zool. Lett. 3, 8 (2017).
Long, J. H., Pabst, D. A., Shepherd, W. R. & McLellan, W. A. Locomotor design of dolphin vertebral columns: bending mechanics and morphology of Delphinus delphis. J. Exp. Biol. 200, 65–81 (1997).
Oliver, J. D., Jones, K. E., Hautier, L., Loughry, W. J. & Pierce, S. E. Vertebral bending mechanics and xenarthrous morphology in the nine-banded armadillo (Dasypus novemcinctus). J. Exp. Biol. 219, 2991–3002 (2016).
Jeffcott, L. B. & Dalin, G. Natural rigidity of the horse’s backbone. Equine Vet. J. 12, 101–108 (1980).
Gál, J. M. Mammalian spinal biomechanics 1: static and dynamic mechanical-properties of intact intervertebral joints. J. Exp. Biol. 174, 247–280 (1993).
Jenkins, F. A. & Goslow, G. The functional anatomy of the shoulder of the savannah monitor lizard (Varanus exanthematicus). J. Morphol. 175, 195–216 (1983).
Carrier, D. R. The evolution of locomotor stamina in tetrapods: circumventing a mechanical constraint. Paleobiology 13, 326–341 (1987).
Hopson, J. A. in Great Transformations in Vertebrate Evolution (eds Dial, K. P. et al.) 125–141 (Univ. Chicago Press, 2015).
Molnar, J. L., Pierce, S. E. & Hutchinson, J. R. An experimental and morphometric test of the relationship between vertebral morphology and joint stiffness in Nile crocodiles (Crocodylus niloticus). J. Exp. Biol. 217, 758–768 (2014).
Macpherson, J. M. & Ye, Y. The cat vertebral column: stance configuration and range of motion. Exp. Brain Res. 119, 324–332 (1998).
Carrier, D. Activity of the hypaxial muscles during walking in the lizard Iguana iguana. J. Exp. Biol. 152, 453–470 (1990).
Montuelle, S. J., Herrel, A., Libourel, P.-A., Reveret, L. & Bels, V. L. Separating the effects of prey size and speed on the kinematics of prey capture in the omnivorous lizard Gerrhosaurus major. J. Comp. Physiol. A 196, 491–499 (2010).
Mosauer, W. On the locomotion of snakes. Science 76, 583–585 (1932).
Moon, B. R. Testing an inference of function from structure: snake vertebrae do the twist. J. Morphol. 241, 217–225 (1999).
Kemp, T. S. The origin of mammalian endothermy: a paradigm for the evolution of complex biological structure. Zool. J. Linn. Soc. 147, 473–488 (2006).
Schilling, N. & Hackert, R. Sagittal spine movements of small therian mammals during asymmetrical gaits. J. Exp. Biol. 209, 3925–3939 (2006).
Alexander, R. M., Dimery, N. J. & Ker, R. F. Elastic structures in the back and their role in galloping in some mammals. J. Zool. 207, 467–482 (1985).
Jones, K. Preliminary data on the effect of osseous anatomy on ex vivo joint mobility in the equine thoracolumbar region. Equine Vet. J. 48, 502–508 (2015).
Townsend, H. G. G. & Leach, D. H. Relationship between intervertebral joint morphology and mobility in the equine thoracolumbar spine. Equine Vet. J. 16, 461–465 (1984).
Kambic, R. E., Biewener, A. A. & Pierce, S. E. Experimental determination of three-dimensional cervical joint mobility in the avian neck. Front. Zool. 14, 37 (2017).
Karakasiliotis, K., Schilling, N., Cabelguen, J.-M. & Ijspeert, A. J. Where are we in understanding salamander locomotion: biological and robotic perspectives on kinematics. Biol. Cybern. 107, 529–544 (2013).
Frolich, L. M. & Biewener, A. A. Kinematic and electromyographic analysis of the functional role of the body axis during terrestrial and aquatic locomotion in the salamander Ambystoma tigrinum. J. Exp. Biol. 162, 107–130 (1992).
Angielczyk, K. D. & Kammerer, C. F. in Handbook of Zoology: Mammalia: Mammalian Evolution, Diversity, and Systematics (eds Zachos, F. E. & Asher, R. J.) 117–198 (De Gruyter, 2018).
Bennett, S. C. Aerodynamics and thermoregulatory function of the dorsal sail of Edaphosaurus. Paleobiology 22, 496–506 (1996).
Huttenlocker, A. K., Rega, E. & Sumida, S. S. Comparative anatomy and osteohistology of hyperelongate neural spines in the Sphenacodontids Sphenacodon and Dimetrodon (Amniota: Synapsida). J. Morphol. 271, 1407–1421 (2010).
Rega, E. A. et al. Healed fractures in the neural spines of an associated skeleton of Dimetrodon: implications for dorsal sail morphology and function. Fieldiana Life Earth Sci. 5, 104–111 (2012).
Sumida, S. S. Vertebral Morphology, Alternation of Neural Spine Height, and Structure in Permo-Carboniferous Tetrapods, and a Reappraisal of Primitive Modes of Terrestrial Locomotion (Univ. California Press, 1990).
Jones, K. E., Angielczyk, K. D. & Pierce, S. E. Stepwise shifts underlie evolutionary trends in morphological complexity of the mammalian vertebral column. Nat. Commun. 10, 5071 (2019).
Lungmus, J. K. & Angielczyk, K. D. Antiquity of forelimb ecomorphological diversity in the mammalian stem lineage (Synapsida). Proc. Natl Acad. Sci. USA 116, 6903–6907 (2019).
Rubidge, B. S. & Sidor, C. A. Evolutionary patterns among Permo-Triassic therapsids. Annu. Rev. Ecol. Syst. 32, 449–480 (2001).
Erwin, D. H. Novelty and innovation in the history of life. Curr. Biol. 25, R930–R940 (2015).
Erwin, D. H. Early metazoan life: divergence, environment and ecology. Phil. Trans. R. Soc. B 370, 20150036 (2015).
Jablonski, D. Approaches to macroevolution: 1. General concepts and origin of variation. Evol. Biol. 44, 427–450 (2017).
Roberts, S. F. et al. Testing biological hypotheses with embodied robots: adaptations, accidents, and by-products in the evolution of vertebrates. Front. Robot. AI 1, 12 (2014).
Ruben, J., Hillenius, W., Kemp, T., Quick, D. & Chinsamy-Turan, A. in Forerunners of Mammals: Radiation, Histology, Biology (ed. Chinsamy-Turan, A.) 273–286 (Indiana Univ. Press, 2011).
Bennett, A. F. & Ruben, J. A. Endothermy and activity in vertebrates. Science 206, 649–654 (1979).
Buchholtz, E. A. et al. Fixed cervical count and the origin of the mammalian diaphragm. Evol. Dev. 14, 399–411 (2012).
Hirasawa, T. & Kuratani, S. A new scenario of the evolutionary derivation of the mammalian diaphragm from shoulder muscles. J. Anat. 222, 504–517 (2013).
Perry, S. F., Similowski, T., Klein, W. & Codd, J. R. The evolutionary origin of the mammalian diaphragm. Respir. Physiol. Neurobiol. 171, 1–16 (2010).
Sues, H. D. & Jenkins, F. A., Jr. in Amniote Paleobiology: Perspectives on the Evolution of Mammals, Birds and Reptiles (eds Carrano, M. T. et al.) 114–152 (Univ. Chicago Press, 2006).
Kühne, W. The Liassic therapsid Oligokyphus (British Museum (Natural History), 1956).
Guignard, M. L., Martinelli, A. G. & Soares, M. B. The postcranial anatomy of Brasilodon quadrangularis and the acquisition of mammaliaform traits among non-mammaliaform cynodonts. PLoS ONE 14, e0216672 (2019).
Oliveira, T. V., Schultz, C. L. & Soares, M. B. A partial skeleton of Chiniquodon (Cynodontia, Chiniquodontidae) from the Brazilian Middle Triassic. Rev. Bras. Paleontol. 12, 113–122 (2009).
Jenkins, F. A.Jr. The Chanares (Argentina) Triassic reptile fauna VII. The postcranial skeleton of the transversodontid Massetognathus pascuali (Therapsida, Cynodontia). Breviora 352, 1–28 (1970).
Jenkins, F. A. Jr. The postcranial skeleton of African cynodonts. Bull. Peabody Mus. Nat. Hist. 36, 1–216 (1971).
Jenkins, F. A. J. & Parrington, F. R. Postcranial skeletons of Triassic mammals Eozostrodon, Megazostrodon and Erythrotherium. Phil. Trans. R. Soc. B 273, 387–431 (1976).
Rey, K. et al. Oxygen isotopes suggest elevated thermometabolism within multiple Permo-Triassic therapsid clades. eLife 6, e28589 (2017).
Huttenlocker, A. K. & Farmer, C. Bone microvasculature tracks red blood cell size diminution in Triassic mammal and dinosaur forerunners. Curr. Biol. 27, 48–54 (2017).
Benoit, J., Manger, P. & Rubidge, B. Palaeoneurological clues to the evolution of defining mammalian soft tissue traits. Sci. Rep. 6, 25604 (2016).
Benoit, J. et al. The evolution of the maxillary canal in probainognathia (Cynodontia, Synapsida): reassessment of the homology of the infraorbital foramen in mammalian ancestors. J. Mamm. Evol. https://doi.org/10.1007/s10914-019-09467-8 (2019).
Benoit, J., Abdala, F., Manger, P. R. & Rubidge, B. S. The sixth sense in mammalian forerunners: variability of the parietal foramen and the evolution of the pineal eye in South African Permo-Triassic eutheriodont therapsids. Acta Palaeontol. Pol. 61, 777–789 (2016).
LeBlanc, A. R., Brink, K. S., Whitney, M. R., Abdala, F. & Reisz, R. R. Dental ontogeny in extinct synapsids reveals a complex evolutionary history of the mammalian tooth attachment system. Proc. R. Soc. B 285, 20181792 (2018).
Guignard, M. L., Martinelli, A. G. & Soares, M. B. Reassessment of the postcranial anatomy of Prozostrodon brasiliensis and implications for postural evolution of non-mammaliaform cynodonts. J. Vertebr. Paleontol. 38, e1511570 (2018).
Hillenius, W. J. Septomaxilla of nonmammalian synapsids: soft‐tissue correlates and a new functional interpretation. J. Morphol. 245, 29–50 (2000).
Zhou, C.-F., Wu, S., Martin, T. & Luo, Z.-X. A Jurassic mammaliaform and the earliest mammalian evolutionary adaptations. Nature 500, 163–167 (2013).
Gleizes, V., Viguier, E., Feron, J., Canivet, S. & Lavaste, F. Effects of freezing on the biomechanics of the intervertebral disc. Surg. Radiol. Anat. 20, 403–407 (1998).
Tan, J. S. & Uppuganti, S. Cumulative multiple freeze–thaw cycles and testing does not affect subsequent within-day variation in intervertebral flexibility of human cadaveric lumbosacral spine. Spine 37, E1238–E1242 (2012).
ImageJ (National Institutes of Health, 2004).
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2009).
Collyer, M. L. & Adams, D. C. RRPP: an r package for fitting linear models to high‐dimensional data using residual randomization. Methods Ecol. Evol. 9, 1772–1779 (2018).
Oksanen, J. et al. Vegan: Community ecology package. R version 1.17-4 http://cran.r-project.org (2010).
Adams, D. C. & Otarola-Castillo, E. Geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol. Evol. 4, 393–399 (2013).
Jones, K. E. et al. Dryad Data from: fossils reveal the complex evolutionary history of the mammalian regionalized spine. Dryad Digital Repository https://doi.org/10.5061/dryad.jm820mg (2018).
Kammerer, C. F. Revision of the Tanzanian dicynodont Dicynodon huenei (Therapsida: Anomodontia) from the Permian Usili formation. PeerJ 7, e7420 (2019).
We thank E. Hanslowe, J. Josimovich, B. Falk and R. Reed at the United States Geological Survey Daniel Beard Center, Invasive Species Science Branch, for providing the tegu cadavers used in this study. The cat cadavers were purchased directly from Carolina Biological. For advice on the functional distribution method we thank D. Polly and for general research support we thank all members of the Pierce Lab, particularly P. Lai. This research was supported by an American Association of Anatomists Fellowship (K.E.J.), the Harvard College Research Program and Museum of Comparative Zoology Grants-In-Aid of Undergraduate Research (S.G.), Harvard University (S.E.P), NSF EAR-1524938 (K.D.A.) and NSF EAR-1524523 (S.E.P.).
The authors declare no competing interests.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Jones, K.E., Gonzalez, S., Angielczyk, K.D. et al. Regionalization of the axial skeleton predates functional adaptation in the forerunners of mammals. Nat Ecol Evol 4, 470–478 (2020). https://doi.org/10.1038/s41559-020-1094-9
Communications Biology (2021)