Johannes Müller a,1, Torsten M. Scheyer b, Jason J. Head c, Paul M. Barrett d, Ingmar Werneburg b, Per G. P. Ericson e, Diego Pol f, and Marcelo R. Sánchez-Villagra b,1
-Author Affiliations
aMuseum für Naturkunde – Leibniz-Institut für Evolutions- und Biodiversitätsforschung an der Humboldt-Universität zu Berlin, D-10115 Berlin, Germany;
bPaläontologisches Institut und Museum, Universität Zürich, CH-8006 Zürich, Switzerland;
cDepartment of Biology, University of Toronto Mississauga, Mississauga, ON L5L 1C6, Canada;
dDepartment of Palaeontology, Natural History Museum, London SW7 5BD, United Kingdom;
eDepartment of Vertebrate Zoology, Swedish Museum of Natural History, SE-10405 Stockholm, Sweden; and
fConsejo Nacional de Investigaciones Científicas y Técnicas, Museo Paleontológico Egidio Feruglio, Trelew CP 9100, Argentina
Edited by Clifford J. Tabin, Harvard Medical School, Boston, MA, and approved December 4, 2009 (received for review November 3, 2009)
Abstract
The development of distinct regions in the amniote vertebral column results from somite formation and Hox gene expression, with the adult morphology displaying remarkable variation among lineages. Mammalian regionalization is reportedly very conservative or even constrained, but there has been no study investigating vertebral count variation across Amniota as a whole, undermining attempts to understand the phylogenetic, ecological, and developmental factors affecting vertebral column variation. Here, we show that the mammalian (synapsid) and reptilian lineages show early in their evolutionary histories clear divergences in axial developmental plasticity, in terms of both regionalization and meristic change, with basal synapsids sharing the conserved axial configuration of crown mammals, and basal reptiles demonstrating the plasticity of extant taxa. We conducted a comprehensive survey of presacral vertebral counts across 436 recent and extinct amniote taxa. Vertebral counts were mapped onto a generalized amniote phylogeny as well as individual ingroup trees, and ancestral states were reconstructed by using squared-change parsimony. We also calculated the relationship between presacral and cervical numbers to infer the relative influence of homeotic effects and meristic changes and found no correlation between somitogenesis and Hox-mediated regionalization. Although conservatism in presacral numbers characterized early synapsid lineages, in some cases reptiles and synapsids exhibit the same developmental innovations in response to similar selective pressures. Conversely, increases in body mass are not coupled with meristic or homeotic changes, but mostly occur in concert with postembryonic somatic growth. Our study highlights the importance of fossils in large-scale investigations of evolutionary developmental processes.
constraint development Hox genes segmentation paleontology
Footnotes
1To whom correspondence may be addressed. E-mail:johannes.mueller@mfn-berlin.de or m.sanchez@pim.uzh.ch.
Author contributions: J.M., T.M.S., J.J.H., P.M.B., and M.S.-V. designed research; J.M., T.M.S., J.J.H., and M.R.S.-V. performed research; J.M., T.M.S., J.J.H., P.M.B., I.W., P.G.P.E., D.P., and M.R.S.-V. contributed new reagents/analytic tools; J.M., T.M.S., J.J.H., and M.R.S.-V. analyzed data; and J.M., J.J.H., and M.R.S.-V. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/cgi/content/full/0912622107/DCSupplemental.
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