Homeotic Effects, Somitogenesis and the Evolution of Vertebral Numbers in Recent and Fossil Amniotes

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Homeotic Effects, Somitogenesis and the Evolution of Vertebral Numbers in Recent and Fossil Amniotes Homeotic effects, somitogenesis and the evolution of vertebral numbers in recent and fossil amniotes Johannes Müllera,1, Torsten M. Scheyerb, Jason J. Headc, Paul M. Barrettd, Ingmar Werneburgb, Per G. P. Ericsone, Diego Polf, and Marcelo R. Sánchez-Villagrab,1 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) The development of distinct regions in the amniote vertebral subdivided still further into thoracic and lumbar vertebrae in column results from somite formation and Hox gene expression, mammals). These regional identities result from different Hox gene with the adult morphology displaying remarkable variation among expressions along the vertebrate body axis (7, 8); consequently, the lineages. Mammalian regionalization is reportedly very conserva- vertebral column can be viewed as a result of the transformation of tive or even constrained, but there has been no study investigating repeated developmental modules into different evolutionary mod- vertebral count variation across Amniota as a whole, undermining ules (9, 10). Hox genes are activated in the lateral somite precursors attempts to understand the phylogenetic, ecological, and develop- in the epiblast, so the timing of Hox activation during gastrulation mental factors affecting vertebral column variation. Here, we show largely determines the position of expression domains of Hox genes that the mammalian (synapsid) and reptilian lineages show early in along the anteroposterior body axis, whereas the stem cell-derived their evolutionary histories clear divergences in axial developmen- medial somite precursors control segmentation (11). Because of the tal plasticity, in terms of both regionalization and meristic change, spatial dissociation between segmentation and axial regionalization, with basal synapsids sharing the conserved axial configuration of it has recently been suggested that the two processes are uncoupled crown mammals, and basal reptiles demonstrating the plasticity of (11, 12), despite some indication of crosstalk between the segmen- extant taxa. We conducted a comprehensive survey of presacral tation machinery and Hox patterning (11, 13). vertebral counts across 436 recent and extinct amniote taxa. Verte- The vertebral column has recently attracted the interest of many bral counts were mapped onto a generalized amniote phylogeny as evolutionary and developmental biologists because the formative well as individual ingroup trees, and ancestral states were recon- roles of somitogenesis, somatic growth, and Hox gene expression are structed by using squared-change parsimony. We also calculated the coupled with easily observable adult phenotypes. For example, relationship between presacral and cervical numbers to infer the there have been investigations into vertebral count variation in relative influence of homeotic effects and meristic changes and numerous taxa, including fish, amphibians, reptiles, and mammals found no correlation between somitogenesis and Hox-mediated (5, 9, 14–21). Most of these studies ask whether, and how, vertebral regionalization. Although conservatism in presacral numbers char- counts are affected by developmental constraints and modular acterized early synapsid lineages, in some cases reptiles and synap- evolution, and how changing vertebral counts effect body size evo- sids exhibit the same developmental innovations in response to similar selective pressures. Conversely, increases in body mass are lution. Mammals in particular have attracted much attention not coupled with meristic or homeotic changes, but mostly occur in because, with few exceptions, their precaudal vertebral counts are concert with postembryonic somatic growth. Our study highlights highly conserved, or constrained (15, 17). By contrast, reptiles (including birds) are more variable in their vertebral numbers; the the importance of fossils in large-scale investigations of evolution- > ary developmental processes. most dramatic example are snakes, with some taxa possessing 300 precaudal vertebrae (5). However, all of these comparisons have constraint | development | Hox genes | segmentation | paleontology suffered from the fact that there has, so far, been no comprehensive treatment of vertebral count variation across Amniota as a whole, and none that have taken full account of extinct taxa that include omitogenesis, somatic growth, and Hox gene expression are morphologies that are unrepresented in the modern biota. primary factors driving the formation of the vertebrate body axis S Amniota is the tetrapod clade that is composed of Synapsida (1, 2). Somitogenesis occurs via the rhythmic budding of embryonic (crown mammals and their fossil relatives) and Reptilia (including somites from the anterior part of the presomitic mesoderm, until a birds), and is diagnosed by a suite of adaptations for terrestrial point when the latter has shrunk to such a degree that no further habits, including extraembryonic membranes (22). The oldest rep- somites can be formed (3). Periodic somite formation is controlled by a molecular oscillator or “segmentation clock” (4), whereas the resentatives of modern amniote crown clades have been recovered speed of the clock is highly variable across different vertebrate lin- from Triassic deposits (23). Here, we examine variation of presacral vertebral counts across all eages. For example, the segmentation clock in snakes ticks much SI Methods SI Appendix faster than in a mouse, resulting in a higher number of relatively major amniote clades ( and ), fossil and smaller somites (3). Because the ossified vertebrae are derived from the embryonic somites through resegmentation (1), vertebral num- bers can provide insights into the speed of the segmentation clock 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 the pattern of somitogenesis. In addition, the relative size of and M.R.S.-V. contributed new reagents/analytic tools; J.M., T.M.S., J.J.H., and M.R.S.-V. vertebrae relative to the number of vertebrae provides information analyzed data; and J.M., J.J.H., and M.R.S.-V. wrote the paper. about the rate of somatic growth (5, 6). The authors declare no conflict of interest. Besides the marked variation in the number and sizes of verte- This article is a PNAS Direct Submission. brae, the vertebrate body axis is also highly regionalized. In tetra- 1To whom correspondence may be addressed. E-mail: [email protected] or pods, this regionalization is expressed in the formation of presacral, [email protected]. sacral, and caudal vertebral series, and the presacral portion can be This article contains supporting information online at www.pnas.org/cgi/content/full/ further subdivided into cervical and dorsal series (with the latter 0912622107/DCSupplemental. 2118–2123 | PNAS | February 2, 2010 | vol. 107 | no. 5 www.pnas.org/cgi/doi/10.1073/pnas.0912622107 Downloaded by guest on September 29, 2021 extant. We focus on the presacral portion of the body axis because it whereas placodonts, the sister taxon to plesiosaurs and other is regionalizedin most amniotes, and because the caudal skeleton is a eosauropterygians, exhibit a CP ratio of 0.32. single, anatomically undifferentiated region whose segmentation is Lepidosauromorpha includes the taxa with the strongest temporally disjunct from the presacral region and is derived by ter- deviations from the ancestral amniote condition; the CP ratios minal addition at the tailbud, a different patterning than in the found include the lowest among all amniotes. Squamata as a presacral region (9, 24). As a result, changes in caudal somite counts whole has an ancestral CP value of 0.08. In rhynchocephalians, are uninformative with respect to the relative roles of both homeotic the aquatic pleurosaurids have a CP ratio of 0.18, whereas the and meristic changes within specific regions of the axial skeleton. terrestrial species such as the tuatara remain comparatively close Additionally, the posterior parts of the vertebral column such as the to the ancestral amniote condition (CP = 0.28). sacral and caudal regions are often not preserved in fossils and The aquatic choristoderes have a high CP ratio of 0.43, and so do therefore are difficult to study. By including fossils, we trace the archosauromorphs, with a CP ratio of 0.41. The values remain high evolutionary developmental history of extant taxa through the throughout the various archosauromorph lineages, which also inclusion of their extinct relatives and examine developmental pat- applies to turtles (CP = 0.44) despite their very low count of only 18 terns in different ecologies within a comparative phylogenetic presacrals. The paraphyletic prolacertiforms differ strongly from framework. In
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