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Paleontological and Developmental Evidence Resolve the Homology and Dual Embryonic Origin of a Mammalian Skull Bone, the Interparietal

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Paleontological and Developmental Evidence Resolve the Homology and Dual Embryonic Origin of a Mammalian Skull Bone, the Interparietal Paleontological and developmental evidence resolve the homology and dual embryonic origin of a mammalian skull bone, the interparietal Daisuke Koyabua,b,1, Wolfgang Maierc, and Marcelo R. Sánchez-Villagraa,1 aPalaeontological Institute and Museum, University of Zürich, 8006 Zürich, Switzerland; bKyoto University Museum, Kyoto University, Kyoto 606-8501, Japan; and cInstitute of Evolution and Ecology, University of Tübingen, 72076 Tübingen, Germany Edited by Clifford J. Tabin, Harvard Medical School, Boston, MA, and approved July 16, 2012 (received for review May 23, 2012) The homologies of mammalian skull elements are now fairly well supraoccipital (17). In contrast to the human pattern, it is gen- established, except for the controversial interparietal bone. A erally regarded for mammals that the interparietal arises in de- previous experimental study reported an intriguing mixed origin velopment as a pair of bones that soon fuse at the midline to form of the interparietal: the medial portion being derived from the a single bone (6, 8, 18). However, the absence of the interparietal neural crest cells, whereas the lateral portion from the mesoderm. has been pointed out in marsupials (11, 18), xenarthrans (19), The evolutionary history of such mixed origin remains unresolved, shrews (4), seals (10), hippopotamuses (10), and pangolins (11). and contradictory reports on the presence or absence and de- The classic work of de Beer (20) reported that the interparietal is velopmental patterns of the interparietal among mammals have lacking in monotremes, bandicoots, armadillos, and pigs. The paucity of appropriate embryonic material across mamma- complicated the question of its homology. Here we provide an lian species has undoubtedly hindered evaluations as to the pri- alternative perspective on the evolutionary identity of the interpar- mordial anlage, general presence, and variation of the interparietal. ietal, based on a comprehensive study across more than 300 extinct As exemplified in humans, the interparietal generally fuses with and extant taxa, integrating embryological and paleontological neighboring bones early in the perinatal period (12). Because the data. Although the interparietal has been regarded as being lost majority of work has been based on mature specimens, previous in various lineages, our investigation on embryos demonstrates its observers could have been misled by the early fusion of the inter- EVOLUTION presence in all extant mammalian “orders.” The generally accepted parietal with other bones. Here, with the unique availability of wide paradigm has regarded the interparietal as consisting of two ele- taxonomic and ontogenetic sampling across all extant mammalian ments that are homologized to the postparietals of basal amniotes. orders and major nonmammalian fossil taxa, we address the issues The tabular bones have been postulated as being lost during the of variation, patterns, and homology of the interparietal. Our rise of modern mammals. However, our results demonstrate that results question the generally accepted homology hypothesis, and the interparietal consists not of two but of four elements. We pro- we suggest an alternative model that explains the intriguing dual pose that the tabulars of basal amniotes are conserved as the lat- tissue origin of the interparietal. Our integrative study provides eral interparietal elements, which quickly fuse to the medial a bridge between paleontology and developmental biology and elements at the embryonic stage, and that the postparietals are a synthetic understanding of the dermal skull roof of vertebrates. homologous to the medial elements. Hence, the dual developmen- tal origin of the mammalian interparietal can be explained as the Results evolutionary consequence of the fusion between the crest-derived Below we present an overview of our findings. A full description of “postparietals” and the mesoderm-derived “tabulars.” our detailed survey is given in SI Appendix. All 51 nonmammalian synapsid species examined possessed the postparietal, which has embryology | morphological evolution | synapsids | fossil | occipital been posited as homologous to the interparietal (9), either unpaired or paired (SI Appendix,Fig.S3and Table S1). The Jurassic docodont mammal Haldanodon exspectatus reportedly possesses the inter- he evolutionary identity or homology of most mammalian skull parietal (21), as do the extant monotremes including the platypus Telements is now well established (1–3), although many con- Ornithorhynchus (22) and the long-beaked echidna Zaglossus (23). tradictory statements still exist on the interparietal, a dermal skull A small medial membrane bone, a remnant of the interparietal, roof element situated between the parietal and supraoccipital (e. is found in the short-beaked echidna Tachyglossus aculeatus (24). g., 4–8). Several authors have suggested a homology of the paired Marsupials reportedly lack the interparietal (11), but we confirmed mammalian interparietals to the paired postparietals in more its presence in various species (Trichosurus, Monodelphis, Didelphis, basal reptiles (6, 9). However, inconsistent patterns reported Macropus,andSminthopsis). Contrary to the reported absence of the among mammals (7, 10, 11), and even humans (12), and a unique interparietal in Monodelphis (25), in the examined embryonic series mixed embryonic origin (1) make the question of the homology of of the gray short-tailed opossum Monodelphis domestica,boththe the interparietal an unresolved issue of vertebrate anatomy. supraoccipital and interparietal are present. Here, the interparietal An experimental embryological study in the mouse by Jiang was found to be unpaired, paired, tripartite, and quadripartite, de- et al. (13) demonstrated a striking dual developmental origin of pending on the stage (SI Appendix,Fig.S4). the interparietal: the median portion is derived from the neural We recorded the presence of dermal interparietal bone in four crest cells, whereas the lateral portion is derived from the me- xenarthran species, including the long-nosed armadillo Dasypus soderm. This report has triggered a renewed interest among developmental biologists in the evolution of the interparietal in amniotes (1, 14, 15). Although integrating fossil record and Author contributions: D.K., W.M., and M.R.S.-V. designed research; D.K., W.M., and comparative anatomical data with newly gained experimental M.R.S.-V. performed research; D.K. analyzed data; and D.K. and M.R.S.-V. wrote findings should provide relevant information for the current the paper. discussions on the origin of skull roof bones, it has been ham- The authors declare no conflict of interest. pered by terminological inconsistencies, even within the stem This article is a PNAS Direct Submission. mammal (synapsid) lineage, and unsolved homologies across 1To whom correspondence may be addressed. E-mail: [email protected] or major living groups (4, 6, 7, 9, 11, 16). In humans, the interparietal [email protected]. fi develops from two pairs of ossi cation centers, one medial pair This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. and one lateral pair, eventually fusing seamlessly to the 1073/pnas.1208693109/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1208693109 PNAS | August 28, 2012 | vol. 109 | no. 35 | 14075–14080 Downloaded by guest on September 29, 2021 hybridus (Fig. 1A and SI Appendix, Table S1). Our investigation The interparietal is present in artiodactyls, cetaceans, peri- confirmed the presence of the interparietal across afrotherians ssodactyls, carnivorans, bats, and pangolins (Fig. 2 B–H and SI (SI Appendix, Figs. S5 A and B and S6 and Table S1). We Appendix, Fig. S9 A–C and Table S1). The bottle-nosed dolphin identified unpaired, paired, and tripartite interparietals in the Tursiops truncatus possesses an expanded median and two lateral tree hyrax Dendrohyrax arboreus. The interparietal in the rock interparietal elements (Fig. 2G). Eales (28) described the greatly hyrax Procavia capensis was found to be unpaired, paired, tri- expanded four-element interparietal in the narwhal Monodon partite, and quadripartite. In some individuals, the lateral ele- monoceros. The cow Bos primigenius exhibited quadripartite ments fuse earlier to the supraoccipital rather than to the medial interparietal (Fig. 2H). The tripartite interparietal is reported for elements (SI Appendix, Fig. S5B). Tripartite interparietal ele- the yak Bos grunniens (29). Wegner (1960) documented the tri- ments were described for the cape golden mole Chrysochloris partite interparietal in the jaguar Panthera onca and cougar asiatica (2). In sirenians (Dugong dugon, Trichechus manatus, and Puma concolor. Although Giebel (10) noted that seals lack the Trichechus senegalensis) the interparietal showed a maximum of interparietal, we observed that prenatal skulls of fur seals Arc- four elements. Among extinct South American notoungulates, tocephalus (SI Appendix, Fig. S5G) and Callorhinus ursinus (SI Toxodon burmeisteri, Typotherium cristatum, Nesodon imbricatus, Appendix, Fig. S8B) display enlarged interparietals and that the and Pachyrucus were confirmed to possess the interparietal. supraoccipital is extremely reduced in size compared with the We observed the interparietal universally in Euarchontoglires interparietal, which dominates the caudal portion of the vault. (Fig. 2 I–J and SI Appendix, Fig. S9 D–F and Table S1). In the The earless seal Phoca is reported to exhibit the lateral inter-
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