{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,15]],"date-time":"2026-06-15T15:48:54Z","timestamp":1781538534364,"version":"3.54.5"},"reference-count":63,"publisher":"PeerJ","license":[{"start":{"date-parts":[[2024,8,12]],"date-time":"2024-08-12T00:00:00Z","timestamp":1723420800000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"JSPS KAKENHI","award":["JP 19H03290"],"award-info":[{"award-number":["JP 19H03290"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:p>Heterodonty and complex molar morphology are important characteristics of mammals acquired during the evolution of early mammals from non-mammalian synapsids. Some non-mammalian synapsids had only simple, unicuspid teeth, whereas others had complex, multicuspid teeth. In this study, we reconstructed the ancestral states of tooth morphological complexity across non-mammalian synapsids to show that morphologically complex teeth evolved independently multiple times within Therapsida and that secondary simplification of tooth morphology occurred in some non-mammalian Cynodontia. In some mammals, secondary evolution of simpler teeth from complex molars has been previously reported to correlate with an anterior shift of tooth eruption position in the jaw, as evaluated by the dentition position relative to the ends of component bones used as reference points in the upper jaw. Our phylogenetic comparative analyses showed a significant correlation between an increase in tooth complexity and a posterior shift in the dentition position relative to only one of the three specific ends of component bones that we used as reference points in the upper jaw of non-mammalian synapsids. The ends of component bones depend on the shape and relative area of each bone, which appear to vary considerably among the synapsid taxa. Quantification of the dentition position along the anteroposterior axis in the overall cranium showed suggestive evidence of a correlation between an increase in tooth complexity and a posterior shift in the dentition position among non-mammalian synapsids. This correlation supports the hypothesis that a posterior shift of tooth eruption position relative to the morphogenetic fields that determine tooth form have contributed to the evolution of morphologically complex teeth in non-mammalian synapsids, if the position in the cranium represents a certain point in the morphogenetic fields.<\/jats:p>","DOI":"10.7717\/peerj.17784","type":"journal-article","created":{"date-parts":[[2024,8,12]],"date-time":"2024-08-12T09:33:42Z","timestamp":1723455222000},"page":"e17784","source":"Crossref","is-referenced-by-count":3,"title":["Evolution of tooth morphological complexity and its association with the position of tooth eruption in the jaw in non-mammalian synapsids"],"prefix":"10.7717","volume":"12","author":[{"given":"Tomohiro","family":"Harano","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Masakazu","family":"Asahara","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"4443","published-online":{"date-parts":[[2024,8,12]]},"reference":[{"issue":"2","key":"10.7717\/peerj.17784\/ref-1","doi-asserted-by":"publisher","first-page":"301","DOI":"10.4202\/app.2010.0063","article-title":"On the affinities of Tetraceratops insignis, an Early Permian synapsid","volume":"56","author":"Amson","year":"2011","journal-title":"Acta Palaeontologica Polonica"},{"key":"10.7717\/peerj.17784\/ref-2","doi-asserted-by":"publisher","first-page":"e24","DOI":"10.7717\/peerj.24","article-title":"Development and evolution of the unique cetacean dentition","volume":"1","author":"Armfield","year":"2013","journal-title":"PeerJ"},{"issue":"1832","key":"10.7717\/peerj.17784\/ref-3","doi-asserted-by":"publisher","first-page":"20160375","DOI":"10.1098\/rspb.2016.0375","article-title":"Unique pattern of dietary adaptation in the dentition of Carnivora: its advantage and developmental origin","volume":"283","author":"Asahara","year":"2016","journal-title":"Proceedings of the Royal Society B: Biological Sciences"},{"issue":"1","key":"10.7717\/peerj.17784\/ref-4","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1111\/j.1469-7998.1939.tb00021.x","article-title":"Studies of the mammalian dentition.\u2013differentiation of the post-canine dentition","volume":"109","author":"Butler","year":"1939","journal-title":"Proceedings of the Zoological Society of London"},{"key":"10.7717\/peerj.17784\/ref-5","volume-title":"Colbert\u2019s evolution of the vertebrates: a history of the backboned animals through time","author":"Colbert","year":"2001","edition":"5"},{"key":"10.7717\/peerj.17784\/ref-6","first-page":"324","article-title":"On the trituberculate type of molar tooth in the Mammalia","volume":"21","author":"Cope","year":"1883","journal-title":"Proceedings of the American Philosophical Society"},{"key":"10.7717\/peerj.17784\/ref-7","doi-asserted-by":"publisher","first-page":"568","DOI":"10.1111\/evo.12866","article-title":"The role of inhibitory dynamics in the loss and reemergence of macropodoid tooth traits","volume":"70","author":"Couzens","year":"2016","journal-title":"Evolution"},{"key":"10.7717\/peerj.17784\/ref-8","doi-asserted-by":"publisher","DOI":"10.1101\/833749","article-title":"Predicting evolutionary transitions in tooth complexity with a morphogenetic model","author":"Couzens","year":"2019","journal-title":"BioRxiv"},{"key":"10.7717\/peerj.17784\/ref-9","doi-asserted-by":"publisher","first-page":"e2019294118","DOI":"10.1073\/pnas.2019294118","article-title":"Developmental influence on evolutionary rates and the origin of placental mammal tooth complexity","volume":"118","author":"Couzens","year":"2021","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"10.7717\/peerj.17784\/ref-10","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1111\/j.1469-185X.1968.tb00966.x","article-title":"Molar occlusion in Late Triassic mammals","volume":"43","author":"Crompton","year":"1968","journal-title":"Biological Reviews"},{"key":"10.7717\/peerj.17784\/ref-11","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-319-98280-9","volume-title":"Marine mammals: adaptations for an aquatic life","author":"Davis","year":"2019"},{"key":"10.7717\/peerj.17784\/ref-12","first-page":"381","article-title":"A revised description of the skull of Moschorhinus (Therapsida, Therocephalia)","volume":"99","author":"Durand","year":"1991","journal-title":"Annals of the South African Museum"},{"key":"10.7717\/peerj.17784\/ref-13","volume-title":"Mammalogy: adaptation, diversity, and ecology","author":"Feldhamer","year":"2003","edition":"2"},{"issue":"7","key":"10.7717\/peerj.17784\/ref-14","doi-asserted-by":"publisher","first-page":"1367","DOI":"10.1111\/j.1420-9101.2009.01757.x","article-title":"The seven deadly sins of comparative analysis","volume":"22","author":"Freckleton","year":"2009","journal-title":"Journal of Evolutionary Biology"},{"issue":"4","key":"10.7717\/peerj.17784\/ref-15","doi-asserted-by":"publisher","first-page":"708","DOI":"10.1046\/j.1365-2656.2001.00524.x","article-title":"On the misuse of residuals in ecology: testing regression residuals vs. the analysis of covariance","volume":"70","author":"Garc\u00eda-Berthou","year":"2001","journal-title":"Journal of Animal Ecology"},{"issue":"2","key":"10.7717\/peerj.17784\/ref-16","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1111\/j.1469-7998.1978.tb03282.x","article-title":"The jaw lever system in ungulates: a new model","volume":"184","author":"Greaves","year":"1978","journal-title":"Journal of Zoology"},{"key":"10.7717\/peerj.17784\/ref-17","first-page":"169","article-title":"A half century of trituberculy the Cope-Osborn theory of dental evolution with a revised summary of molar evolution from fish to man","volume":"73","author":"Gregory","year":"1934","journal-title":"Proceedings of the American Philosophical Society"},{"key":"10.7717\/peerj.17784\/ref-18","doi-asserted-by":"publisher","first-page":"2986","DOI":"10.1111\/evo.14637","article-title":"The anteriorization of tooth position underlies the atavism of tooth morphology: insights into the morphogenesis of mammalian molars","volume":"76","author":"Harano","year":"2022a","journal-title":"Evolution"},{"issue":"2","key":"10.7717\/peerj.17784\/ref-19","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1111\/jzo.13005","article-title":"Correlated evolution of craniodental morphology and feeding ecology in carnivorans: a comparative analysis of jaw lever arms at tooth positions","volume":"318","author":"Harano","year":"2022b","journal-title":"Journal of Zoology"},{"issue":"7389","key":"10.7717\/peerj.17784\/ref-20","doi-asserted-by":"publisher","first-page":"324","DOI":"10.1038\/nature10876","article-title":"On the difficulty of increasing dental complexity","volume":"483","author":"Harjunmaa","year":"2012","journal-title":"Nature"},{"issue":"7512","key":"10.7717\/peerj.17784\/ref-21","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1038\/nature13613","article-title":"Replaying evolutionary transitions from the dental fossil record","volume":"512","author":"Harjunmaa","year":"2014","journal-title":"Nature"},{"issue":"3","key":"10.7717\/peerj.17784\/ref-22","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1093\/sysbio\/syu005","article-title":"A linear-time algorithm for Gaussian and non-Gaussian trait evolution models","volume":"63","author":"Ho","year":"2014","journal-title":"Systematic Biology"},{"key":"10.7717\/peerj.17784\/ref-23","first-page":"5","article-title":"A probainognathian cynodont from South Africa and the phylogeny of nonmammalian cynodonts","volume":"156","author":"Hopson","year":"2001","journal-title":"Bulletin of the Museum of Comparative Zoology"},{"issue":"23","key":"10.7717\/peerj.17784\/ref-24","doi-asserted-by":"publisher","first-page":"10718","DOI":"10.1073\/pnas.92.23.10718","article-title":"The hypocone as a key innovation in mammalian evolution","volume":"92","author":"Hunter","year":"1995","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"issue":"6","key":"10.7717\/peerj.17784\/ref-25","doi-asserted-by":"publisher","first-page":"2641","DOI":"10.1073\/pnas.050586297","article-title":"Linking development with generation of novelty in mammalian teeth","volume":"97","author":"Jernvall","year":"2000","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"10.7717\/peerj.17784\/ref-26","doi-asserted-by":"publisher","first-page":"1489","DOI":"10.1126\/science.274.5292.1489","article-title":"Molar tooth diversity, disparity, and ecology in Cenozoic ungulate radiations","volume":"274","author":"Jernvall","year":"1996","journal-title":"Science"},{"issue":"1","key":"10.7717\/peerj.17784\/ref-27","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41467-019-13026-3","article-title":"Stepwise shifts underlie evolutionary trends in morphological complexity of the mammalian vertebral column","volume":"10","author":"Jones","year":"2019","journal-title":"Nature Communications"},{"issue":"2001","key":"10.7717\/peerj.17784\/ref-28","doi-asserted-by":"publisher","first-page":"e1608","DOI":"10.7717\/peerj.1608","article-title":"Systematics of the Rubidgeinae (Therapsida: Gorgonopsia)","volume":"4","author":"Kammerer","year":"2016","journal-title":"PeerJ"},{"issue":"7014","key":"10.7717\/peerj.17784\/ref-29","doi-asserted-by":"publisher","first-page":"211","DOI":"10.1038\/nature02927","article-title":"Nonindependence of mammalian dental characters","volume":"432","author":"Kangas","year":"2004","journal-title":"Nature"},{"key":"10.7717\/peerj.17784\/ref-30","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1098\/rstb.1979.0001","article-title":"The primitive cynodont Procynosuchus: functional anatomy of the skull and relationships","volume":"285","author":"Kemp","year":"1979","journal-title":"Philosophical Transactions of the Royal Society B: Biological Sciences"},{"key":"10.7717\/peerj.17784\/ref-31","volume-title":"The origin and evolution of mammals","author":"Kemp","year":"2005"},{"key":"10.7717\/peerj.17784\/ref-32","doi-asserted-by":"publisher","first-page":"1231","DOI":"10.1111\/j.1420-9101.2005.01076.x","article-title":"The origin and early radiation of the therapsid mammal-like reptiles: a palaeobiological hypothesis","volume":"19","author":"Kemp","year":"2006","journal-title":"Journal of Evolutionary Biology"},{"key":"10.7717\/peerj.17784\/ref-33","doi-asserted-by":"crossref","DOI":"10.7312\/kiel11918","volume-title":"Mammals from the age of dinosaurs: origins, evolution, and structure","author":"Kielan-Jaworowska","year":"2004"},{"key":"10.7717\/peerj.17784\/ref-34","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41467-021-26285-w","article-title":"Multiple evolutionary origins and losses of tooth complexity in squamates","volume":"12","author":"Lafuma","year":"2021","journal-title":"Nature Communications"},{"key":"10.7717\/peerj.17784\/ref-35","doi-asserted-by":"publisher","first-page":"1011","DOI":"10.1038\/nature06277","article-title":"Transformation and diversification in early mammal evolution","volume":"450","author":"Luo","year":"2007","journal-title":"Nature"},{"key":"10.7717\/peerj.17784\/ref-36","article-title":"Mesquite: a modular system for evolutionary analysis. Version 3.61","author":"Maddison","year":"2019"},{"issue":"1","key":"10.7717\/peerj.17784\/ref-37","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1111\/joa.12992","article-title":"Disconnecting bones within the jaw-otic network modules underlies mammalian middle ear evolution","volume":"235","author":"Navarro-D\u00edaz","year":"2019","journal-title":"Journal of Anatomy"},{"issue":"264","key":"10.7717\/peerj.17784\/ref-38","doi-asserted-by":"publisher","first-page":"1067","DOI":"10.1086\/274831","article-title":"The evolution of mammalian molars to and from the tritubercular type","volume":"22","author":"Osborn","year":"1888","journal-title":"The American Naturalist"},{"issue":"372","key":"10.7717\/peerj.17784\/ref-39","doi-asserted-by":"publisher","first-page":"993","DOI":"10.1086\/276747","article-title":"Trituberculy: a review dedicated to the late Professor Cope","volume":"31","author":"Osborn","year":"1897","journal-title":"The American Naturalist"},{"key":"10.7717\/peerj.17784\/ref-40","volume-title":"R: a language and environment for statistical computing","author":"R Development Core Team","year":"2022"},{"issue":"2","key":"10.7717\/peerj.17784\/ref-41","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1111\/j.2041-210X.2011.00169.x","article-title":"phytools: an R package for phylogenetic comparative biology (and other things)","volume":"3","author":"Revell","year":"2012","journal-title":"Methods in Ecology and Evolution"},{"key":"10.7717\/peerj.17784\/ref-42","volume-title":"tpsDig, digitize landmarks and outlines, version 2.31","author":"Rohlf","year":"2017"},{"key":"10.7717\/peerj.17784\/ref-43","volume-title":"The vertebrate body","author":"Romer","year":"1986","edition":"6"},{"issue":"3","key":"10.7717\/peerj.17784\/ref-44","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1080\/02724634.1988.10011708","article-title":"Definition, diagnosis, and origin of Mammalia","volume":"8","author":"Rowe","year":"1988","journal-title":"Journal of Vertebrate Paleontology"},{"issue":"7241","key":"10.7717\/peerj.17784\/ref-45","doi-asserted-by":"publisher","first-page":"1021","DOI":"10.1038\/nature07985","article-title":"A semi-aquatic Arctic mammalian carnivore from the Miocene epoch and origin of Pinnipedia","volume":"458","author":"Rybczynski","year":"2009","journal-title":"Nature"},{"issue":"6838","key":"10.7717\/peerj.17784\/ref-46","doi-asserted-by":"publisher","first-page":"684","DOI":"10.1038\/35079567","article-title":"Earliest evidence for efficient oral processing in a terrestrial herbivore","volume":"411","author":"Rybczynski","year":"2001","journal-title":"Nature"},{"issue":"7288","key":"10.7717\/peerj.17784\/ref-47","doi-asserted-by":"publisher","first-page":"583","DOI":"10.1038\/nature08838","article-title":"A computational model of teeth and the developmental origins of morphological variation","volume":"464","author":"Salazar-Ciudad","year":"2010","journal-title":"Nature"},{"issue":"1","key":"10.7717\/peerj.17784\/ref-48","doi-asserted-by":"publisher","first-page":"e2008850118","DOI":"10.1073\/pnas.2008850118","article-title":"Mammalian molar complexity follows simple, predictable patterns","volume":"118","author":"Selig","year":"2021","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"10.7717\/peerj.17784\/ref-49","first-page":"145","article-title":"\u00c9tude du premier cas\u00e9id\u00e9 (Reptilia, Pelycosauria) d\u2019Europe occidentale","volume":"230","author":"Sigogneau-Russell","year":"1974","journal-title":"Bulletin du Mus\u00e9um National d\u2019histoire Naturelle"},{"key":"10.7717\/peerj.17784\/ref-50","doi-asserted-by":"publisher","first-page":"481","DOI":"10.1002\/bies.950190607","article-title":"Patterning of the mammalian dentition in development and evolution","volume":"19","author":"Stock","year":"1997","journal-title":"Bioessays"},{"key":"10.7717\/peerj.17784\/ref-51","first-page":"1","article-title":"Morphology and systematics of the Northern Dvina cynodonts (Reptilia, Therapsida; Upper Permian)","volume":"125","author":"Tatarinov","year":"1968","journal-title":"Postilla"},{"issue":"9","key":"10.7717\/peerj.17784\/ref-52","doi-asserted-by":"publisher","first-page":"2326","DOI":"10.1139\/z91-327","article-title":"Cranial strength in relation to estimated biting forces in some mammals","volume":"69","author":"Thomason","year":"1991","journal-title":"Canadian Journal of Zoology"},{"key":"10.7717\/peerj.17784\/ref-53","first-page":"131","article-title":"The evolution of the teeth in the Mammalia","volume":"37","author":"Tims","year":"1903","journal-title":"Journal of Anatomy and Physiology"},{"issue":"1713","key":"10.7717\/peerj.17784\/ref-54","doi-asserted-by":"publisher","first-page":"20150483","DOI":"10.1098\/rstb.2015.0483","article-title":"Major evolutionary transitions and innovations: the tympanic middle ear","volume":"372","author":"Tucker","year":"2017","journal-title":"Philosophical Transactions of the Royal Society B: Biological Sciences"},{"key":"10.7717\/peerj.17784\/ref-55","doi-asserted-by":"crossref","DOI":"10.1353\/book.485","volume-title":"Mammal teeth: origin, evolution, and diversity","author":"Ungar","year":"2010"},{"issue":"1","key":"10.7717\/peerj.17784\/ref-56","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1093\/icb\/icm016","article-title":"D\u00e9j\u00e0 vu: the evolution of feeding morphologies in the Carnivora","volume":"47","author":"Van Valkenburgh","year":"2007","journal-title":"Integrative and Comparative Biology"},{"key":"10.7717\/peerj.17784\/ref-57","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-019-49116-x","article-title":"Homeobox code model of heterodont tooth in mammals revised","volume":"9","author":"Wakamatsu","year":"2019","journal-title":"Scientific Reports"},{"key":"10.7717\/peerj.17784\/ref-58","doi-asserted-by":"publisher","first-page":"e0218791","DOI":"10.1371\/journal.pone.0218791","article-title":"First record of a basal mammaliamorph from the early Late Triassic Ischigualasto Formation of Argentina","volume":"14","author":"Wallace","year":"2019","journal-title":"PLOS ONE"},{"key":"10.7717\/peerj.17784\/ref-59","first-page":"268","article-title":"Evolution of mammalian teeth","volume":"42","author":"Weller","year":"1968","journal-title":"Journal of Paleontology"},{"key":"10.7717\/peerj.17784\/ref-60","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1007\/978-3-030-13739-7_18","article-title":"Feeding in mammals: comparative, experimental, and evolutionary insights on form and function","volume-title":"Feeding in Vertebrates","author":"Williams","year":"2019"},{"key":"10.7717\/peerj.17784\/ref-61","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1016\/j.job.2022.03.007","article-title":"Evolution and development of the mammalian multicuspid teeth","volume":"64","author":"Yamanaka","year":"2022","journal-title":"Journal of Oral Biosciences"},{"key":"10.7717\/peerj.17784\/ref-62","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1111\/ede.12116","article-title":"Patterning of mammalian heterodont dentition within the upper and lower jaws","volume":"17","author":"Yamanaka","year":"2015","journal-title":"Evolution & Development"},{"key":"10.7717\/peerj.17784\/ref-63","doi-asserted-by":"publisher","first-page":"170761","DOI":"10.1098\/rsos.170761","article-title":"Deletion\/loss of bone morphogenetic protein 7 changes tooth morphology and function in Mus musculus: implications for dental evolution in mammals","volume":"5","author":"Zurowski","year":"2018","journal-title":"Royal Society Open Science"}],"container-title":["PeerJ"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/peerj.com\/articles\/17784.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/peerj.com\/articles\/17784.xml","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/peerj.com\/articles\/17784.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/peerj.com\/articles\/17784.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,8,12]],"date-time":"2024-08-12T09:34:19Z","timestamp":1723455259000},"score":1,"resource":{"primary":{"URL":"https:\/\/peerj.com\/articles\/17784"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,8,12]]},"references-count":63,"alternative-id":["10.7717\/peerj.17784"],"URL":"https:\/\/doi.org\/10.7717\/peerj.17784","archive":["CLOCKSS","LOCKSS","Portico"],"relation":{},"ISSN":["2167-8359"],"issn-type":[{"value":"2167-8359","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,8,12]]},"article-number":"e17784"}}