Origins of slow growth on the crocodilian stem lineage

Crocodilians grow slowly and have low metabolic rates similar to other living reptiles, but palaeohistology indicates that they evolved from an ancestor with higher growth rates. 1 Seymour R.S. Bennett-Stamper C.L. Johnston S.D. Carrier D.R. Grigg G.C. Evidence for endothermic ancestors of crocodiles at the stem of archosaur evolution. Physiol. Biochem. Zool. 2004; 77: 1051-1067 Crossref PubMed Scopus (136) Google Scholar ,2 Summers A.P. Evolution: warm-hearted crocs. Nature. 2005; 434: 833-834https://doi.org/10.1038/434833a Crossref PubMed Scopus (20) Google Scholar ,3 Farmer C.G. Sanders K. Unidirectional airflow in the lungs of alligators. Science. 2010; 327: 338-340https://doi.org/10.1126/science.1180219 Crossref PubMed Scopus (109) Google Scholar ,4 Legendre L.J. Segalen L. Cubo J. Evidence for high bone growth rate in Euparkeria obtained using a new paleohistological inference model for the humerus. J. Vertebr. Paleontol. 2013; 33: 1343-1350https://doi.org/10.1080/02724634.2013.780060 Crossref Scopus (37) Google Scholar ,5 Legendre L.J. Guénard G. Botha-Brink J. Cubo J. Palaeohistological evidence for ancestral high metabolic rate in archosaurs. Syst. Biol. 2016; 65: 989-996https://doi.org/10.1093/sysbio/syw033 Crossref PubMed Scopus (84) Google Scholar It remains unclear when slow growth appeared in the clade due to the sparse data on key divergences among early Mesozoic members of their stem lineage. We present new osteohistological data from a broad sample of early crocodylomorphs, evaluated in a phylogenetic context alongside other pseudosuchians. We find that the transition to slow-growing bone types during mid-late ontogeny occurred around the origin of Crocodylomorpha during the Late Triassic. Earlier-diverging pseudosuchians had high maximum growth rates, as indicated by the presence of woven bone during middle and (sometimes) late ontogeny. 6 de Ricqlès A.J. Padian K. Horner J.R. On the bone histology of some Triassic pseudosuchian archosaurs and related taxa. Ann. Paleontol. 2003; 89: 67-101 Crossref Scopus (138) Google Scholar ,7 de Ricqlès A. Padian K. Knoll F. Horner J.R. On the origin of high growth rates in archosaurs and their ancient relatives: complementary histological studies on Triassic archosauriforms and the problem of a “phylogenetic signal” in bone histology. Ann. Paleontol. 2008; 94: 57-76 Crossref Scopus (137) Google Scholar ,8 Botha-Brink J. Smith R.M.H. Osteohistology of the Triassic archosauromorphs Prolacerta, Proterosuchus, Euparkeria, and Erythrosuchus from the Karoo Basin of South Africa. J. Vertebr. Paleontol. 2011; 31: 1238-1254https://doi.org/10.1080/02724634.2011.621797 Crossref Scopus (75) Google Scholar ,9 Klein N. Foth C. Schoch R.R. Preliminary observations on the bone histology of the Middle Triassic pseudosuchian archosaur Batrachotomus kupferzellensis reveal fast growth with laminar fibrolamellar bone tissue. J. Vertebr. Paleontol. 2017; 37: e1333121https://doi.org/10.1080/02724634.2017.1333121 Crossref Scopus (23) Google Scholar Large-bodied pseudosuchians in particular exhibit some of the fastest-growing bone types, giving evidence for prolonged, rapid growth. By contrast, early-branching crocodylomorphs, including a new large-bodied taxon, had slow maximum rates of bone deposition, as evidenced by the presence of predominantly parallel-fibered or lamellar bone tissue during middle-late ontogeny. Late Triassic crocodylomorphs show skeletal anatomy consistent with “active” terrestrial habits, 10 Walker A.D. A revision of Sphenosuchus acutus Haughton, a crocodylomorph reptile from the Elliot Formation (Late Triassic or Early Jurassic) of South Africa. Phil. Trans. R. Soc. Lond. B. 1990; 330: 1-120https://doi.org/10.1098/rstb.1990.0185 Crossref Google Scholar ,11 Colbert E.H. Mook C.C. The ancestral crocodile Protosuchus. Bull. Am. Museum Nat. Hist. 1951; 97: 147-182 Google Scholar ,12 Parrish J.M. The origin of crocodilian locomotion. Paleobiology. 1987; 13: 396-414https://doi.org/10.1017/S0094837300009003 Crossref Scopus (124) Google Scholar and their slow growth rates reject hypotheses linking this transition with sedentary, semiaquatic lifestyles or sprawling posture. Faster-growing pseudosuchian lineages go extinct in the Triassic, whereas slow-growing crocodylomorphs do not. This contrasts with the Jurassic radiation of fast-growing dinosaurs on the bird-stem lineage, 13 de Buffrénil V. de Ricqlès A.J. Zylberberg L. Padian K. Skeletal Histology and Paleohistology. CRC Press, 2021 Crossref Scopus (12) Google Scholar suggesting that the End-Triassic mass extinction initiated a divergent distribution of growth strategies that persist in present-day archosaurs.