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Growth and miniaturization among alvarezsauroid dinosaurs

2021; Elsevier BV; Volume: 31; Issue: 16 Linguagem: Inglês

10.1016/j.cub.2021.06.013

1879-0445

Zichuan Qin, Qi Zhao, Jonah N. Choiniere, James M. Clark, Michael J. Benton, Xing Xu,

Amphibian and Reptile Biology

Sustained miniaturization, here defined as a drop in body size of at least two orders of magnitude from ancestors to descendants, is a widespread and important phenomenon in animals,1Lee M.S.Y. Cau A. Naish D. Dyke G.J. Dinosaur evolution. Sustained miniaturization and anatomical innovation in the dinosaurian ancestors of birds.Science. 2014; 345: 562-566Crossref PubMed Scopus (167) Google Scholar, 2Hanken J. Wake D.B. Miniaturization of body size: organismal consequences and evolutionary significance.Annu. Rev. Ecol. Syst. 1993; 24: 501-519Crossref Scopus (363) Google Scholar, 3Puttick M.N. Thomas G.H. Benton M.J. High rates of evolution preceded the origin of birds.Evolution. 2014; 68: 1497-1510Crossref PubMed Scopus (55) Google Scholar but among dinosaurs, miniaturization occurred only rarely, once in the lineage leading to birds and once in the Alvarezsauroidea,1Lee M.S.Y. Cau A. Naish D. Dyke G.J. Dinosaur evolution. Sustained miniaturization and anatomical innovation in the dinosaurian ancestors of birds.Science. 2014; 345: 562-566Crossref PubMed Scopus (167) Google Scholar,3Puttick M.N. Thomas G.H. Benton M.J. High rates of evolution preceded the origin of birds.Evolution. 2014; 68: 1497-1510Crossref PubMed Scopus (55) Google Scholar, 4Brusatte S.L. Lloyd G.T. Wang S.C. Norell M.A. Gradual assembly of avian body plan culminated in rapid rates of evolution across the dinosaur-bird transition.Curr. Biol. 2014; 24: 2386-2392Abstract Full Text Full Text PDF PubMed Scopus (189) Google Scholar, 5Benson R.B.J. Hunt G. Carrano M.T. Campione N. Cope's rule and the adaptive landscape of dinosaur body size evolution.Palaeontology. 2018; 61: 13-48Crossref Scopus (94) Google Scholar one of the most bizarre theropod groups.1Lee M.S.Y. Cau A. Naish D. Dyke G.J. Dinosaur evolution. Sustained miniaturization and anatomical innovation in the dinosaurian ancestors of birds.Science. 2014; 345: 562-566Crossref PubMed Scopus (167) Google Scholar,5Benson R.B.J. Hunt G. Carrano M.T. Campione N. Cope's rule and the adaptive landscape of dinosaur body size evolution.Palaeontology. 2018; 61: 13-48Crossref Scopus (94) Google Scholar, 6Benson R.B.J. Campione N.E. Carrano M.T. Mannion P.D. Sullivan C. Upchurch P. Evans D.C. Rates of dinosaur body mass evolution indicate 170 million years of sustained ecological innovation on the avian stem lineage.PLoS Biol. 2014; 12: e1001853Crossref PubMed Scopus (251) Google Scholar, 7Bonaparte J.F. Los vertebrados fósiles de la Formación RíoColorado, de la ciudad de Neuquén y cercanías, Cretácico superior, Argentina.Rev. Museo Argent. Ciencias Naturales. "Bernardino Rivadavia". Paleontologia. 1991; 4: 15-123Google Scholar Miniaturization and powered flight are intimately linked in avialan theropods,3Puttick M.N. Thomas G.H. Benton M.J. High rates of evolution preceded the origin of birds.Evolution. 2014; 68: 1497-1510Crossref PubMed Scopus (55) Google Scholar,5Benson R.B.J. Hunt G. Carrano M.T. Campione N. Cope's rule and the adaptive landscape of dinosaur body size evolution.Palaeontology. 2018; 61: 13-48Crossref Scopus (94) Google Scholar,6Benson R.B.J. Campione N.E. Carrano M.T. Mannion P.D. Sullivan C. Upchurch P. Evans D.C. Rates of dinosaur body mass evolution indicate 170 million years of sustained ecological innovation on the avian stem lineage.PLoS Biol. 2014; 12: e1001853Crossref PubMed Scopus (251) Google Scholar,8Turner A.H. Pol D. Clarke J.A. Erickson G.M. Norell M.A. A basal dromaeosaurid and size evolution preceding avian flight.Science. 2007; 317: 1378-1381Crossref PubMed Scopus (245) Google Scholar, 9Xu X. Zhou Z. Dudley R. Mackem S. Chuong C.-M. Erickson G.M. Varricchio D.J. An integrative approach to understanding bird origins.Science. 2014; 346: 1253293Crossref PubMed Scopus (195) Google Scholar, 10Rezende E.L. Bacigalupe L.D. Nespolo R.F. Bozinovic F. Shrinking dinosaurs and the evolution of endothermy in birds.Sci. Adv. 2020; 6: eaaw4486Crossref PubMed Scopus (17) Google Scholar, 11Legendre L.J. Davesne D. The evolution of mechanisms involved in vertebrate endothermy.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2020; 375: 20190136Crossref PubMed Scopus (43) Google Scholar but the causes and patterns of body size reduction are less clear in the non-volant Alvarezsauroidea.1Lee M.S.Y. Cau A. Naish D. Dyke G.J. Dinosaur evolution. Sustained miniaturization and anatomical innovation in the dinosaurian ancestors of birds.Science. 2014; 345: 562-566Crossref PubMed Scopus (167) Google Scholar,5Benson R.B.J. Hunt G. Carrano M.T. Campione N. Cope's rule and the adaptive landscape of dinosaur body size evolution.Palaeontology. 2018; 61: 13-48Crossref Scopus (94) Google Scholar,6Benson R.B.J. Campione N.E. Carrano M.T. Mannion P.D. Sullivan C. Upchurch P. Evans D.C. Rates of dinosaur body mass evolution indicate 170 million years of sustained ecological innovation on the avian stem lineage.PLoS Biol. 2014; 12: e1001853Crossref PubMed Scopus (251) Google Scholar,12Nesbitt S.J. Clarke J.A. Turner A.H. Norell M.A. A small alvarezsaurid from the eastern Gobi Desert offers insight into evolutionary patterns in the Alvarezsauroidea.J. Vertebr. Paleontol. 2011; 31: 144-153Crossref Scopus (34) Google Scholar,13Qin Z. Clark J. Choiniere J. Xu X. A new alvarezsaurian theropod from the Upper Jurassic Shishugou Formation of western China.Sci. Rep. 2019; 9: 11727Crossref PubMed Scopus (17) Google Scholar Here, we present results from analyses on a comprehensive dataset, which not only includes new data from early-branching alvarezsauroids but also considers the ontogenetic effect based on histological data. Our analyses show that alvarezsauroid body mass underwent rapid miniaturization from around 110 to 85 mya and that there was a phylogenetic radiation of small-sized alvarezsauroids in the Late Cretaceous. Our analyses also indicate that growth strategies were highly variable among alvarezsauroids, with significant differences among extremely small taxa. The suggested alvarezsauroid miniaturization and associated phylogenetic radiation are coincident with the emergence of ants and termites, and combining previous functional morphological data, our study suggests that alvarezsauroid miniaturization might have been driven by ecological changes during the Cretaceous Terrestrial Revolution, more specifically by a shift to the myrmecophagous ecological niche.