Dinosaurs and the Cretaceous Terrestrial Revolution Graeme T. Lloyd*1, Katie E. Davis2, Davide Pisani3, James E. Tarver1, Marcello Ruta1, Manabu Sakamoto1, David W. E. Hone4,5, Rachel Jennings1 and Michael J. Benton1 1Department of Earth Sciences, University of Bristol, Wills Memorial Building, Queens Road, Bristol BS8 1RJ, UK; 2DEEB, FBLS, Graham Kerr Building, University of Glasgow, Glasgow G12 8QP, UK; 3Laboratory of Evolutionary Biology, Department of Biology, The National University of Ireland, Maynooth, Co. Kildaire, Ireland; 4Bayerischen Staatssammlung für Paläontologie und Geologie, Richard Wagner-Strasse 10, München 80333, Germany; 5Institute of Vertebrate Paleontology and Paleoanthropology, Xizhimenwai Daije 142,100044 Beijing, People’s Republic of China; Correspondence: [email protected]
Abstract Figure 2 (below). Majority-rule consensus tree of the reduced Baum Figure 4. A summary version of the supertree (figure 2) drawn against Basal Ornithischia (3)* and Ragan MRP matrix. Abbreviated clade names are: Mam. = stratigraphy. The 11 statistically significant diversification shifts Basal Thyreophora (3)* Huayangosaurus taibaii The observed diversity of dinosaurs reached its highest peak during the mid- and Late Mamenchisauridae, Br. = Brachiosauridae, Her. = present in both the entire tree (figure 2) and at least one Stegosauridae (11) Struthiosaurus austraicus Cretaceous, the 50Myr that preceded their extinction, and yet this explosion of dinosaur diversity Herrerasauridae, Compsog. = time-sliced tree are marked with white arrows denoting Ankylosauria (27) Stormbergia dangershoeki may be explained largely by sampling bias. It has long been debated whether dinosaurs were “Compsognathoidea”, Ornithomimo. = the branch leading to the more speciose clade. Heterodontosauridae (2) part of the Cretaceous Terrestrial Revolution (KTR), from 125–80Myr ago, when flowering plants, Ornithomimosauria, Therizino. = Taxa in bold represent the collapsing of a Pachycephalosauria (16) Basal Ceratopsia (18)* herbivorous and social insects, squamates, birds and mammals all underwent a rapid expansion. Therizinosauroidea, Alvar. = ia larger clade or group, the size of which Avaceratops lammersi Although an apparent explosion of dinosaur diversity occurred in the mid-Cretaceous, Alvarezsauridae and ch is indicated in parentheses. An ‘*’ Ceratopsidae (18) is Basal Euornithopoda (17)* coinciding with the emergence of new groups (e.g. neoceratopsians, ankylosaurid ankylosaurs, Troodon. = th ia indicates the collapsing of a Dryosauridae (2) ni tops Camptosaurus dispar hadrosaurids and pachycephalosaurs), results from the first quantitative study of diversification Troodontidae. r era Eu paraphyletic group and a ‘†’ Basal Iguanodontoidea (16)* O C orn Euhadrosauria (24) applied to a new supertree of dinosaurs show that this apparent burst in dinosaurian diversity in ith that of an extant clade Basal Sauropodomorpha (6)* the last 18 Myr of the Cretaceous is a sampling artefact. Indeed, major diversification shifts op (i.e. birds). Prosauropoda (14)* od Basal Sauropoda (18)* occurred largely in the first one-third of the group’s history. Despite the appearance of new a Neosauropoda (60) Basal Theropoda (5)* clades of medium to large herbivores and carnivores later in dinosaur history, these new Coelophysoidea (10) Chasmosaurus mariscalensis
Arrhinoceratops brachyops Arrhinoceratops Pachyrhinosaurus canadensis hongheensis Yandusaurus Neoceratosauria (15) originations do not correspond to significant diversification shifts. Instead, the overall geometry multidens Hexinlusaurus "Szechuanoraptor" zigongensis Pentaceratops sternbergii
Agilisaurus louderbacki Agilisaurus ia Einiosaurus procurvicornis Chasmosaurus irvinensis Megalosauroidea (14) of the Cretaceous part of the dinosaur tree does not depart from the null hypothesis of an equal Anchiceratopsornatus r Pachyrhinosaurus n. sp. Chasmosaurusrusselli Bagaceratops rozhdestvenskyi u Graciliceratops mongoliensis Styracosaurus albertensis Centrosaurus brinkmani horridus Triceratops Carnosauria (12) Achelousaurus horneri a hatcheri Diceratops rates model of lineage branching. Furthermore, we conclude that dinosaurs did not experience Zuniceratops christopheri s Montanoceratops cerorhynchus Chasmosaurusbelli o Protoceratops hellenikorhinus Basal Neotetanura (3)* Centrosaurus apertus l latus Torosaurus Udanoceratops tschizhovi Siamotyrannus isanensis a progressive decline at the end of the Cretaceous, nor was their evolution driven directly by the a Prenoceratops pieganensis Protoceratops andrewsiAvaceratops lammersi Monoclonius crassus h Yamaceratops dorngobiensis Tyrannosauroidea (15) p ‘Compsognathoidea’ (8) KTR. e LiaoceratopsArchaeoceratops yanzigouensis oshimaiLeptoceratops gracilis yc Psittacosaurus mongoliensis Scipionyx samniticus h Basal Coelurosauria (5)* c Psittacosaurus guyangensisPsittacosaurus sinensis Ornithomimosauria (11) a PachycephalosaurusPrenocephale wyomingensis edmontonensisChaoyangsaurus youngi P Xuanhuaceratops niei Basal Maniraptora (2) Sphaerotholus buchholtzae Oviraptorosauria (22) 20 Alvarezsauridae (5)
Othnielia rex Orodromeus makelai Zephyrosaurus schaffi Jeholosaurus shangyuanensis Hypsilophodon foxii Gasparinisaura cincosaltensis Prenocephale brevis Parksosaurus warreni Thescelosaurus neglectus Prenocephale goodwini Tenontosaurus dossi Gugyedong maniraptoran Tenontosaurus tilletti Excluded Trees: Included Trees: Muttabarrasaurus langdoni Rhabdodon priscus Zalmoxes robustus Zalmoxes shqiperorum Dryosaurus lettowvorbecki Dryosaurus altus Protarchaeopteryx robusta 18 Camptosaurus dispar Yinlong downsi Lurdusaurus arenatus Uncorroborated trees Independent trees Equijubus normani Stygimoloch spinifer Iguanodon bernissartensis Iguanodon atherfieldensis Eumaniraptora (26)† Ouranosaurus nigeriensis HomalocephaleDwarf calathocercos pachycephalosaur Fukuisaurus tetoriensis Redundant trees Dependent trees Tylocephale gilmorei Altirhinus kurzanovi Nanyangosaurus zhugeii Prenocephale prenes Jinzhousaurus yangi 16 Probactrosaurus gobiensis Eolambia caroljonesa Protohadros byrdi Bactrosaurus johnsoni 1 2 3 4 5 6 7 8 9 10 11 12 Gilmoreosaurus mongoliensis OrnatotholusStegoceras browni validum Telmatosaurus transsylvanicus 14 WannanosaurusGoyocephale yansiensis lattimorei Fontllonga euhadrosaur Lophorhothon atopus 225 200 175 150 125 100 75 Gryposaurus notabilis Brachylophosaurus canadensis Maiasaura peeblesorum Yaverlandia bitholus Edmontosaurus annectens P Time (Ma) 12 Edmontosaurus regalis Heterodontosaurus tucki Kerberosaurus manakini l StormbergiaAbrictosaurus Stenopelixdangershoeki consors valdensis Prosaurolophus maximus a e Naashoibitosaurus ostromi "Kritosaurus" australis t 10 a Nodocephalosaurus kirtlandensis Saurolophus osborni e Pararhabdodon isonensis d Tsintaosaurus spinorhinus o i PinacosaurusAnkylosaurus mephistocephalusSaichania magniventris chulsanensis Jaxartosaurus aralensis r Amurosaurus riabinini s 8 EuoplocephalusTarchia tutusgigantea Charonosaurus jiayinensis a u Parasaurolpohus walkeri u
N Source Trees a Lambeosaurus lambei Lambeosaurus magnicristatus r 6 s Corythosaurus casuarius i o TalarurusPinacosaurus plicatospineus grangeri Olorotitan arharensis a Dinosaur diversification: diversification shifts l Tsagantegia longicranialis Hypacrosaurus stebingeri Hypacrosaurus altispinus 4 y Tianzhenosaurus youngi Nipponosaurus sachalinensis k Saturnalia tupiniquim Thecodontosaurus antiquus n Shamosaurus scutatus Pantydraco caducus An alternative approach to analysing diversification is to compare 2 Gobisaurus domoculus Mussaurus patagonicus A Jingshanosaurus xinwaensis Efraasia minor observed tree shape with a null model. The simplest null model is Ammosaurus major 0 Polacanthus foxii Riojasaurus incertus equal-rates Markov (ERM), where all branches have the same GargoyleosaurusMymoorapelta parkpinorum maysi Lufengosaurus huenei 1984 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006 Animantarx ramaljonesiGastonia burgei "Gyposaurus" sinensis Minmi paravertebra Massospondylus carinatus probability of splitting resulting in a fully balanced tree. Significant 1985 1987 1989 1991 1993 1995 1997 1999 2001 2003 2005 Yunnanosaurus huangi Edmontonia rugosidens Plateosaurus gracilis Publication Year Plateosaurus cullingworthi excursions from stochastic variation around this model indicates a Edmontonia longiceps Coloradisaurus brevis Panoplosaurus mirus Plateosaurus engelhardti more complex two-parameter model, where, following a split, one Figure 1. Filtering of source trees results in decreased redundancy Unaysaurus tolentinoi SauropeltaSilvisaurus edwardsorum condrayi Anchisaurus polyzelus and a strong skew towards more recent analyses. Uncorroborated Pawpawsaurus campbelli Melanorosaurus readi branch shows a greater probability of splitting than the other. This Cedarpelta bilbeyhallorum Camelotia borealis Lessemsaurus sauropoides M is a diversification shift (Chan and Moore 2005). Here 11 trees lack a numerical cladistic analysis and redundant trees have e Hylaeosaurus armatus Blikanasaurus cromptoni a a Antetonitrus ingenipes m significant shifts (which were also found on time-sliced trees, a been superceded by more recent work. Independent trees StruthiosaurusHungarosaurus austriacus tormai Gongxianosaurus shibeiensis d Isanosaurus attavipachi . i way of testing a potential bias in the assumptions of the ERM r Tazoudasaurus naimi represent a unique combination of taxa and characters, whereas Stegosaurus stenops Kotasaurus yamanpalliensis u LexovisaurusStegosaurus durobrivensis armatus Vulcanodon karibaensis model) were discovered. These are shown in figure 4 as arrows dependent trees have equal claim to novelty with at least one a Kentrosaurus aethiopicus Shunosaurus lii s Tuojiangosaurus multispinus Barapasaurus tagorei indicating the more speciose branch following the shift. These other analysis. o Mamenchisaurus constructus Omeisaurus junghsiensis S g Hesperosaurus mjosi Omeisaurus yianfuensis are concentrated early in dinosaur evolution. An alternative e Dacentrurus armatus Patagosaurus fariasi t Wuerhosaurus homheni Cetiosaurus oxoniensis a way of showing this is to plot the mean likelihood of the S ChungkingosaurusChialingosaurus jiangbeiensis kuani Losillasaurus giganteus Zapalasaurus bonapartei u two-parameter model through time (figure 5). This shows that Jobaria tiguidensis Supertree Construction Paranthodon africanus Haplocanthosaurus priscus diversification was furthest from the ERM model in the Early Huayangosaurus taibaii Amphicoelias altus r Scelidosaurus harrisonii Limaysaurus tessonei D
o Jurassic and closest during the Cretaceous. Emausaurus ernsti Nigersaurus taqueti i A novel formal supertree was produced and used as a Scutellosaurus lawleri Rayososaurus agrioensis p
Rebbachisaurus garasbae l Lesothosaurus diagnosticus p Suuwassea emilieae o framework to investigate different metrics of diversification in Amargasaurus cazaui Eocursor parvus d
Pisanosaurus mertii Brachytrachelopan mesai o non-avian dinosaurs. Here, new source tree filtering methods Dicraeosaurus hansemanni o
Dinheirosaurus lourinhanensis c
D Atrociraptor marshalli d were used to reduce redundancy and ensure that source trees Tornieria africana o
Barosaurus lentus Dinosaur diversification: the Cretaceous Terrestrial r Deinonychus antirrhopus
i o Diplodocus longus d represented current consensus as far as possible (figure 1). Bambiraptor feinbergorum Apatosaurus louisae o Revolution
m Velociraptor mongoliensis e Tsaagan mangas Apatosaurus sp.
Multiple supertree algorithms were then employed to combine Apatosaurus ajax a a Saurornitholestes langstoni Apatosaurus excelsus m source trees in different ways, but we found that the Baum and e Utahraptor ostrommaysi Apatosaurus parvus The removal of a Late Cretaceous diversification peak by o Atlasaurus imelakei
Dromaeosaurus albertensis Haplocanthosaurus delfsi Ragan MRP method produced the best representation of the o s Achillobator giganticus Camarasaurus supremus subsampling and the better fit of an ERM model during the original source trees (by the V1 index of Wilkinson et al. 2005). a Adasaurus mongoliensis Amazonsaurus maranhensis u Cretaceous indicate relatively quiescent speciation during this
Buitreraptor gonzalezorum Brachiosaurus brancai r r Europasaurus holgeri
A manual reduced consensus approach was then used to remove Sinornithosaurus millenii i Lapparentosaurus madagascarensis p interval. This contrasts strongly with the pattern from other d Microraptor zhaoianus Brachiosaurus altithorax taxa that were phylogenetically unstable in order to obtain a tree Cedarosaurus weiskopfae
a Neuquenraptor argentinus terrestrial clades (e.g. herbivorous and social insects, squamates, Datousaurus bashanensis h e Euhelopus zdanskyi
that more closely represented complete bifurcation. The resulting SaurornithoidesSaurornithoidesTroodon mongoliensis formosus junior Tehuelchesaurus benitezii birds and mammals) that show major diversifications at this time Antarctosaurus wichmannianus a tree of 420 species is shown in figure 2. Byronosaurus jaffei Quaesitosaurus orientalis following the origin and radiation of angiosperms, an event we T Sinornithoides youngi Rapetosaurus krausei . r Dornogov troodontidMei long Nemegtosaurus mongoliensis r o term the Cretaceous Terrestrial Revolution (KTR). Direct evidence Sinovenator changii Bellusaurus sui B Phuwiangosaurus sirindhornae o Andesaurus delgadoi of dinosaurian diet (gut contents, coprolites) already suggests that d Pleurocoelus nanus Jinfengopteryx elegans Ampelosaurus atacis o Rahonavis ostromi Agustinia ligabuei dinosaurs did not adapt to feed exclusively on angiosperms and we Dinosaur diversification: taxon counting methods n Archaeopteryx lithographica Paralititan stromeri . Epachthosaurus sciuttoi conclude that dinosaurs did not participate in the KTR. Unenlagia comahuensis Austrosaurus mckillopi Malawisaurus dixeyi A Protarchaeopteryx robusta Gondwanatitan faustoi GugyedongParvicursor maniraptoran remotus Isisaurus colberti Three taxon-counting methods were used to look at a simple metric of v Shuvuuia deserti Titanosaurus indicus e Mononykus olecranus Alamosaurus sanjuanensis s Pellegrinisaurus powelli diversification (% change in species richness per million years). The first Patagonykus puertai Argyrosaurus superbus AlvarezsaurusIngenia yanshini calvoi Rocasaurus muniozi References cited involved counts of raw data taken from The Dinosauria II (Weishampel et Japalpur titanosaur indet. Malagasy Taxon B ConchoraptorKhaan mckennaigracilis Saltasaurus loricatus al. 2004), the second used the supertree to add ghost ranges to this data Aeolosaurus rionegrinus A Oviraptor philoceratops Toba titanosaur a Chan, K. M. and Moore, B. R., 2005. Bioinformatics, 21, 1709-1710. Citipati osmolskae Argentinosaurus huinculensis i and the third used a subsampling approach whereby the data were l Opisthocelocaudia skarzynskii v Peiropolis titanosaur r Weishampel, D. B. et al., 2004. The Dinosauria (Second Edition). a Lirainosaurus astibiae u resampled 1,000 times and the number of species present in 36 occurrences Microvenator celer Staurikosaurus pricei r Rinchenia mongoliensis Herrerasaurus ischigualastensis a University of California Press, Berkeley. . Kamyn KhondtNomingia oviraptorine gobiensis Chindesaurus bryansmalli s tallied. This last count represents a way of artifically setting the global quality Eoraptor lunensis El Brete oviraptor Guabiasaurus candelariensis o O Sarcosaurus woodi Wilkinson, M. et al., 2005. Systematic Biology, 54, 823-831. Caudipteryx zoui Zupaysaurus rougieri n of the record as equal to the worst part. The results are shown in figure 3, with ChirostenotesAvimimus portentosuspergracilis Dilophosaurus wetherilli a v Gojirasaurus quayi t i Lophostropheus airelensis i the raw and ghost-range corrected data showing increased diversification in the r Liliensternus lilliensterni Procompsognathus triassicus T a Incisivosaurus gauthieri Syntarsus rhodesiensis Full publication Coelophysis bauri Late Triassic, Middle Jurassic and Late Cretaceous and decreased diversification in p Erlikosaurus andrewsi Segisaurus halli Segnosaurus galbinensis Elaphrosaurus bambergi t Ceratosaurus nasicornis o Spinostropheus gautieri Velocisaurus unicus the Early Jurassic and Early Cretaceous. However, all peaks and troughs are r Xenotarsosaurus bonapartei Falcarius utahensis Rugops primus o Masiakasaurus knopfleri Lloyd, G. T. et al., 2008. Proceedings of the Royal Society B, 275, 2483-2490. Eshanosaurus deguchiianus Noasaurus leali Beipiaosaurus inexpectus Ilokelesia aguadagrandensis removed by subsampling, suggesting minimally that the dinosaur record is seriously s EnigmosaurusNothronychus mongoliensis mckinleyi Abelisaurus comahuensis a Aucasaurus garridoi Quarry 9 coelurosaur Carnotaurus sastrei Bajo Barreal abelisaur u Bagaraatan ostromi Lameta abelisaur biased by sampling and maximally that the true picture is one of near constant diversity Majungasaurus crenatissimus "Szechuanoraptor" zigongensis r Afrovenator abakensis Ornithomimus velox Piatnitzkysaurus floresi i Xinjiangovenator parvus Megalosaurus bucklandi Poekilopleuron bucklandii a Torvosaurus tanneri implying a logistic model of species richness. Struthiomimus altus Dubreuillosaurus valesdunensis Eustreptospondylus oxoniensis "Megalosaurus" hesperis Gallimimus bullatus Chilantaisaurus tashuikouensis Cristatusaurus lapparenti Baryonyx walkeri Suchomimus tenerensis Irritatorchallengeri Spinosaurus aegypticus Nanshinungosaurus brevispinus Lourinhanosaurusantunesi Monolophosaurusjiangi Cryolophosaurus ellioti Cryolophosaurus Sinraptor dongi Sinraptor Yangchuanosaurusshangyouensis Allosaurus fragilis Allosaurus Acrocanthosaurus atokensis Acrocanthosaurus salerii Neovenator T chubutensis Tyrannotitan h Coelurus fragilis 0.7 e Ornithomimus Sinornithomimusedmontonicus dongi . r AnserimimusGarudimimus planinychus brevipes r iz e in Harpymimus okladnikoviDeltadromeus agilis H Pelecanimimus polyodon 0.6 12.0% o ArchaeornithomimusShenzhousaurus asiaticusOrnitholestes orientalis hermanni . Scipionyx samniticus ProceratosaurusMirischia bradleyi asymmetrica . Aristosuchus pussilus s Tarbosaurus bataar y 0.5 Sinosauropteryx prima Tyrannosaurus rex Compsognathus longipes Eotyrannus lengi h O Xuanhanosaurus qilixiaensis Nqwebasaurus thwazi Guanlong wucaii p Huaxiagnathus orientalis Alioramus remotus 8.0% r Gasosaurus constructus Dilong paradoxus o Gorgosaurus libratus l n Nanotyrannus lancensis Alectrosaurus olseni
Mapusaurus roseae e i Nedcolberti justinhofmanniDaspletosaurus torosus Figure 3. th Tugulusaurus faciles Co 0.4 om Stokesosaurus clevelandi Siamotyrannus isanensis
Giganotosaurus carolinii Figure 5. Diversification i Albertosaurus sarcophagus Dryptosaurus aquilunguis m Fukuiraptor kitadaniensis o Two Medicine tyrannosaurine ria 0.3 4.0% rates based on the . au M e a n os values of the raw record (blue Magnosaurus nethercombensis t Carcharodontosaurus saharicus ra Appalachiosaurus montgomeriensis ce Delta-2 shift 0.2 line), the raw record Co eo 0.0% plus additional ghost ranges m N statistic through time. ps Mean Delta-2 shift statistic og a Higher values indicate a 0.1 % change in diversity/m.y. % change e (green line) and subsampled . Ty oid ran saur better fit of the two-parameter data (red line, including 95% C.I.). Th nosau egalo -4.0% e roidea ria M model, i.e. a higher likelihood of a 0 3 4 5 6 7 8 9 10 11 12 Boxes 1-12 are approximately r Carnosau 1 2 3 4 5 6 7 8 9 10 11 12 o diversification shift. Lower values equal-length time bins made by clumping po 225 200 175 150 125 100 75 200 175 150 125 100 75 geologic stages together. da indicate preference of the one-parameter Time (Ma) (equal-rates Markov) model. Time (Ma)