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Home , Abrictosaurus, Aeolosaurus, Alvarezsauridae, Alvarezsaurus, Alxasaurus, Anserimimus

Received 24 September 2001 Accepted 3 December 2001 Published online 9 April 2002

A -level supertree of the Dinosauria Davide Pisani1,2*, Adam M. Yates1, Max C. Langer1 and Michael J. Benton1 1Department of Earth Sciences, University of Bristol, Bristol BS8 1RJ, UK 2Department of Zoology, The Natural History Museum, Cromwell Road, SW7 5BD, UK One of the ultimate aims of systematics is the reconstruction of the tree of life. This is a huge undertaking that is inhibited by the existence of a computational limit to the inclusiveness of phylogenetic analyses. Supertree methods have been developed to overcome, or at least to go around this problem by combining smaller, partially overlapping . Here, we present a very inclusive generic-level supertree of Dinosauria (covering a total of 277 genera), which is remarkably well resolved and provides some clarity in many contentious areas of systematics. Keywords: supertrees; phylogeny; ; ;

1. INTRODUCTION tations of the information conveyed by the trees in the input set. In the last few decades, advances in theoretical system- The original MRP method of Baum (1992) and Ragan atics, as well as in computer sciences, have provided bio- (1992), referred to as component coding-MRP (CC- logists and palaeontologists with tools to investigate the MRP) in this paper, was used to combine 126 `partial phy- phylogenetic relationships among organisms, yet phylo- logenies’ of dinosaurs (covering a total of 277 genera) with genetic inference is computationally expensive and analy- the aim of obtaining a single, genus-level supertree. CC- ses of large datasets hardly feasible (Graham & Foulds MRP makes use of the fact that a tree can be represented 1982). This problem is exacerbated in palaeontology, in a matrix by means of a set of binary `characters’. Fol- where missing data can lead to an exponential increase in lowing Baum & Ragan (1993), we refer to these `charac- the number of most-parsimonious solutions permitted by ters’ as matrix elements. Matrix representations of a given dataset. However, `partial phylogenies’ (i.e. phy- different source trees can be readily combined with miss- logenies including only a subset of the taxa known to ing entries in the matrix elements corresponding to taxa belong to a certain group) are accumulating at an increas- that are not present in the matching source tree. Parsi- ing rate, and the Dinosauria represent a typical, if not mony analysis of the combined matrix representations extreme, example of this trend. yields one or more most parsimonious trees (MPTs), the Supertree methods, formally introduced by Gordon CC-MRP supertree(s), which comprise all the included (1986), can be implemented to combine such `partial phy- taxa (see Baum 1992; Ragan 1992 for more details). logenies’ and obtain more inclusive estimates without the need to pool the original datasets. Accordingly, whenever a collection of `partial phylogenies’ exists, supertrees can 2. MATERIAL AND METHODS represent an alternative to a direct analysis of the primary Potential source trees were identi® ed from online searches. data (i.e. the pooled dataset). Two electronic literature databases were searched for publications Several supertree methods have been developed (e.g. with relevant source trees, BFV (Bibliography of Fossil Verte- Sanderson et al. 1998; Wilkinson et al. 2001 for review), brates) online (http://eteweb.lscf.ucsb.edu/bfv/bfv_form.html) but only those using matrix representation with parsimony and Web of Science (http://wos.mimas.ac.uk/). BFV online does (MRP methods) have software implementation (Swofford not allow the enquirer to con® ne his search to a limited number 1998; Thorley & Page 2000) and these are currently the of and it was thus screened over the whole time-span that only viable choice in supertree reconstruction. Neverthe- it covers (1509± 1993), while Web of Science was searched for less, their characterization is still incomplete. In particular, the years 1993± 2001. All publications that were likely to include when the source trees are incompatible (i.e. they disagree a were examined. Because the aim of this analysis about the relationships of the taxa that overlap), their was to obtain a consensus representation of cladistic views on behaviour is not completely understood. In these cases, dinosaur systematics, the earliest of which date back to the MRP methods can be inaccurate. It is debatable whether beginning of the 1980s (Benton 1990), publications presented MRP estimates are accurate enough to be useful tree- before the 1980 have been excluded a priori. Publications reconstruction methods (Purvis 1995a; Wilkinson et al. after this date were retained when they presented cladogram(s) 2001). Yet, there is evidence (Bininda-Emonds & San- resulting from an original study, or from the modi® cation of a derson 2001) that, if the set of source trees is large pre-existing dataset. The list of all retained publications is avail- enough, the MRP supertree(s) are accurate represen- able (see electronic appendix). For each selected cladogram, a Nexus (Swofford 1998) tree ® le was produced using MacClade (Maddison & Maddison 1997). Some terminal genera were omitted a priori (see electronic appendix, available on The Royal * Author for correspondence ([email protected]). Society’s Publications Web site, for the list of the omitted taxa).

Proc. R. Soc. Lond. B (2002) 269, 915± 921 915 Ó 2002 The Royal Society DOI 10.1098/rspb.2001.1942 916 D. Pisani and others A supertree of Dinosauria

These were either nomina dubia, unconstrained taxa, or both. of support, following Bininda-Emonds et al. (1999) and Liu et The former are taxa based on material inadequate for diagnosis al. (2001), decay indices (Bremer 1988) are provided. Decay and for proper phylogenetic analysis. The latter may be valid values have been calculated for Matrices II± IV, but because of taxa but they appear only in one source tree and as members the size of the resulting supertree, they have not been calculated of a polytomy. Accordingly, their inclusion adds nothing to the for Matrix I. However, it is our opinion that this measure cannot analysis but an increase in the number of possible MPTs. Most be considered really representative of the support for the original studies included a variable proportion of suprageneric recovered by the supertree. Accordingly, decay values should be terminal taxa. For analytical proposes, their was interpreted with care. Consider, for example, that novel clades assumed and a standard substitution (Wilkinson et al. (sensu Bininda-Emonds & Bryant 1998), despite being unsup- 2001) was performed. Each suprageneric taxon was substituted ported (Pisani & Wilkinson 2002), have a positive decay index. with a star tree (i.e. an unresolved polytomy) including either: Thus, new support measures for MRP supertrees are needed (i) the taxa embodied in each of them when explicitly given in and are under development (D. Pisani, unpublished data), but the original study; or (ii) only its non-controversial members in they will not be considered any further in this paper. the case that no such de® nition was given (see electronic appen- dix for the minimal non-controversial de® nition of each supra- 3. RESULTS generic taxon). When multiple MPTs were presented, strict reduced consensus (RC; Wilkinson 1994) was implemented A total of 34 900 MPTs was found from the analysis of using RadCon (Thorley & Page 2000) and the tree in the RC Matrix I before the search had to be aborted because of pro® le with the highest cladistic information content (Thorley memory limitations. We suggest that this sample of et al. 1998) was retained for the CC-MRP analysis. MPTs, although less than the set of all possible supertrees, Five CC-MRP matrices (see electronic appendix), one scoring is representative of the whole. This is because the topology all of the 277 included taxa (Matrix I), one for Sauropodomor- of their strict consensus agrees perfectly with those of the pha (Matrix II), one for (Matrix III) and two for strict consensus trees summarizing the results obtained (Matrices IV and V) were produced using RadCon. from the compartmentalized analyses (Matrices II, III and These have been analysed separately, resulting in one compre- V), which have been run to completion. It is thus possible hensive (Matrix I) and four compartmentalized (Matrices II± V) to argue that increasing the number of retained MPTs supertrees. It is important to note that Matrices II± V are matr- from the analysis of Matrix I will result in a more compre- ices in their own right, not subsamples of Matrix I. They have hensive collection of alternative solutions for the polytom- not been obtained by pruning the excluded taxa, e.g. all thero- ies seen in ® gure 2 and not in the collapse of its resolved pods and all ornithischians (in the case of Matrix II) from Matrix areas. The strict consensus of the 34 900 MPTs from the I, but by pruning the source trees and then recoding them in a analysis of Matrix I (® gure 2) therefore represents the new CC-MRP matrix. This approach, implemented here for the most inclusive estimate that has ever, to our knowledge, ® rst time, to our knowledge, is important because each matrix been presented of the phylogeny of the Dinosauria. element is representative of a node in a tree. Thus, pruning a Contentious issues in dinosaur systematics are resolved taxon from an MRP matrix will create a matrix that is not rep- in the present supertree. is composed resentative of the real topology of the pruned tree (® gure 1). of Saturnalia and monophyletic Prosauropoda and Sauro- Because objective functions for implementing a correct, poda (Sereno 1999; Benton et al. 2000; contra Gauthier unequal character-weighting scheme in MRP analyses are still 1986). Within Prosauropoda, a monophyletic Melanoro- unknown (Bininda-Emonds et al. 1999; Bininda-Emonds & sauridae (, and ) Sanderson 2001), equally weighted parsimony was used to ana- emerges as the of (Masso- lyse the ® ve CC-MRP matrices. spondylus, and ). Within

Paup¤ (Swofford 1998) was used to analyse the data matrices , is the sister group to all other with parsimony and, in to avoid the problem of being (Upchurch 1998; contra Wilson & Sereno `bogged down’ in sub-optimal tree islands, the following tree- 1998) and is more closely related to Neosauro- search protocol was applied: (1) 100 heuristic searches were poda than it is to (Wilson & Sereno 1998; carried out using tree bisection± reconnection (TBR) branch contra Upchurch 1998). The early dinosaurs and swapping with the `multrees’ option not in effect; random step- the are theropods (Sereno et al. wise addition was used to obtain the starting trees for these repli- 1993; contra Langer et al. 1999). is a mono- cates; (2) the MPTs found were retained and swapped using phyletic group containing and Neocerato- TBR branch swapping with the `multrees’ option in effect. (Sereno 1999; Holtz 2000; contra Forster 1999), A potentially serious problem of MRP supertree methods is while torvosaurids are more closely related to derived their ability to resolve con¯ ict among the source trees by the tetanurans () than to spinosaurids (Holtz generation of novel clades (sensu Bininda-Emonds & Bryant 2000; contra Sereno et al. 1994). Therizinosauroidea is the 1998). Bininda-Emonds et al. (1999) and Bininda-Emonds & sister group of (Russell & Dong 1993; Sanderson (2001) have likened the appearance of such clades in Holtz 2000; contra Sereno 1999), but is a MRP to their appearance in Total Evidence analyses. However, basal member of : it is excluded from both Ovira- as shown by Pisani & Wilkinson (2002), this cannot be the case ptorosauria (contra Sereno 1999) and (contra Ji and such novel clades should always be collapsed. No novel et al. 1998), while Metornithes is monophyletic and con- clades (sensu Bininda-Emonds & Bryant 1998) are present in the tains , (Chatterjee 1991; contra dinosaur supertree. Holtz 1994) and (Chiappe et al. 1996; A poorly understood problem in MRP supertree building is contra Sereno 1999). how to evaluate the support for the resulting clades. For those Within Ornithischia, Minmi and Gargoyleosaurus are who feel that an MRP supertree is naked without some measure basal Ankylosauridae (Sereno 1999; contra Kirkland

Proc. R. Soc. Lond. B (2002) A supertree of Dinosauria D. Pisani and others 917

(tree A) (tree B) A B C D E F A B C E F

node 1 node 1 node 2 node 3 node 3 pruning taxon D node 4 node 4

CC-MRP representation of tree A CC-MRP representation of tree B

nodes: N1 N2 N3 N4

A 0 0 0 0 B 0 0 0 1 C 0 0 1 1 The deletion of taxon D implies the D 0 1 1 1 E 1 1 1 1 suppression of node 2. F 1 1 1 1 Accordingly, the corresponding matrix element (N2) is not present in the correct CC-MRP representation Matrix obtained when pruning of tree B. taxon D from the CC-MRP representation of tree A (i.e. using the PAUP option ‘Delete-

Restore taxa’). Note that the

new matrix is not a correct CC- MRP representation of tree B.

nodes: N1 N2 N3 N4 nodes: N1 N3 N4

A 0 0 0 0 A 0 0 0 B 0 0 0 1 B 0 0 1 C 0 0 1 1 C 0 1 1 E 1 1 1 1 E 1 1 1 F 1 1 1 1 F 1 1 1

Figure 1. A tree on six (tree A) and its corresponding pruned version (tree B), from which taxon D has been deleted. Pruning taxon D from the CC-MRP representation of tree A results in a matrix that is not the correct CC-MRP matrix representing tree B.

1998). A monophyletic (Norman 1998; three long-necked Chinese taxa, Omeisaurus, Mamenchi- contra Sereno 1999) containing , Altirhinus and saurus and , and to the poorly constrained pos- is recovered, while the Hadrosauridae ition of . The ® rst problem re¯ ects differences appears more closely related to than to in the results obtained by different authors on the relation- Iguanodontidae. Leptoceratops and Udanoceratops are ships of those taxa. Among the source trees, two classes excluded from Coronosauria (Protoceratopsidae plus of cladogram exist. Upchurch (1995, 1998) includes all Ceratopsoidea) and a monophyletic Protoceratopsidae three Chinese taxa in a nested outside Neosauro- containing Bagaceratops, Breviceratops, Graciliceratops and poda, while Wilson & Sereno (1998; also Sereno 1999) is recovered (Sereno 2000; contra Chinnery & do not include and consider Omeisaurus Weishampel 1998). and Euhelopus to be distantly related. In the supertree, The present supertree contains three important poly- Omeisaurus and Euhelopus are nested according to the tomies. One lies within Sauropoda and the other two second of these two hypotheses, but Mamenchisaurus is within Theropoda: one at the base of and free to cluster with either of the two. Implementing RC, the other within Coelurosaria, at the base of the Eumanir- two `rogue’ taxa (Cetiosaurus and Mamenchisaurus) are aptora. identi® ed. With their exclusion (® gure 3a), the following The polytomy within Sauropoda involves the taxa more taxonomic statements are true in all the supertrees: (i) derived than Shunosaurus and is due to both the existence falls within (de® ned by of con¯ icting hypotheses concerning the relationships of the node connecting and ) and is

Proc. R. Soc. Lond. B (2002) 918 D. Pisani and others A supertree of Dinosauria

Saturnalia 1 P

Melanorosaurus r 1 1 o 1 Riojasaurus s 7 a

1 Camelotia u

1 Yunnanosaurus r o

Massospondylus p o 1 d

Lufengosaurus a 1 Riojasaurus 1 Sellosaurus 1 1 1 Barapasaurus Shunosaurus 1 Omeisaurus Mamenchisaurus 1 Cetiosaurus 1 Haplocantosaurus Gongbusaurus 2 1 Euhelopus D 2 i a p i 1 l r

Dacentrurus 1 o

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a Toujiangosaurus

1 o s 3

Lexovisaurus c o 1 2 o g Stegosaurus 2 i e 1 d t Wuerhosaurus

Barosaurus e S 1

Kentrosaurus a 1 Diplodocus Apatosaurus Pawpawsaurus 2 2 1 3 Silvisaurus 1

2 T a 4

i 2 1 i r t

Gargoyleosaurus a u n a Minmi 1 Opisthocoelocaudia

s 1 o 1 Peiropolis titanosaur o Shamosaurus 1 s l Tsagantegia a

y 1 1 1 u k r i n 1 Mymoorapelta a A 2 1 1 Saltasaurus Opistocelicaudia 1 Pinacosaurus 1 Nequensaurus Euoplocephalus Eoraptor 2 1 Tarchia 9 1 2 Nodocephalosaurus a 3 1 i r 2 2 u a 1 C s 2

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l 1 7 4 Syntarsus r a Ornatotholus 3 a h 3 t o p s e 1 a c 2 1 i Dwarf pachicephalosaur 2 3 u

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P Noasaurus Stygimoloch 1 1 15 Abelisaurus Chaoyangsaurus S e 4 Majungatholus p a Archaeoceratops 1 i

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a

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Harpymimus n a Probactrosaurus 3 i u

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I 1

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Gilmoreosaurus 2 1 m

Eolambia 1 i m 1 1 1 o Pararabdodon 1 s 1 a 1 1 u

Charonosaurus 1 1 r

1 i a e 1 Dromiceomimus a Quarry 9 coelurosaur d 2 i 2 Galimimus r 4 u O a

s v 2 1 1 o Aralosaurus i r r 2

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Sinornithoides a n

1 i r

Troodon a 1 p 1 t o

1 r

Ornithothoraces a Avimimus Rahonavis 1 1 1 Hell Creek alvaresaurid 1 Parvicursor 1

Proc. R. Soc. Lond. B (2002) A supertree of Dinosauria D. Pisani and others 919

(a) Shunosaurus Omeisaurus Patagosaurus Camarasaurus Haplocanthosaurus Euhelopus Phuwiangosaurus Nemegtosaurus Quaesitosaurus Chubutisaurus

(b) Coelurus Proceratosaurus Ornitholestes Scipionyx Bagarataan Sinosauroptreryx Compsognathus Oviraptosauria Eumaniraptoria

Figure 3. (a) Reduced consensus of the 14 323 MPTs of length 356 obtained from the analyses of Matrix II. (b) Reduced consensus of the 85 900 MPTs of length 910 obtained from the analysis of Matrix V. more closely related to Camarasaurus, Brachiosaurus and RC identi® es these taxa and their omission allows extra Titanosauria than to ; (ii) Euhelopus, Chubut- resolution of the supertree (® gure 3b). Conversely, the isaurus, Phuwiangosaurus, Nemegtosaurus, Quaesitosaurus variable placement of eumaniraptorians in the source trees and Titanosauria are more closely related to each other seems to be due to real character incongruences (Holtz than they are to any other retained sauropod; (iii) Nemeg- 2000) and leads to an unresolved polytomy in the super- tosaurus and Quaesitosaurus are more closely related to the tree topology. derived Titanosauria than they are to Diplodocidae. Within Theropoda, the polytomy at the base of Coelu- rosauria is simply caused by a few poorly constrained gen- 4. DISCUSSION era (i.e. genera that are present in few trees and are not tightly bracketed by taxa of a relatively stable position) Supertree techniques are now becoming commonplace in biology (e.g. Purvis 1995b; Bininda-Emonds et al. 1999; Deltadromeus, Dryptosaurus and Nqwebasaurus. As above, Liu et al. 2001), but this is the ® rst time, to our know- ledge, that a supertree method has been implemented to Figure 2. (Opposite.) The strict consensus of the 34 900 disentangle the phylogeny of a fossil group. MPTs of length 1988 obtained from the analysis of Matrix Supertree methods resemble meta-analysis in several I. Numbers along the branches correspond to the decay respects (see also Sanderson et al. 1998). In meta-analysis, values of the supertrees obtained in the compartmentalized formal statistical techniques are implemented to sum up a analyses (which are not reported). body of separate (but similar) experiments (Mann 1990).

Proc. R. Soc. Lond. B (2002) 920 D. Pisani and others A supertree of Dinosauria

Similarly, supertree methods exploit either the existence The authors thank O.R.P. Bininda-Emonds and M.J. San- of a one-to-one relation between a tree and its matrix rep- derson for providing a preprint of their simulation work and resentation (Ragan 1992), or subtrees± tree reconstruction three anonymous referees for their useful comments on the manuscript. A.M.Y. and M.J.B. were funded by the Lever- algorithms (e.g. Aho et al. 1981; Semple & Steel 2000) hulme Trust, D.P. was partially funded by the University of to combine a body of different (but partially overlapping) Bristol through the Bob Savage Memorial Fund, and M.C.L. phylogenies. Meta-analysis is like an ordinary scienti® c was supported by an ORS grant. review of research, except that ordinary reviews provide a qualitative, and often subjective, assessment of few stud- REFERENCES ies, while meta-analysis promises a quantitative synthesis of all available data (Mann 1990). In the same way, super- Aho, A. 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Proc. R. Soc. Lond. B (2002) A supertree of Dinosauria D. Pisani and others 921

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Proc. R. Soc. Lond. B (2002)