Gradual Assembly of Avian Body Plan Culminated in Rapid Rates of Evolution across the Dinosaur-Bird Transition

Transcription

1 Current Biology, Volume 24 Supplemental Information Gradual Assembly of Avian Body Plan Culminated in Rapid Rates of Evolution across the Dinosaur-Bird Transition Stephen L. Brusatte, Graeme T. Lloyd, Steve C. Wang, and Mark A. Norell

2 Supplemental Data Figure S1, Related to Figure 1. Reduced strict consensus of the most parsimonious trees recovered by the cladistic analysis (tree length=3360 steps; consistency index=0.322; retention index=0.777). The reduced strict consensus is calculated after the a posteriori removal of five taxa: Kinnareemimus, Epidendrosaurus, Pyroraptor, Hesperonychus, and Limenavis. Numbers next to nodes denote Bremer support value/jackknife percentage. Those nodes without any numbers are characterized by Bremer values of 1 and a jackknife percentage of less than 60%. The Oviraptorosauria + Paraves clade is collapsed here for space reasons but is fully shown in the following figure (Figure S2).

3 Figure S2, Related to Figure 1. Reduced strict consensus relationships within the Oviraptorosauria + Paraves clade (see the placement of this clade among higher-level coelurosaur phylogeny in Figure S1above). Refer to the caption of Figure S1 for explanation.

4 Figure S3, Related to Figure 2. Results of 100 dating uncertainty replicates for the clade test on the first sampled tree. For a higher resolution version of the figure please see our Dryad appendix.

5 Table S1, Related to Disparity and Morphospace Occupation: Morphospace Separation Tests Comparing Avialans vs. Other Coelurosaurs Avialans vs. All Other Coelurosaurs Permutation (2000 replicates, Mesozoic avialans only): Mahalanobis distance=205.91, p= Permutation (2000 replicates, all avialans): Mahalanobis distance=168.64, p= Permutation (2000 replicates, Anchiornis, Aurornis, Xiaotingia as avialans): Mahalanobis distance=122.99, p= Additional Comparisons for Context Dromaeosaurids vs. all other coelurosaurs: Mahalanobis distance=124.61, p= Troodontids vs. all other coelurosaurs: Mahalanobis distance=104.13, p= Oviraptorosaurs vs. all other coelurosaurs: Mahalanobis distance=179.14, p= Ornithomimosaurs vs. all other coelurosaurs: Mahalanobis distance=260.96, p= Therizinosauroids vs. all other coelurosaurs: Mahalanobis distance=142.8, p= Alvarezsauroids vs. all other coelurosaurs: Mahalanobis distance=100.22, p= Compsognathids vs. all other coelurosaurs: Mahalanobis distance=396.97, p= Tyrannosauroids vs. all other coelurosaurs: Mahalanobis distance=108.64, p= Deinonychosaurs vs. all other coelurosaurs: Mahalanobis distance=131.79, p=

6 Table S2, Related to Disparity and Morphospace Occupation: Morphospace Separation Tests Comparing Avialans vs. Sister Taxa/Closest Relatives Deinonychosaurs vs. Avialans Permutation (2000 replicates, Mesozoic avialans only, on only 57 PC axes): Mahalanobis distance=7636.3, p= Permutation (2000 replicates, all avialans, on only first 63 PC axes): Mahalanobis distance=1445.6, p= Permutation (2000 replicates, Anchiornis, Aurornis, Xiaotingia as avialans, on only first 63 PC axes): Mahalanobis distance=354.79, p= Dromaeosaurids vs. Avialans Permutation (2000 replicates, Mesozoic avialans only, on only 41 PC axes): Mahalanobis distance=4154.1, p= Permutation (2000 replicates, all avialans, on only first 47 PC axes): Mahalanobis distance=2231.2, p= Permutation (2000 replicates, Anchiornis, Aurornis, Xiaotingia as avialans, on only first 50 PC axes): Mahalanobis distance=829.46, p= Troodontids vs. Avialans Permutation (2000 replicates, Mesozoic avialans only, on only 36 PC axes): Mahalanobis distance=32207, p= Permutation (2000 replicates, all avialans, on only first 42 PC axes): Mahalanobis distance=831780, p= Permutation (2000 replicates, Anchiornis, Aurornis, Xiaotingia as avialans, on only first 42 PC axes): Mahalanobis distance=91317, p= Additional Comparisons for Context Compsognathids vs. ornithomimosaurs: 17 axes, Mahalanobis distance=3900.2, p= Therizinosauroids vs. alvarezsauroids: 23 axes, Mahalanobis distance=1666.2, p= Troodontids vs. dromaeosaurids: 35 axes, Mahalanobis distance=381.96, p= Oviraptorosaurs vs. deinonychosaurs: 45axes, Mahalanobis distance=135.71, p= Ornithomimosaurs vs. alvarezsauroids: 24 axes, Mahalanobis distance=146.34, p= Compsognathids vs. tyrannosauroids: 21 axes, Mahalanobis distance=132.31, p= Ornithomimosaurs vs. tyrannosauroids: 29 axes, Mahalanobis distance=783720, p= Oviraptorosaurs vs. therizinosauroids: 20 axes, Mahalanobis distance=29042, p=

7 Table S3, Related to Disparity and Morphospace Occupation: Comparative Disparity Values Group SoR PoR SoV PoV Mesozoic avialans alvarezsauroids compsognathids dromaeosaurids ornithomimosaurs oviraptorosaurs therizinosauroids troodontids tyrannosauroids (SoR=sum of ranges; PoR=product of ranges; SoV=sum of variances; PoV=product of variances)

8 Supplemental Experimental Procedures Note: Datasets, appendices and code relevant to this section are posted on Dryad: doi: /dryad.84t75 1) Phylogenetic Analysis Taxon Sampling: The cladistic analysis includes 152 taxa scored for 853 characters. This analysis is an expanded version of the American Museum of Natural History s Theropod Working group (TWiG) dataset. This dataset has grown iteratively over the past decade with the addition of new taxa and characters, and previous versions have been presented by [S1-S10]. The most recent versions include a large amount of data relevant to avialan phylogeny that was originally presented by [S11]. These studies are considered precursors to the current analysis and many of the character data employed here were first established in these earlier works. Several other authors have also used published TWiG phylogenies as a backbone for additional phylogenetic work, especially analyses targeting the interrelationships of certain coelurosaurian subgroups [eg. S12-S21]. The focus of most previous work from the Theropod Working Group, and the focal point of all published TWiG phylogenies, is maniraptoran theropods (therizinosauroids, oviraptorosauroids, paravians, most likely alvarezsauroids). More specifically, the overwhelming focus has been on the paravian theropods, which include dromaeosaurids, troodontids, and avialans (birds). This focus reflects longstanding interest in the origin of birds and the relationships of birds and their closest dinosaurian relatives. In this paper we add a wealth of new data relevant to non-maniraptoran basal coelurosaurs (tyrannosauroids, ornithomimosaurs, compsognathids, and many singleton taxa), as well as non-paravian maniraptorans (therizinosauroids, alvarezsauroids). As a result, the cladistic analysis presented here includes a nearly complete sample of Mesozoic coelurosaurs, but the majority of new data (new characters and taxa, revised character scores) are relevant to basal coelurosaurs. Compared to the hitherto most recent TWiG dataset [S9], this analysis includes 41 new taxa, all of which are basal coelurosaurs except for two derived paravians closely related to birds that have been described very recently (Eosinopteryx, Aurornis). This section includes a list of basal coelurosaur taxa included in the analysis, sources of coding data, and notes relevant to individual taxa. General Comments: The starting point for this analysis was the latest published version of the TWiG dataset [S9]. As previous TWiG work has largely focused on the paravian theropods, character scores for these taxa were mostly accepted without revision. In some cases, however, paravian taxa had to be rescored when characters were modified (e.g., by the addition of one or more new states to encapsulate wider variation among coelurosaurs). Character scores for non-paravian maniraptorans were also largely accepted without critical revision, although scores relevant to therizinosauroids and alvarezsauroids were carefully checked. Character scores for non-maniraptoran basal coelurosaurs, however, were carefully checked and in some cases modified. Several new basal coelurosaurs, alvarezsauroids, and therizinosauroids were added to the dataset of [S9], along with the paravians Eosinopteryx and Aurornis, but no new oviraptorosauroids were added. The analysis presented here includes several new characters and these were scored for both basal coelurosaurs and maniraptorans. The following is a brief description of taxon data sources; a full explanation can be found in [S22]. Outgroup Taxa: The outgroups employed here are the non-coelurosaurian tetanurans Allosaurus and Sinraptor. These taxa were scored based on the literature and personal observation of specimens. The Utah Museum of Natural History, American Museum of Natural History, and Carnegie Museum of Natural History collections of Allosaurus were studied firsthand, as was the holotype of Sinraptor

9 (IVPP 10600). Monographs of both taxa were also used to score characters (Allosaurus: [S23]; Sinraptor: [S24]). Paravians, Oviraptorosaurs, and Therizinosauroids: Maniraptorans were scored for new characters based on the literature and personal observation of specimens. Several maniraptorans were studied firsthand as part of this project. The complete Utah Museum of Natural History collection of the basal therizinosauroid Falcarius was studied, as was the American Museum of Natural History temporary collection of IGM Gobi oviraptorosauroid material. Characters were also scored directly for some Mongolian troodontids from the AMNH and IGM collections (Byronosaurus: IGM 100/983; Saurornithoides: AMNH FARB 6516), although most new scores for troodontids were based on the literature (including those for Eosinopteyx and Aurornis). Several dromaeosaurids were studied firsthand, including Austroraptor (MML 195), Balaur (EME PV.313; LVP [FGGUB] R ), Bambiraptor (AMNH FR 30556), Buitreraptor (MPCA 245, 238), Deinonychus (YPM 5025 and hypodigm series), Dromaeosaurus (AMNH FARB 5356), Tsaagan (IGM 100/1015), Unenlagia/Neuquenraptor (MCF PVPH 77, 78), and Velociraptor (AMNH temporary collection of IGM specimens: see [S25-S26]). Finally, the basal avialan Archaeopteryx was also observed firsthand (Berlin and Eichstatt specimens), as was the enigmatic Epidexipteryx (IVPP V15471). Note that for all new characters, the five extant bird taxa included in the dataset (Crypturellus, Chauna, Anas, Crax, and Gallus) were scored in a very conservative manner, due to the great morphological differences between extant birds and basal coelurosaurs (which all new characters relate to). This was a pragmatic decision because it is often very difficult to confidently score living taxa for characters relevant to taxa such as tyrannosauroids and therizinosauroids, and therefore the possibility of making incorrect primary homology hypotheses is high. The extant birds have essentially been scored for only those characters that relate to skeletal ratios or measurements, or straightforward anatomical features that require no ambiguity to score in the living species. Alvarezsauroids: The alvarezsauroids Mononykus (AMNH IGM collection, including casts), Patagonykus (MCF PVPH 37), and Shuvuuia (IGM 100/975, 100/99, 100/10001) were studied firsthand. The basal alvarezsauroid Haplocheirus was scored based on extensive photographs provided by Jonah Choiniere, as well as the initial description of the taxon [S18]. Other alvarezsauroids were scored based on the literature and on notes and advice provided by Choiniere, whose dissertation and postdoctoral work focused largely on alvarezsauroids. Character scores for TWiG characters and some new characters were taken from [S18-20]. These scores were carefully checked and in rare cases modified. Tyrannosauroids: The character dataset of [S27], which focused on the ingroup phylogeny of tyrannosauroids, was incorporated into the dataset used here. The tyrannosauroid dataset was constructed based on extensive first-hand observation of tyrannosauroid specimens, as detailed by [S22, S27]. Ornithomimosaurs: Several ornithomimosaurian taxa were studied firsthand whereas others were scored based on the literature and photographs. Studied specimens include the holotype of Pelecanimimus polydon (LH 7777), the holotype of Shenzhousaurus orientalis (NGMC ), the full lectotype and paratype series of Archaeornithomimus asiaticus (American Museum of Natural History specimens), casts of Sinornithomimus dongi in the University of Chicago research collection, the vast Polish Academy of Sciences collection of Gallimimus bullatus and the well-preserved Gallimimus skull IGM 100/1133, and the collection of Struthiomimus altus and Ornithomimus edmonticus material in the AMNH and Royal Ontario Museum collections.

10 There is considerable uncertainty about the alpha level taxonomy of Late Cretaceous ornithomimosaurs from North America, particularly the number of different species among specimens that are commonly referred to as Struthiomimus, Ornithomimus, and Dromiceiomimus (see [S28]). The likely synonymy of Ornithomimus and Dromiceiomimus is accepted here, but considerable specimenlevel work on North American Late Cretaceous orntihomimosaurs is needed before the systematics of these taxa are resolved. We consider those specimens labeled as Struthiomimus in the AMNH collection to belong to this taxon, and consider keystone specimens of Struthiomimus and Ornithomimus described in publications such as [S28-S29] to belong to the taxon they are assigned to. We are cognizant, however, that future work may show that some of these assignments are incorrect. Compsognathids and Additional Basal Coelurosaurs: Many compsognathids and other basal coelurosaurs were studied firsthand whereas others were scored based on the literature and photographs. Studied specimens include the holotype and syntype of Coelurus fragilis (YPM 2012, ), the holotype (BSP AS I 563) and the referred French specimen (MNHN CNJ 79) of Compsognathus longipes, the holotype of Juravenator starki (JME Sch 200), the holotype of Mirischia asymmetrica (SMNK 2349 PAL), the holotype of Ornitholestes hermanni (AMNH FARB 619), the holotype of Sinosauropteryx prima (NGMC 2123), the holotype of Tanycolagreus topwilsoni (TPII ), and the holotype of Tugulusaurus faciles (IVPP V4025). Excluded Taxa: Some basal coelurosaur taxa were excluded from the analysis for various reasons. Some taxa were excluded because they are represented only by highly immature specimens, and therefore the sub-adult or adult morphologies of these taxa are unknown. It is likely that such immature specimens would not be placed accurately in a phylogenetic analysis, and thus these taxa were excluded. Scipionyx was not included because the holotype and only known specimen is a remarkably young individual, which perhaps died soon after hatchling [S30-S31]. Similarly, the tyrannosauroid Raptorex was excluded because its holotype is also a young individual which probably died within the first five years of life [S32]. Note, however, that a few taxa are included in the analysis even though they are based on young specimens (e.g., Juravenator and potentially other compsognathids, Epidendrosaurus). All compsognathid taxa are retained because detailed histological data on the ages of the relevant specimens is not yet available. Furthermore, Juravenator is retained because it is known from a nearly complete skeleton that can be scored for more characters than nearly any other basal coelurosaur, whereas Epidendrosaurus is retained because it is one of the few examples of a newly discovered and aberrant coelurosaurian subgroup, Scansoriopterygidae, whose phylogenetic placement demands testing in a large-scale analysis. However, when both Juravenator and Epidendrosaurus are removed in certain iterations of this analysis to gauge the effect of their inclusion on the results, the topology of the remainder of the tree does not change. Other taxa were excluded because they are known only from highly incomplete remains and/or because they are not described in detail in the literature. These taxa were carefully considered during the start of this project and were excluded when it became clear that they could not be scored for the vast majority of characters in the analysis. Some of these taxa could potentially be included, but were stricken from the analysis because they were not examined firsthand and are the subject of only brief reports in the literature. Xinjiangovenator was excluded because it is represented only by fragmentary hindlimb material (tibia and fibula: [S33]), whereas Santanaraptor [S34] and Yixianosaurus [S35-36] were excluded because they are known from fragmentary specimens that were not able to be observed firsthand. Finally, the recently described Yutyrannus was excluded even though it is known from a reasonably complete specimen [S37]. This decision was made because it has yet to be examined firsthand and the published figures are not adequate for carefully checking the character scores used by the authors in their phylogenetic analysis, which is a variation of the Brusatte et al. [S27] analysis that is incorporated into this dataset.

11 Other taxa are excluded because of serious doubts regarding their coelurosaurian affinities or their taxonomic status. Aniksosaurus was not included because it is unclear if it possesses any clear coelurosaurian characters [S38]. Material of Nedcolbertia was examined firsthand as part of this project (CEUM ), but this taxon was excluded because it is unclear if all of the referred material (which comes from several individuals) belongs to the same taxon. Furthermore, the histological ages of the specimens are uncertain, leaving open the possibility that some or all of them represent very young individuals and/or juveniles of a large-bodied non-coelurosaurian theropod. For more information on this taxon see [S39]. Bagaraatan was excluded because it is strongly suspected that the holotype material described by [S40] is a chimera of tyrannosauroid and non-tyrannosauroid coelurosaurian material (P. Makovicky, pers. comm., corroborated by specimen observation of SLB). The tyrannosauroid Alectrosaurus is excluded because this taxon is currently under revision by Thomas Carr, and the derived tyrannosaurid Zhuchengtyrannus [S41] is excluded because it is unclear if this taxon, represented only by a few fragmentary skull bones, can be differentiated from Tarbosaurus. Finally, note that the Argentine taxon Orkoraptor, which appears in many phylogenetic analyses of Coelurosauria, is not included here because recent work convincingly shows that this taxon belongs to the non-coelurosaurian clade Neovenatoridae [S42]. Character Sampling and Scoring: As outlined above, previous versions of the Theropod Working Group (TWiG) matrix have focused predominately on maniraptoran theropods, especially dromaeosaurids, troodontids, and avialans. A major goal of this project was to expand taxon and character sampling relevant to more basal coelurosaurian theropods such as tyrannosauroids and ornithomimosaurs, so that the TWiG dataset now represents a more-or-less complete coverage of coelurosaurian taxa and characters. The character list employed here is built upon the most recent published version of the TWiG dataset [S9]. The Turner et al. (2012) [S9] dataset included 474 characters, among which are characters used in previous TWiG analyses, characters relevant to avialan phylogeny published by Clarke et al. (2006) [S11], and new characters outlined by Turner et al. that were gleaned from new research or scrutiny of other published theropod phylogenies. These characters are included in the current dataset. In the current analysis, however, some of these characters have been expanded with the addition of new states or redefined, in order to better account for the full range of morphological variation expressed by coelurosaurs (e.g., so they could be scored in taxa as disparate as tyrannosauroids and basal birds). Some have also been divided into multiple characters, to ensure character independence. We have also attempted to standardize character statements by subtly rewriting each character so that the relevant bone (or other portion of the anatomy) is listed first, followed by the aspect of that feature that varies among taxa, followed by the category of variation (number, form, etc.), followed by the types of variation (the character states) [S43]. In addition to the 474 characters employed by Turner et al. (2012) [S9], the current analysis includes an additional 379 characters, resulting in a total of 853 characters. These new characters were compiled from several sources. Most new characters are novel characters stemming from this project, many of which are relevant to the ingroup relationship of tyrannosauroids and were published by [S27]. Other souces of new characters include recent phylogenetic analyses of basal coelurosaurian subgroups such as ornithomimosaurs [S44-45], therizinosauroids [S16-S17], and alvarezsauroids [S18- S19]. The character lists in these analyses were carefully scrutinized and we retained all those characters that were not redundant with current TWiG characters, were understandable, and were consistent with personal observations of specimens. Finally, 28 new characters that were not previously published were also included. The full list of 853 characters is presented in our Dryad Supplementary Appendix 1. Characters used by Turner et al. (2012) [S9] are listed first, followed by a handful of new characters created when original TWiG characters were divided into two or more characters, and then followed by the

12 characters added to the TWiG dataset in this project. Among these new characters, those presented by Brusatte et al. (2010) [S27] are listed first, followed by those added from other published datasets, and finally followed by the 28 characters completely new to this paper. Note that several characters (142 in total) are treated as ordered because they describe numerical transformational sequences (e.g. two vertebrae-three vertebrae-four vertebrae), nested sets of homologies (e.g., small process, medium process, large process), or combine presence/absence and transformational data (e.g., process absent, process small, process large). These decisions were based upon prior TWiG usage and the recent proposals of [S43, S46]. Each multistate character is denoted as either ordered or unordered in Dryad Supplementary Appendix 1. The character dataset is provided in our Dryad Supplementary Appendix 2. Methodological Protocols: The dataset was analyzed with equally weighted parsimony in the phylogenetic program TNT v. 1.1 [S47]. Following previous TWiG protocol, the outgroup Allosaurus was used to root the tree because it the best known, most extensively studied, and best described of the two outgroup taxa. Because of the large size of the dataset a heuristic search strategy was necessary. As a first step the data matrix was analyzed under the New Technology search options, using sectorial search, ratchet, tree drift, and tree fuse options with default parameters. The minimum length tree was found in 10 replicates, a procedure that aims to initially sample as many tree islands as possible. The generated trees were then analyzed under traditional TBR branch swapping, a procedure that aims to more fully explore each tree island. Zero-length branches were collapsed following Rule 1 of [S48]. Cladistic Analysis: Results: Most Parsimonious Topologies: The initial New Technology search recovered 75 most parsimonious trees (MPTs) of 3360 steps (consistency index=0.322; retention index=0.777). Additional TBR branch swapping on these 75 trees resulted in total MPTs trees is the memory limit in the utilized version of TNT, so it is likely that several other MPTs are left unrecovered, which is always the reality under a heuristic search. To further check the results, therefore, several additional searches using identical protocols were run, as was a different type of heuristic search using the protocol outlined in Turner et al. (2012) [S9], in which 1000 replicates of Wagner trees are followed by TBR branch swapping. All of these analyses returned an identical strict consensus of recovered MPTs, suggesting that this consensus topology is more-or-less representative of the full range of most parsimonious trees. Tree Summary: The individual most parsimonious trees were combined into a strict consensus topology (Dryad Fig. S1). Portions of the strict consensus are highly resolved and the monophyly of several major coelurosaurian subgroups is corroborated (e.g., Tyrannosauroidea, Compsognathidae, Alvarezsauroidea, Therizinosauroidea, Troodontidae). The ingroup relationships of some of these clades are also well resolved. However, several portions of this consensus phylogeny are unresolved. Perhaps surprisingly, Ornithomimosauria is not found to be monophyletic and there is a large polytomy at the base of the clade that includes all coelurosaurs more derived (closer to avialans) than tyrannosauroids. This lack of resolution is due to the uncertain phylogenetic position of a small handful of taxa, including the fragmentary basal coelurosaur Kinnareemimus (a purported ornithomimosaur: [S49]), the aberrant coelurosaur Epidendrosaurus (which is known only from two juvenile individuals: [S50]), the paravians Pyroraptor and Hesperonychus, and the avialan Limenavis. Pyroraptor and Limenavis were also found to be unstable in the analysis of Turner et al. (2012) [S9], whereas Epidendrosaurus was excluded from the primary version of that analysis. The wildcard nature of

13 these five taxa is largely due to enormous amounts of missing data each taxon can only be scored for a small fraction of the 853 characters in the analysis. In order to ameliorate the effects of these fragmentary wildcard taxa, a reduced strict consensus topology was created based on the most parsimonious trees. This procedure uses the original MPTs as source trees but simply excludes these five taxa when calculating the strict consensus. This is preferred to excluding these taxa from the analysis a priori, as it allows the taxa (and their character scores) to contribute information to the analysis and prevents the somewhat subjective decision of discarding taxa that seem too fragmentary from the outset. The reduced strict consensus topology is shown in Figures S1-S2 (and Dryad Figs. S2-S3) and is used here as the preferred phylogeny and basis for character optimization and discussion of coelurosaurian phylogeny and evolution. This topology is considerably more resolved than the strict consensus, and recovers a monophyletic Ornithomimosauria and better resolution among basal coelurosaurs and paravians. Clade Support Values: The degree of support for individual clades was assessed in two ways. First, Bremer support values were calculated. These values, sometimes referred to as decay indices, denote the number of extra steps required for the clade to fall apart in the strict consensus of less optimal topologies. In the current case, a Bremer support value of 1 indicates that the clade in question is not recovered in the strict consensus of all trees of length 3361 or less (i.e., one step longer than the MPT length of 3360). Second, jackknife percentages were calculated. The jackknife is a resampling technique, in which the phylogeny is systematically reanalyzed as characters are randomly deleted. The jackknife percentage of each clade indicates the percent of trees recovered in the jackknife analysis that includes the clade in question. Both Bremer supports and jackknife percentages (absolute values) were calculated in TNT using standard scripts. The jackknife was run using the default parameter of 36% character removal probability and 1000 replicates. Salient Phylogenetic Results: All of the major coelurosaurian subgroups that have long been considered monophyletic are also found to be monophyletic here. These include Tyrannosauroidea, Compsognathidae, Ornithomimosauria, Alvarezsauroidea, Therizinosauroidea, Oviraptorosauria, Dromaeosauridae, Troodontidae, and Avialae. Relationships within these clades are relatively well resolved in most cases. The exceptions include: Compsognathidae, whose ingroup relationships are completely unresolved; Ornithomimosauria, in which several intermediate taxa such as Harpymimus and Garudimimus fall into a polytomy; and Therizinosauroidea, in which the basal relationships are well resolved but numerous more derived taxa fall into a polytomy. Corroborating recent studies, Haplocheirus is found to be the basal-most alvarezsauroid [S18], Nqwebasaurus is recovered as a basal ornithomimosaur [S20], Xiaotingia and Anchiornis are recovered as basal troodontids [S9], Mahakala is a basal dromaeosaurid [S8-S9], and Archaeopteyx is the basal-most availan (as traditionally found, contra [S21]). These results indicate that the phylogenetic positions of these taxa are robust to the inclusion of a large amount of new data relevant to basal coelurosaurs. Among basal coelurosaurs, Bicentenaria is found to be the basal-most coelurosaurian taxon. Its position at the base of the clade is well supported: the clade of all other coelurosaurs is recovered in 65% of jackknife replicates and has a Bremer support value of 2. This is largely concordant with the phylogenetic analysis of [S51], which recovered Tugulusaurus as the most basal coelurosaur, followed by Bicentenaria. Here, Tugulusaurus and Zuolong are recovered in a slightly more derived position (i.e., they are more closely related to avialans than is Bicentenaria). Tugulusaurus and Zuolong comprise a polytomy with two other groups: Tyrannosauroidea and the clade of all other coelurosaurs. The small-bodied basal coelurosaurs Guanlong, Dilong, and Proceratosaurus are members of the clade Tyrannosauroidea, defined as all taxa more closely related to Tyrannosaurus than to Ornithomimus, Velociraptor, and Troodon [S52]. This corroborates previous arguments in favor of the tyrannosauroid affinities of these taxa, which were largely based on shared, derived characters but

14 were often not tested with large-scale phylogenetic analyses that included a broad array of basal coelurosaurs (e.g., [S27, S53-S54]). More recent analyses with increased basal coelurosaur taxon and character sampling have found some or all of Guanlong, Dilong, and Proceratosaurus to group with tyrannosauroids [e.g. S12-14, S16, S18-19, S31, S55-56], but the Turner et al. (2012) phylogeny [S9] found Dilong and Proceratosaurus to be closer to avialans than to taxa such as Eotyrannus and Tyrannosaurus, and therefore not part of the tyrannosauroid clade. Here, the clade consisting of Guanlong, Dilong, Proceratosaurus, and traditionally recognized tyrannosauroids is strongly supported by a jackknife percentage of 82% and a Bremer support of 2. Furthermore, Coelurus and Tanycolagreus form a sister taxon pair at the base of the tyrannosauroid lineage. This result was also recovered by [S12-14, S31, S51], whereas Coelurus occupies a range of other positions in other phylogenetic analyses (see below). Tanycolagreus has been included in only a few phylogenetic analyses; it groups with Coelurus as a basal tyrannosauroid in the studies of [S12-14, S51] but is placed elsewhere in other studies [S18, S55-S56] (see below). In the current analysis the sister taxon grouping of Coelurus and Tanycolagreus is well supported, as it is characterized by a jackknife percentage of 74% and a Bremer support of 2. The tyrannosauroid placement of these two genera is less supported, however, as the clade Tyrannosauroidea (Coelurus, Tanycolagreus, and all other tyrannosauroids) is characterized by a jackknife percentage of less than 50% and a Bremer value of 2). Relationships within Tyrannosauroidea are well resolved and largely follow those reported by Brusatte et al. [S27] in their tyrannosauroid-specific phylogenetic analysis. This is not surprising considering that the Brusatte et al. [S27] character set has been integrated into the present analysis. The current study, however, reports slightly less resolution than the Brusatte et al. analysis [S27], which had recovered a single most parsimonious tree. Here Proceratosaurus, Sinotyrannus, and Guanlong fall into a polytomy within Proceratosauridae. Furthermore, Proceratosauridae, Dilong, and the Eotyrannus + Tyrannosauridae clade also fall into a polytomy, and Eotyrannus and Juratyrant are in a polytomy at the base of the Eotyrannus + Tyrannosauridae clade. Many tyrannosauroid ingroup clades are well supported by high jackknife and Bremer support values. All other coelurosaurs form a clade exclusive of Bicentenaria, Tugulusaurus, Zuolong, and tyrannosauroids. This clade Maniraptoriformes is only poorly supported (Bremer support of 1 and jackknife percentage of less than 50%), and relationships at its base are unresolved. There is a basal polytomy consisting of four clades: Ornitholestes, Compsognathidae, Ornithomimosauria, and Maniraptora (i.e., the clade of all taxa more closely related to birds than to Ornithomimus: [S52]). Maniraptora the clade defined as all taxa closer to birds than to Ornithomimus is comprised in the present study of Alvarezsauroidea, Therizinosauroidea, Oviraptorosauria, and Paraves. This clade is supported by a Bremer value of 2 but a jackknife percentage of less than 50%. The clade consisting of Oviraptorosauria and Paraves is supported by a Bremer value of 1 and a jackknife percentage of less than 50%. Paraves consisting of dromaeosaurids, troodontids, and avialans is also poorly supported, as it also has a Bremer value of 1 and a jackknife of less than 50%. The recently-described Aurornis and Eosinopteryx form a clade with Anchiornis and Xiaotingia, which is placed as an earlydiverging group of troodontids. These relationships are supported by moderate Bremer values of 2 (for the troodontid placement of the Anchiornis clade and for the Anchiornis clade itself). The latter three of these taxa were recovered as troodontids by [S57], whereas Aurornis, Anchiornis, and Xiaotingia were recovered as basal avialans by [S58]. One intriguing result of the present analysis is that Epidexipteryx and Pedopenna, which together comprise a sister taxon group usually referred to as Scansoriopterygidae, are placed as the basal-most lineage of oviraptorosaurs. This result occurs in the reduced strict consensus after Epidendrosaurus, which is also usually placed in Scansoriopterygidae, is excluded a posteriori because of its status as a wildcard taxon. Scansoriopterygids are usually considered very basal avialans, possibly the basal-most members of the group (i.e., more basal than Archaeopteryx). This result is

15 recovered, for example, by [S12-S15, S18, S20-21, S51]. Turner et al. [S9] reported a different result in which Epidexipteryx is placed as the immediate outgroup of the clade consisting of dromaeosaurids, troodontids, and paravians, but also discussed how a grouping of Epidexipeteryx and oviraptorosaurs is only slightly less parsimonious. In the present analysis, characters supporting the scansoriopterygid + oviraptorosaur grouping largely relate to features of the short and deep skull shared by both clades. It must be stated, however, that the scansoriopterygid + oviraptorosaur clade is poorly supported (Bremer support of 1, jackknife percentage of less than 50%). The Status of Juravenator: As mentioned above, Juravenator was retained in the phylogenetic analysis even though its holotype and only known specimen is a very young individual. To assess any possible bias this may cause, Juravenator was excluded from the strict consensus tree construction a posteriori. Other than the omission of Juravenator, the resulting reduced strict consensus is identical to the reduced strict consensus that includes Juravenator. This exercise indicates that the phylogeny of Coelurosauria is robust to the inclusion or exclusion of Juravenator and that the monophyly and placement of Compsognathidae are not dependent on the inclusion of Juravenator. The Status of Jixiangornis: The avialan taxon Jixiangornis may be a junior synonym of Jeholornis, another avialan included in our dataset. We retain both Jixiangornis and Jeholornis in the primary version of our dataset, following the protocol of previous TWiG analyses, and because our analysis does not find them as sister taxa (which may argue against their synonymy). However, when Jixiangornis is removed from the analysis most parsimonious trees of 3338 steps are recovered (CI=0.324, RI=0.779). The strict consensus with the five wildcards removed is nearly identical to the strict consensus of the primary analysis, with just two minor discrepancies: Sapeornis and Jeholornis now fall into a polytomy at the base of the clade of avialans more derived than Archaeopteryx (rather than as successive outgroups at the base of this clade in the primary analysis) and Apsaravis falls into a polytomy with Yanornis, Yixianornis, Songlingornis, and the clade of derived avialans including Ichthyornis and extant birds (rather than the immediate outgroup of the Ichthyornis + extant bird clade in the primary analysis). Clades and Synapomorphies: In this section the synapomorphies uniting major coelurosaurian clades are listed. The focus here is on basal coelurosaurian clades (those taxa outside of Oviraptorosauria + Paraves), as the new data in this analysis focuses on these taxa. For these taxa, full diagnoses are presented for each clade in the strict reduced consensus topology. A full diagnosis is not presented for clades within Oviraptorosauria + Paraves, as the diagnoses of these clades are very similar to those presented and described in detail by the precursor analysis to this dataset [S9]. However, the major groups among Oviraptorosauria + Paraves, as well as particularly interesting or novel groups, are diagnosed below. All synapomorphies listed here are unambiguous synapomorphies of the clade in question, as optimized onto the reduced strict consensus tree in TNT. In this section character numbers are followed by a period and then the synapomorphic character state number. Coelurosauria: 35.0; 194.1; 543.0; Clade of Coelurosauria other than Bicentenaria: 99.0; 176.1; 675.0; Tyrannosauroidea: 75.1; 256.1; 664.1; 839.1; Coeluridae (Coelurus + Tanycolagreus): 142.1; 684.1; 836.1; 841.1; 842.2; 843.2; Clade of Tyrannosauroidea other than Coeluridae: 24.1; 76.2; 481.1; 485.1,2; 514.3; 683.1; 702.1; 711.1; 712.1; 745.1; 790.1; 838.1; Proceratosauridae: 270.1; 483.1; Proceratosaurus + Guanlong + Sinotyrannus: 498.1; 631.0; 635.0

16 Clade of Tyrannosauroidea other than Coeluridae, Proceratosauridae, and Dilong: 23.0; 72.1; 89.2; 169.1; 262.1; 263.1; 296.0; 501.1; 507.1; 514.1; 631.2; 632.1; 648.2; 668.1; 673.1; 684.1; 686.1; 694.1; 705.1; 714.1; 715.1; 751.1; 773.0; Clade of Xiongguanlong + Tyrannosaurus: 24.2; 30.0; 154.1; 155.2; 496.1; 566.1; 662.1; 664.0; 695.1; 696.1; Clade of Dryptosaurus + Tyrannosaurus: 182.1; 185.0; Clade of Appalachiosaurus + Tyrannosaurus: Clade of Bistahieversor + Tyrannosaurus: 235.2; 596.1; 597.1; 598.1; 600.1; 642.2; 726.1; Tyrannosauridae (Albertosaurus + Tyrannosaurus): 491.1; 515.1; 538.1; 588.1; Albertosaurinae (Albertosaurus + Gorgosaurus): 533.0; 534.1; 542.1; 548.1; 549.1; 570.1; 592.1; 614.1; Tyrannosaurinae (Alioramus + Tyrannosaurus): 482.2; 497.1; 522.1; 529.1; 554.1; 555.1; 560.2; 586.1; 589.1; 590.1; 618.1; 675.1; Clade of Tyrannosaurinae other than Alioramus: 91.1; 518.0; 562.2; 573.1; 577.1; Clade of Tyrannosaurinae other than Alioramus and Teratophoneus: 28.0; 234.0; 488.2; 517.1; 519.1; 524.1; 535.1; 553.1; 557.2; 579.2; 606.1; Tyrannosaurus + Tarbosaurus: 3.2; 9.1; 10.1; 242.2; 256.2; 476.1; 490.0; 514.0; 537.1; 541.1; 543.1; 576.2; 579.3; 580.0; 587.1; 591.1; 602.1; 603.1; 612.0; 626.1; 627.1; 628.2; 635.2; 645.1; 646.1; 651.2; 653.1; 654.1; Maniraptoriformes (clade of Coelurosauria other than Tyrannosauroidea and basal taxa): 19.0; 30.0; 60.1; 81.2; 97.1; 110.1; 117.1; 159.1; 235.0; 247.0; 252.0; 258.0; 275.1; 443.0; 460.0; 529.0; 605.0; 613.0; 631.0; 663.1; 691.1; 701.0; 740.1; 756.0; 780.1; 829.1; Compsognathidae: 76.1; 81.1; 89.0; 94.1; 122.2; 174.1; 175.2; 206.1; 207.1; 452.0; 478.1; 479.1; 498.1; 551.1; 571.1; 622.2; 670.0; Ornithomimosauria: 20.2; 25.2; 28.0; 132.1; 134.2; 146.1; 148.1; 190.1; 209.1; 386.0; 475.1; 684.1; 739.1; 754.2; 768.1; 778.1; Clade of Ornithomimosauria other than Nqwebasaurus: 211.1; 263.1; 767.1; Clade of Ornithomimosauria other than Nqwebasaurus and Pelecanimimus: 78.1; 80.1; 212.1; Beishanlong + Ornithomimus: 108.1; 151.1; 164.1; 501.1; 624.1; 700.1; Ornithomimidae: 31.1; 50.1; 72.1; 92.1; 133.1; 146.2; 200.2; 210.1; 214.1; 252.1; 260.0; 397.2; 442.1; 561.1; 563.1; 609.1; 610.1; 668.1; 689.1; 723.1; 742.1; Gallimimus + Anserimimus: 736.1; Ornithomimus + Struthiomimus + Qiupalong: 208.1; 285.1; 731.0; 734.1; 741.1; 744.1; Maniraptora (clade of Coelurosauria other than Tyrannosauroidea, Ornithomimosauria, Compsognathidae, Ornitholestes, basal taxa): 4.1; 20.1; 41.1; 46.1; 86.1; 89.0; 115.1; 118.2; 143.1; 145.0; 156.1; 158.0; 161.1; 171.1; 185.0; 186.0; 214.1; 280.1; 464.1; 552.2; 680.1; 751.1; 763.1; 780.2; Alvarezsauroidea: 18.2; 21.1; 39.2; 66.1; 71.1; 75.1; 93.1; 101.1; 104.0; 134.2; 140.2; 141.1; 149.1; 207.1; 208.1; 222.1; 351.1; 406.1; 527.1; 678.1; 682.1; 757.1; 767.1; 826.1; Clade of Alvarezsauroidea other than Haplocheirus: 154.1; 161.2; 181.1; Clade of Alvarezsauroidea other than Haplocheirus and Achillesaurus: Clade of Alvarezsauroidea other than Haplocheirus, Achillesaurus, and Alvarezsaurus: 99.1; 195.2; 697.1; 722.1; Ceratonykus + Parvicursor: 102.0; 178.3; 181.2; 184.1; 187.1; 188.1; 189.1; 191.1; 192.1; 193.2; 200.3; 345.1; 407.1; 666.1; 669.0; 746.1; 755.1; 763.0; 764.1; Bonapartenykus + Patagonykus: 161.1; Parvicursorinae (Parvicursor + Mononykus): 138.3; 337.1; 720.1; Shuvuuia + Linhenykus + Parvicursor: 104.1; 778.0

17 Linhenykus + Parvicursor: Therizinosauroidea: 8.1; 13.1; 63.1; 68.0; 81.0; 90.1; 98.1; 111.2; 117.0; 193.1; 348.1; 352.1; 366.1; 505.1; 610.1; 683.1; 745.1; 754.1; 775.1; 788.1; 789.1; 796.1; 798.1; 802.1; 815.1; 824.0; 842.1; All Therizinosauroidea other than Falcarius: 64.1; 67.1; 84.0; 85.1; 165.2; 212.1; 462.1; 701.1; 804.1; 806.1; 813.1; 817.1; 823.1; All Therizinosauroidea other than Falcarius and Beipiaosaurus: 151.2; 154.1; 167.1; 182.1; 203.1; 629.2; 711.2; 799.1; 805.1; All Therizinosauroidea other than Falcarius, Beipiaosaurus, and Alxasaurus: 740.0; 797.1; 800.1; All Therizinosauroidea other than Falcarius, Beipiaosaurus, Alxasaurus, and Erliansaurus: 133.1; 185.1; 713.1; 763.2; 805.2; 811.1; Oviraptorosauria (including Scansoriopterygidae): 64.1; 68.0; 113.1; 217.1; 248.2; 623.2; Dromaeosauridae: 17.1; 54.0; 56.1; 86.1; 101.1; 198.1; 201.1; 447.1; 607.1; Troodontidae (including Anchiornis clade): 21.1; 50.1; 68.0; 69.1; 87.1; 200.1/2; 348.1; 491.1; Anchiornis + Aurornis + Eosinopteryx + Xiaotingia: 51.1; 160.1; 206.1; 231.1; 241.1; 246.0; 503.1; 629.1; Avialae (Archaeopteryx node): 1.1; 18.2; 46.0; 114.2; 119.3/4; 152.1; 202.3; 233.1; 240.1; 262.3; 278.1; 279.1; 312.0; 421.1; 434.0; 444.1; ) Rates of Morphological Evolution Methods: In order to test for unusually high or low rates of morphological evolution we adopted the two likelihood tests presented in Lloyd et al. [S59]. The first of these asks whether an individual branch has a significantly higher or lower rate of evolution than the rest of the tree. The second asks whether a particular clade has a signficiantly higher or lower rate of evolution than the rest of the tree. In both cases rates are measured using discrete morphological characters, which are listed in our Dryad Supplementary Appendices 1 and 2. All analyses were conducted in R by GTL and all code and data used are made available in our Dryad Dataset. Only Mesozoic coelurosaurs were included in these analyses; the six post-mesozoic avialan exemplars in the phylogenetic dataset were excluded, as they are only a small sample of post-mesozoic avialan diversity. Our analyses essentially take the K-Pg boundary as a time horizon and test differences in rates between coelurosaurs living before this time. Originally the Lloyd et al. [S59] tests required three items of data: 1) a tree with branches scaled to the number of character changes, 2) a set of numeric ages (in millions of years) for each taxon present in the tree, and 3) a vector indicating the number of missing characters for each taxon present in the tree. This last piece of information was used to correct for the number of changes it is possible to observe along terminal branches. That incompleteness only affected terminal branches was due to the fact that ancestral states for each discrete character were inferred using parsimony algorithms (ACCTRAN or DELTRAN). Such algorithms do not adequately account for uncertainty, nor do they use branch durations in their inferences. Furthermore, they can lead to clumps of character changes at nodes that precede, or follow, stretches of taxa with large amounts of missing data. Consequently here we adopt the core of the Lloyd et al. [S59] approach, but make some modifications to the input data. This new approach begins by time-scaling the tree before inferring the ancestral states, and by extension the number of character changes. Consequently the Ruta et al. [S60] method used in Lloyd et al. [S59] could not be employed here (as it time-scales a tree in part using the number of character changes on each branch to infer temporal branch lengths), and instead the equal approach of Brusatte et al. [S61] as implemented in the R package paleotree [S62]. After time-scaling each tree, ancestral character states were estimated using the likelihood-based rerooting method function in the R package phytools [S63]. As the algorithm can only make estimates where data is available, taxa that could not

18 be a coded for a character were dropped from the tree, and any nodes that were consequently removed were scored as question marks (missing data). For nodes that remain the most likely state was recorded, or if more than one state were equally likely then each equally likely state was recorded in a polymorphism. Once all characters had been estimated in this way the total number of changes along each branch could be recorded. This was done by first checking whether the character state was recorded at both ends of each branch. Then if the states were the same no changes wree recorded, and if different either one change (if character was treated as unordered) was recorded, or if ordered the absolute difference between the states was used. If one or more states were polymorphic the closest state was used and the number of changes recorded accordingly. Similarly the number of states recorded at both ends of the branch was used to create the percentage completeness metric used in the Lloyd et al. algorithms [S59]. After these steps were completed the data were passed to the two Lloyd et al. [S59] tests and the number of branches and clades that showed significantly high (red), nonsignificant (white), or significantly low (blue) rates were recorded. As in Lloyd et al. [S59] an alpha of 0.01 was used to assess significance. Multiple replicates are necessary for each analysis, because uncertainty in branch durations affects both how likelihood optimizes character changes and how rates (change over time) for each branch are later calculated. Uncertainities in branch durations occur because our branch-scaling methods rely on the ages of the terminal taxa (Dryad Supplementary Appendix 3), which are rarely dated to a specific age (e.g., 95 million years ago ) but almost always to a broad range of age uncertainty (e.g., Aptian-Albian, which would correspond to somewhere within the time range of million years ago). To take into account this uncertainty, we drew the ages of each taxon from uniform distributions bounded by their first and last possible appearance dates. This uncertainty was visualised by using pie charts at each branch or node (depending on the test), which depict the relative proportion of replicates indicating high, low, or non-significant rates. In the original Lloyd et al. [S59] study, 1,000 replicates were used for each analysis. However, due to the addition of the extra steps we now use here (outlined above), and the large number of characters involved, individual replicates took longer than those in the Lloyd et al. [S59] study. Consequently producing 1,000 replicates for a single topology was not considered tenable here, so fewer numbers of replicates (either 25 or 100) were used for each analysis. For our primary analysis, we randomly selected a single most parsimonious tree (MPT) and applied the modified Lloyd et al. [S59] methods to test which branches and clades had significantly high or low rates of change. For this analysis we used 100 replicates. We followed this with a number of sensitivity tests to gauge how robust the recovered patterns were. The first of these involved randomly selecting nine other MPTs, to assess how differences in tree topology affect the rate results. For these sensitivity analyses 25 replicates were used for each of the nine trees. The second sensitivity test examined the effects of different time-scaling algorithms. Our primary analysis and the analysis on the nine addition MPTs used the equal time-scaling method of Brusatte et al. [S61]. Our sensitivity test used a different time-scaling option, the minimum-branch length method (the mbl option in paleotree; [S62]), and repeated the branch and node rate tests on the first sampled MPT using 100 randomized dating replicates and a vartime value of 1 million years. A third sensitivity analysis tested for rate heterogeneity on a tree where branches were scaled to unit length, in order to gauge how much of the rate results could be explained just by the amount of character change alone (not branch duration). Again 100 dating replicates were used. Note that this is merely a sensitivity test to assess the influence of character changes (not time) in the rate calculations. We are not performing this exercise as a primary analysis in which we assume a speciational model of evolution to measure morphological rates (such a model, where evolution happens only at speciation events, is expected to generate a tree where all branches are equal, and thus unrelated to time, but is