cranial ontogenetic variation in early saurischians and the role of ... · keywords ontogeny,...

Submitted 17 June 2015Accepted 21 December 2015Published 18 January 2016

Corresponding authorChristian Foth chris-tianfothgmxnet

Academic editorJesuacutes Marugaacuten-Loboacuten

Additional Information andDeclarations can be found onpage 28

DOI 107717peerj1589

Copyright2016 Foth et al

Distributed underCreative Commons CC-BY 40

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Cranial ontogenetic variation in earlysaurischians and the role of heterochronyin the diversification of predatorydinosaursChristian Foth123 Brandon P Hedrick45 andMartin D Ezcurra267

1 SNSB Bayerische Staatssammlung fuumlr Palaumlontologie und Geologie Muumlnchen Germany2Department of Earth and Environmental Sciences Ludwig-Maximilians-Universitaumlt Muumlnchen Germany3Department of Geosciences University of FribourgFreiburg Fribourg Switzerland4Department of Earth and Environmental Science University of Pennsylvania Philadelphia PA United States5Department of Biology University of Massachusetts Amherst MA United States6CONICET Seccioacuten Paleontologiacutea de Vertebrados Museo Argentino de Ciencias Naturales Buenos AiresArgentina

7 School of Geography Earth and Environmental Sciences University of Birmingham BirminghamUnited Kingdom

ABSTRACTNon-avian saurischian skulls underwent at least 165 million years of evolution andshapes varied from elongated skulls such as in the theropod Coelophysis to short andbox-shaped skulls such as in the sauropod Camarasaurus A number of factors havelong been considered to drive skull shape including phylogeny dietary preferences andfunctional constraints However heterochrony is increasingly being recognized as animportant factor in dinosaur evolution In order to quantitatively analyse the impactof heterochrony on saurischian skull shape we analysed five ontogenetic trajectoriesusing two-dimensional geometric morphometrics in a phylogenetic framework Thisallowed for the comparative investigation of main ontogenetic shape changes andthe evaluation of how heterochrony affected skull shape through both ontogeneticand phylogenetic trajectories Using principal component analyses and multivariateregressions it was possible to quantify different ontogenetic trajectories and evaluatethem for evidence of heterochronic events allowing testing of previous hypotheses oncranial heterochrony in saurischians We found that the skull shape of the hypotheticalancestor of Saurischia likely led to basal Sauropodomorpha through paedomorphosisand to basal Theropoda mainly through peramorphosis Paedomorphosis then ledfrom Orionides to Avetheropoda indicating that the paedomorphic trend found byprevious authors in advanced coelurosaurs may extend back into the early evolution ofAvetheropoda Not only are changes in saurischian skull shape complex due to the largenumber of factors that affected it but heterochrony itself is complex with a number ofpossible reversals throughout non-avian saurischian evolution In general the samplingof complete ontogenetic trajectories including early juveniles is considerably lower thanthe sampling of single adult or subadult individuals which is a major impediment tothe study of heterochrony on non-avian dinosaurs Thus the current work representsan exploratory analysis To better understand the cranial ontogeny and the impact ofheterochrony on skull evolution in saurischians the data set that we present here mustbe expanded and complemented with further sampling from future fossil discoveriesespecially of juvenile individuals

How to cite this article Foth et al (2016) Cranial ontogenetic variation in early saurischians and the role of heterochrony in the diversifi-cation of predatory dinosaurs PeerJ 4e1589 DOI 107717peerj1589

Subjects Biodiversity Evolutionary Studies Paleontology Taxonomy ZoologyKeywords Ontogeny Sauropodomorpha Evolution Theropoda Skull shape DinosauriaHeterochrony Geometric morphometrics

INTRODUCTIONIn an evolutionary context heterochrony describes phenotypic changes due to shifts inthe timing or rate of developmental processes in an organism relative to its ancestorand can lead to significant evolutionary changes in body plans within relatively shortperiods of time (Gould 1977 Alberch et al 1979McNamara 1982 Reilly Wiley ampMeinhardt 1997 Klingenberg 1998McNamara amp McKinney 2005) Two major typesof heterochronic processes are discerned paedomorphosis and peramorphosis Paedo-morphosis occurs when the later ontogenetic stages of an organism retain characteristicsfrom earlier ontogenetic stages of its ancestor due to a truncation of the growth period(progenesis) decrease of the growth rate (neoteny) or a delayed onset of developmentalprocesses (postdisplacement) In contrast a peramorphic organism is ontogeneticallymore developed than the later ontogenetic stages of its ancestor due to the extension ofgrowth period (hypermorphosis) the increase of the growth rate (acceleration) or theearlier onset of developmental processes (predisplacement) (see Gould 1977 Alberch etal 1979 Klingenberg 1998) In practice evidence for heterochronic events in evolutioncan be detected by comparing the ontogenetic trajectories of different taxa under theconsideration of their phylogenetic interrelationships (Alberch et al 1979 Fink 1982)Thus the concept of heterochrony connects two main fields of biological sciencesdevelopmental and evolutionary biology (Gould 1977 Raff 1996) When studyingheterochrony ontogenetic trajectories are characterized by three separate vectors (sizeshape and ontogenetic age) which allows for quantification of heterochronic processeswith slope length and position within a Euclidean space (Alberch et al 1979) In thiscontext geometric morphometrics is a useful method for characterizing shape andsize vectors to investigate heterochrony in organisms within a multivariate framework(Mitteroecker Gunz amp Bookstein 2005)

Documentation of heterochrony in the vertebrate fossil record is limited Preserved fossilontogenetic series covering the whole postnatal development of fossil species are rare due tothe fact that early juvenile specimens are often either lacking or incomplete Furthermoreexact ages of single ontogenetic stages are often not available resulting in the temporalcomponent often being replaced by size which is not an ideal variable for age (Klingenberg1998 Gould 2000) Nevertheless the role of heterochrony has been recognized anddiscussed for the evolution of multiple fossil lineages that do preserve ontogenetic series(Balanoff amp Rowe 2007 Gerber Neige amp Eble 2007 Schoch 2009 Schoch 2010 Schoch2014 Bhullar 2012 Forasiepi amp Saacutenchez-Villagra 2014 Ezcurra amp Butler 2015) includingnon-avian dinosaurs (eg Long amp McNamara 1997 Erickson et al 2004 Guenther 2009Bhullar et al 2012 Canale et al 2014) For example Long amp McNamara (1997) Ericksonet al (2004) and Canale et al (2014) hypothesized that the evolution of large body size incarcharodontosaurids and tyrannosaurids from medium-sized ancestors was the result ofperamorphosis

Foth et al (2016) PeerJ DOI 107717peerj1589 241

There has recently been an increasing interest in shape diversity in non-avian dinosaursin which geometric morphometric methods have been applied on a regular basis(eg Bonnan 2004 Chinnery 2004 Campione amp Evans 2011 Hedrick amp Dodson 2013Lautenschlager 2014 Schwarz-Wings amp Boumlhm 2014 Maiorini et al 2015) Skull shapediversity in saurischian dinosaurs has been studied in particular detail (eg Henderson2002 Young amp Larvan 2010 Rauhut et al 2011 Brusatte et al 2012 Bhullar et al 2012Foth amp Rauhut 2013a Foth amp Rauhut 2013b) but usually in relation to functionalconstraints dietary preferences phylogenetic interrelationships and macroevolutionarypatterns For example these studies have shown that skull shape in sauropodomorphsand theropods is phylogenetically constrained (Young amp Larvan 2010 Brusatte et al2012 Foth amp Rauhut 2013a) and that the shape of the orbit in theropods is functionallyconstrained (Henderson 2002 Foth amp Rauhut 2013a) Thus geometric morphometricsis a powerful method to quantify both intraspecific (eg ontogeny sexual dimorphismpolymorphism) and interspecific (eg systematics macroevolution) shape variation on thebasis of homologous landmarks or outlines which capture more information about shapethan traditional morphometric measurements (Corti 1993 Rohlf amp Marcus 1993 AdamsRohlf amp Slice 2004 Adams Rohlf amp Slice 2013 Slice 2007 Mitteroecker amp Gunz 2009Zelditch Swiderski amp Sheets 2012) As a result geometric morphometrics has also beensuccessfully applied to the study of heterochrony among various tetrapod groups in whichthe univariate mathematical approach of Alberch et al (1979) was adapted to a multivariateframework (eg Berge amp Penin 2004 Mitteroecker et al 2004 Mitteroecker Gunz ampBookstein 2005 Lieberman et al 2007 Drake 2011 Piras et al 2011 Bhullar et al 2012)However only Bhullar et al (2012) have examined cranial shape diversity of theropoddinosaurs using multivariate methods in the context of heterochrony This pioneeringstudy demonstrated that recent birds have highly paedomorphic skulls compared tonon-avian theropods and Mesozoic birds (eg Archaeopteryx and Enantiornithes) whichevolved in a multistep transformation within the clade Eumaniraptora FurthermoreBhullar et al (2012) found evidence for independent peramorphic trends in the skull shapeof large-bodied tyrannosaurids dromaeosaurids and troodontids and proposed a similartrend for allosaurids Finally Bhullar et al (2012) hypothesized a possible paedomorphosisfor Eoraptor and basal sauropodomorphs

The aim of the current study is to investigate the cranial shape diversity of saurischiandinosaurs by comparing the ontogenetic trajectories of different taxa from both qualitativeand quantitative data using two-dimensional geometric morphometrics (2D GM) Thisstudy expands on the work of Bhullar et al (2012) who focused primarily on trends withinManiraptora derived non-avian theropods and basal avian theropods We have builtupon their study by including an improved sample of basal saurischians and theropods(including a number of different ontogenetic series) which should be more sensitive fortesting of the heterochronic changes for allosaurids and basal sauropodomorphs proposedbut not verified statistically by Bhullar et al (2012) The phylogenetic relationships ofthe ontogenetic series sampled in this study are integrated into an ancestor-descendantframework to look for further potential heterochronic processes in the cranial evolutionof saurischians However due to the limited number of ontogenetic series known for


sauropodomorphs the current study focuses primarily on the early evolution of theropodsNevertheless due to the limited number of ontogenetic series currently available in ourtaxonomic sample this work must be viewed as an exploratory study which will need tobe expanded and complemented with further sampling from future fossil discoveries

MATERIALS AND METHODSTaxon samplingWe sampled the crania of 35 saurischian dinosaur taxa (10 sauropodomorphs and 25 non-pennaraptoran theropods see Table S3) on the basis of published reconstructions of adult(or advanced subadult) individuals in lateral view (with exception of the reconstructions ofthe basal tyrannosauroid Dilong [IVPP V14243] and the basal alvarezsauroid Haplocheirus[IVPP V15988] which were based on our personal observations) The data set shows anoverlap of 15 terminal taxa with that of Bhullar et al (2012) and builds on that study with anaddition of 20 new taxa Theropodswith large nasal crests (egCeratosaurusDilophosaurusGuanlong ) were excluded from the primary data set as they were found to have a strongimpact on the ancestral shape reconstruction (see below) of Averostra AvetheropodaCoelurosauria and Tyrannosauroidea (see Fig S5 and Table S6) Although cranial crestsare a common structure among theropod dinosaurs (Molnar 2005) reconstruction ofmoderately to strongly crested hypothetical ancestors within this study would necessarilybe artificial due to the lack of intermediate crested forms and relatively small sample size ofthe available data set Only Monolophosaurus was included in the main data set because itpossesses a rather moderately sized and simple nasal crest lsquoSyntarsusrsquo kayentakatae whichis often reconstructed with a pair of prominent nasal crests (Rowe 1989 Tykoski 1998)was analysed in this study without crests since this structure is probably artificial due topost-mortem displacement of the nasals (Ezcurra amp Novas 2005 Ezcurra amp Novas 2007)As cranial crests usually represent external visual signal structures (Sampson 1999 Padianamp Horner 2011 Hone Naish amp Cuthill 2012) their evolutionary development most likelyrepresents either an evolutionary novelty or was sourced from regional peramorphicprocesses if the primordia were already present in the ancestor (see discussion on theevolution of horns and frills in Ceratopsia by Long amp McNamara (1997)) However wegenerated a second data set that includes crested taxa for comparison with the main dataset (see below)

In our sample five taxa preserve early ontogenetic stages allowing the capture of bothjuvenile and adult skull shapes which were used to reconstruct five simplified ontogeneticseries containing two stages (ie an early juvenile and adult stage) This sample includes thebasal sauropodomorph Massospondylus the basal theropod Coelophysis the megalosauridDubreuillosaurus the allosauroid Allosaurus and the tyrannosaurid Tarbosaurus (seeTable S4) Two of the ontogenetic series sampled (Coelophysis and TyrannosaurusTar-bosaurus) overlap with the data set from Bhullar et al (2012) but we expand on theprevious study by including three more basal trajectories in order to concentrate on adifferent part of the theropod tree As the fossil record of juvenile dinosaur specimens withcomplete skull material is rare the number of ontogenetic series is limited To improve


sampling previous studies have included reconstructions from multiple partial juvenileskulls or juveniles from closely related taxa (eg Bhullar et al 2012) We implemented thisapproach in two cases the reconstruction of the juvenile Coelophysis sample was based onthree incomplete somewhat taphonomically deformed individuals (MCZ 4326 GR 392CM 31375) and the holotype of Sciurumimus (BMMS BK 11) was used as the juvenilerepresentative of the megalosaurid Dubreuillosaurus based on the phylogenetic analyses ofRauhut et al (2012) In contrast to Bhullar et al (2012) we did not include the ontogeneticseries of Byronosaurus Therizinosauridae (represented by a therizinosaurid embryo andthe skull of Erlikosaurus) and Compsognathus (with the juvenile specimen representedby Scipionyx) in the data set because the postorbital region of the juvenile skulls of theformer two taxa is crushed or incomplete (Bever amp Norell 2009 Kundraacutet et al 2008)and the taxonomic referral of Scipionyx to the clade Compsognathidae (see Dal Sasso ampMaganuco 2011) is uncertain and maybe an artefact of coding juvenile character states (seeRauhut et al 2012)

Two-dimensional geometric morphometrics (2D GM)We used 20 landmarks (LMs) and 51 semi-landmarks (semi-LMs) on our sample inorder to accurately capture skull shape The landmarks were collected using the softwaretpsDig2 (Rohlf 2005) and were classified as either type 1 (points where two bone suturesmeet) or type 2 (points of maximum curvature and extremities) (Bookstein 1991) (see FigS1 and Table S1 for full description) Type 3 landmarks (points constructed between twohomologous landmarks which mainly define the shape of the skull or skull openings ratherthan the position of exact homologous points) were not used in our study Semi-landmarkswere used to capture the shape of skull openings and the skull outline by defining a numberof points that are placed equidistantly along respective curves (Bookstein 1991 Bookstein etal 1999) The percent error for digitizing each landmark and semi-landmark was estimatedfor the skull reconstruction of the juvenile Coelophysis (with n= 10 replications) using themethod described by Singleton (2002) Landmark and semi-landmark error varies between0117 percent (LM 51mdashmost posterior point of the descending process of the maxillacontacting the nasal andor the lacrimal) and 0738 (LM 3mdashcontact between the maxillaand jugal along the ventral margin of the skull) with a mean of 0283 The error has nosignificant effect on the shape analyses (see Table S2)

The shape coordinates were then imported into the software package MorphoJ 105d(Klingenberg 2011) and superimposed using generalized Procrustes analysis (GPA) GPArotates translates and resizes landmark coordinates of all specimens accounting forall non-shape related differences between landmark configurations leaving only shapeinformation (Gower 1975 Rohlf amp Slice 1990) Although semi-landmarks have fewerdegrees of freedom than regular landmarks (and thus contain less shape information)(Bookstein 1991) we treated landmarks and semi-landmarks as equivalent for GPA(Zelditch Swiderski amp Sheets 2012) and did not slide the semi-landmarks The slidingprocess created considerable artificial deformation on the Procrustes-fitted shape insome taxa (see Fig S2) However due to the equivalent weighting of landmarks andsemi-landmarks it should be kept in mind that the shape information captured by the


semi-landmarks strongly influences the results (Zelditch Swiderski amp Sheets 2012 seebelow) In order to estimate the influence of the semi-landmarks on the shape data allanalyses described below were also applied to an additional data set that included onlylandmark data (see Supplemental Information)

The generated Procrustes coordinates were used to compare juvenile and adult skullshapes to each other in each ontogenetic series to find ontogenetic patterns betweenand within taxa Furthermore the Procrustes coordinates of all taxa (including juvenilespecimens) were subjected to an exploratory principal components analysis (PCA) usingthe covariance matrix generated from Procrustes coordinates PCA simplifies descriptionsof variation among individuals by creating new sets of variables that are linear combinationsof the original set such that the new sets are independent from one another and have zerocovariance The principal components (PCs) describe successively smaller amounts of totalvariance of the sample This allows for a larger proportion of the variance to be describedusing a smaller number of variables than the original data would have allowed (ZelditchSwiderski amp Sheets 2012) A multivariate regression of the Procrustes coordinates againstlog-transformed centroid sizes (=square root of the sum of the squared distances of eachlandmark to the centroid of the landmark configuration Zelditch Swiderski amp Sheets2012) was performed to test if the skull shape variation is correlated with size and containsallometric information (Drake amp Klingenberg 2008)

Quantification of ontogenetic trajectoriesThe different ontogenetic trajectories generated in the PCA and regression analyses werecompared to each other by calculating pairwise two-dimensional angles between differenttrajectories based on the PC values of the first three axes which are the significant principalcomponents (significance calculated using the broken stick method see Jackson 1993)Each of the two-stage ontogenetic trajectories was described as a phenotypic change vector1Eyi= EyijminusEyik with two shape traits (PC 1 vs PC 2 and PC 1 vs PC 3) where i is a specificontogeny between two fixed stages juvenile (j) and adult (k) (Collyer amp Adams 2007)The difference in direction (angle) between the ontogenetic phenotypic change vectors1Eya1Eyb was calculated using the dot product cosminus1(1Eya1Eyb)=

1Eyamiddot1Eyb|1Eya||1Eyb|

PC valueswere employed to calculate the length of each ontogenetic trajectory Lengths and angleswere used to characterise the differences between the ontogenetic trajectories in relation toshape variation

Phylogenetic framework for heterochronic analysesIn an evolutionary context heterochrony is defined as the change in the timing or rate ofdevelopmental processes in ancestor-descendant relationships (Alberch et al 1979 Fink1982 Klingenberg 1998) and thus a direct comparison of ontogenetic trajectories fromdifferent species (as terminal taxa) can be problematic because it is hard to determinewhich trajectory would represent the ancestral and the descendant form respectively(see Fink 1982) This is exacerbated when the supposed ancestral (terminal) speciespossesses an unknown long evolutionary history resulting from a ghost lineage Thisproblem can be partially solved using a phylogenetic approach (see Alberch et al 1979


Fink 1982 Balanoff amp Rowe 2007 Bhullar 2012 Fritsch Bininda-Emonds amp Richter 2013Mallon Ryan amp Campbell 2015) in which the ancestor of two sister (terminal) taxais represented by the hypothetical last common ancestor (Hennig 1966) Thereforeon the basis of the phylogenetic distribution of the five ontogenetic series sampled wecalculated hypothetical ancestral ontogenetic trajectories for Saurischia NeotheropodaOrionides and Avetheropoda using ancestral shape reconstructions as follows (seeFigs S3 and S4) An informal supertree (sensu Butler amp Goswami 2008) including alltaxa with adult individuals was created based on recent phylogenetic analyses (seeFigs S3 and S4) basal Sauropodomorpha (Cabreira et al 2011) Coelophysoidea(Ezcurra amp Novas 2007) Ceratosauria (Pol amp Rauhut 2012) Tetanurae (Carrano Bensonamp Sampson 2012) and Coelurosauria (Turner Makovicky amp Norell 2012 Loewen etal 2013) The phylogenetic position of Eoraptor follows Martiacutenez et al (2011) andMartiacutenez Apaldetti amp Abelin (2013) The position of Adeopapposaurus as sister taxonof Massospondylus follows Martiacutenez (2009) The position of Herrerasaurus and Tawa atthe base of Theropoda is based on Sues et al (2011) Zupaysaurus was placed outsideCoelophysoidea as one of the successive sister taxa of Averostra (Smith et al 2007 Sues etal 2011 Ezcurra 2012) The supertree was time-calibrated using the stratigraphic age ofeach taxon (as mean of time interval) (see Tables S3 and S5) The assignment of branchlengths was performed in R (R Development Core Team 2011) using the APE package(version 27-2 Paradis Claude amp Strimmer 2004) and a protocol written by Graeme Lloyd(see httpwwwgraemetlloydcommethdpfhtml) for adjusting zero branch lengths bysharing out the time equally between branches (see Brusatte et al 2008 Brusatte 2011)and adding an arbitrary length of 1 million years to the root The time-calibrated supertreewas imported into the software package Mesquite 272 (Maddison amp Maddison 2009)Subsequently Procrustes coordinates and centroid sizes of the adult representatives ofthe taxa were mapped onto the supertree as continuous characters using square changeparsimony This algorithm performs an ancestral state reconstruction by collating the sumof squared changes of continuous characters along all branches of a tree and estimates themost parsimonious ancestral states by minimizing the total sum of squared changes acrossthe tree (Maddison 1991) In the next step we tested if the continuous data contains aphylogenetic signal We performed a permutation test in MorphoJ in which the topologywas held constant and both the Procrustes-fitted shape data and the centroid size for eachtaxon were randomly permuted for all the terminals across the tree 10000 times (Laurin2004 Klingenberg amp Gidaszewski 2010) The data are considered to contain a statisticallysignificant phylogenetic signal if the squared length of the original supertree occurs in atleast 95 of the randomly generated trees Additionally we quantified phylogenetic signalin our data using a multivariate form of the K statistic with 10000 replications (BlombergGarland amp AR 2003 Paradis 2012Adams 2014) in R using the package geomorph (Adamsamp Otaacuterola-Castillo 2013) This test estimates the strength of a phylogenetic signal in a dataset in relation to a simulated Brownian motion model which is expressed as K andp values

To obtain ancestral ontogenetic trajectories the protocol described above was repeatedin a new nexus file containing the Procrustes-fitted shapes and centroid sizes of the juvenile


specimens As the juvenile data set is only represented by five taxa the original supertreewas pruned such that only these taxa remained retaining the original time-calibrationFinally the ancestral Procrustes-fitted shapes and centroid sizes of both juvenile and adultSaurischia Neotheropoda Orionides and Avetheropoda were exported and combined withthe respective data from the ontogenetic trajectories of the terminal taxa The ancestralProcrustes-fitted shape of Averostra was not considered because no ceratosaur juvenileshave been published in detail so far (seeMadsen amp Welles 2000) The new data set includingthe five terminal and four ancestral ontogenetic trajectories was loaded again intoMorphoJ

Regression analyses of ontogenetic trajectoriesA multivariate pooled within-group regression of shape against log-transformed centroidsize including terminal taxa and hypothetical ancestors (see above) was performed (Piraset al 2011 Bhullar et al 2012 Zelditch Swiderski amp Sheets 2012) in which the Procrustescoordinates were transformed into a regression score (see Drake amp Klingenberg 2008)In contrast to many previous studies of heterochrony using geometric morphometricswhich compare only the ontogenetic trajectories of terminal taxa our approach allowsthe determination of possible heterochronic patterns between ancestors and descendantsThe different ontogenetic trajectories were compared regarding slope length angles andrange of shape variation spanned by the predicted regression score The angles betweenontogenetic trajectories were calculated based on Procrustes distances and centroid sizes(see above)

As mentioned above studies of heterochrony require size shape and ontogenetic ageas independent vectors (Klingenberg 1998) Due to missing data on the individual ageof the specimens ontogenetic age could not be taken into account As a consequencethe regression analysis explores allometry and not heterochrony (Klingenberg amp Spence1993 Klingenberg 1998 Gould 2000) While some heterochronic processes can resultfrom allometric changes (eg acceleration and neoteny) allometric studies allow onlyconclusions regarding paedomorphosis and peramorphosis (Klingenberg amp Spence 1993Klingenberg 1998) which are expressed by the shape vector (ie regression score)Peramorphosis can be inferred if the adult individual of the descendant trajectory fallsalong higher regression scores than the respective ancestral one whereas paedomorphosiscan be inferred based along lower scores To verify the results of such regression analyses werepeated the analysis using Euclidean distance which is equivalent to Procrustes distance(see Singleton 2002 Tallman et al 2013) as a separate shape vector measuring differencesin shape The Euclidean distance matrix was calculated in PAST 305 (Hammer Harper ampRyan 2001) on the basis of the Procrustes coordinates of terminal taxa and hypotheticalancestors (see above) which were exported from MorphoJ For regression analysis thejuvenile specimen of Massospondylus which represents the sample with the smallestcentroid size was set to zero for aligning the distance values of the remaining taxa (Fig 4)

To test if the shape changes and as a result the presence of heterochrony of an ancestor-descendant relationship are statistically meaningful we calculated the confidence interval(CI) of the differences between regression scores and Euclidean distances of terminal andancestral taxa (n= 68) and compared themwith the differences of ancestral and descendant


regression scores from the sub-sample containing the ontogenetic trajectories Changeswere considered significant if the differences between regression scores were at least 15times higher than the CI value (see Cumming Fidler amp Vaux 2007)

For comparison we performed another PCA with the data set containing just terminaland ancestral ontogenetic trajectories and calculated the angles and lengths of thetrajectories on the basis of the first two principal components which were found tocontain all significant shape information based on the broken stick method (see above)

Finally the ancestral shape reconstructions calculated for the adult representativesof the taxa were used to qualitatively discuss the evolutionary changes within basalSauropodomorpha and Theropoda with respect to the ontogenetic changes andheterochronic trends found in the different trajectories

RESULTSGeneral ontogenetic changesThe juveniles of the sauropodomorph Massospondylus and the theropods that weresampled here tend to have skulls with a short and abruptly tapering snout short antorbitalfenestrae large subcircular orbits slender jugals and dorsoventrally deep orbital andpostorbital regions relative to the snout In addition the jaw joint is more anteriorly placedrelative to the occiput with exception of the juvenile specimen of Allosaurus sampled hereThe general ontogenetic pattern includes an elongated and dorsoventrally deeper snoutrelative to the orbital and postorbital regions and also a relative increase in size of theantorbital fenestra which correlates with a relative decrease in size of the orbit Finallythe jugal becomes more massive in all taxa which is more pronounced in the large-bodiedtheropods Allosaurus and Tarbosaurus (Fig 1) The relative elongation of the snout andantorbital fenestra were not observed in the Allosaurus or Tarbosaurus ontogenies which isprobably due to the fact that the juveniles sampled do not represent the earliest ontogeneticstages (Loewen 2009 Tsuihiji et al 2011 see lsquoDiscussionrsquo) However the discovery ofan isolated maxilla identified as a hatchling allosauroid might indicate that the snout ofearly Allosaurus juveniles was probably short and subsequently increased in relative lengthduring early ontogeny (Rauhut amp Fechner 2005)

In addition to these more general ontogenetic modifications individual taxa showspecific shape changes (Fig 1)(a) In Massospondylus the external naris becomes larger and expands dorsally The

postorbital also becomes relatively more robust The infratemporal fenestra decreasesin relative size The jaw joint moves anteroventrally

(b) In Coelophysis the external naris becomes smaller and shifts anteriorly The notchof the alveolar margin between the premaxilla and maxilla decreases in relative sizeduring ontogeny while the alveolar margin of the premaxilla becomes more alignedwith that of the maxilla The descending process of the lacrimal becomes more slenderanteroposteriorly The postorbital becomes more gracile in its relative shape Theinfratemporal fenestra increases in relative size The jaw joint moves posterodorsally

(c) In the megalosaurid taxon the external naris becomes relatively larger and expandsposteriorly The lacrimal is inclined strongly backwards and the postorbital becomes


Figure 1 Ontogenetic changes in the skull of saurischian dinosaurs (A) General ontogenetic patternin Saurischia exemplified for the basal theropod Coelophysis bauri (adult specimen modified after Rauhut2003) (BndashF) Specific ontogenetic changes in saurischian dinosaurs visualized as wireframes of Procrustes-fitted shapes (B)Massospondylus (C) Coelophysis bauri (D) Megalosaurid taxon (E) Allosaurus (F) Tar-bosaurus Grey dashed lines represent the juvenile stage and black solid lines represent the adult stage

relatively more robust The infratemporal fenestra increases in its relative size The jawjoint moves posteriorly

(d) In Allosaurus the external naris does not change in relative size but shifts ventrallyThe descending process of the lacrimal becomes more massive anteroposteriorlyThe lacrimal develops a prominent dorsal horn through ontogeny In contrast toprevious taxa the postorbital region of Allosaurus increases dorsoventrally such thatthe postorbital quadratojugal and squamosal become relatively more robust Theventral shift of the jugal leads to the formation of a wide angle between the ventralmargins of the maxilla and jugal Due to its posteroventral expansion the postorbitalaffects the shape of the infratemporal fenestra However the infratemporal fenestradoes not decrease in its relative size but shifts anteroventrally The jaw joint movesanteroventrally


(e) In Tarbosaurus the external naris does not change in relative size but shifts dorsallyAs in Allosaurus the descending process of the lacrimal becomes more massive Thesame is true for the postorbital region which increases in depth dorsoventrally Thischange is correlated with the development of a more robust postorbital quadratojugaland squamosal The jaw joint moves posteroventrally

Principal component analysis and phylogenetic correlationThe first three principal components account for 680 of the total variation (PC 1308 PC 2 239 PC 3 133) in which PC 2 and PC 3 contain the main allometricshape information (see Table S12) PC 1 describes the overall skull depth size andanteroposterior position of the external naris length of the premaxilla size of the maxillaryantorbital fossa and position of the lacrimal and postorbital on the anteroposterioraxis (affecting the size of the antorbital fenestra orbit and infratemporal fenestra) Thedorsoventral dimension of the orbit is affected by the relative depth of the entire orbitaland postorbital regions while that of the infratemporal fenestra is affected by the relativeposition of the jugal-quadratojugal bar The variation in the depth of the skull alsoaffects the position of the jaw joint on the dorsoventral axis (Fig 2C) PC 2 describes thelength of the snout caused by variation in the length of the maxilla and inclination andanteroposterior position of the lacrimal The inclination of the lacrimal affects the sizeof the antorbital fenestra while both position and inclination affect the anteroposteriordimension of the orbit PC 2 also accounts for the length and the dorsoventral positionof the external naris and size of the upper temporal region (Fig 2C) PC 3 describes thelength of the premaxilla posterior extension of the external naris dorsoventral height ofthe maxilla and anteroposterior dimension of the ventral process of the lacrimal (whichaffects the shape of the antorbital fenestra and orbit) The shape of the orbit is furtheraffected by the anteroposterior dimension of the jugal-postorbital bar Further variationcaptured by PC 3 is related to the shape of the skull roof in the orbital and postorbitalregions dorsoventral height of the infratemporal fenestra and position of the jaw joint onthe anterodorsal-posteroventral axis (Fig 2C)

The permutation tests and the multivariate K statistic recovered that both Procrustes-fitted shapes (tree length weighted by branch lengths = 05108 plt 00001 K = 02607p= 00016) and centroid size (tree length weighted by branch lengths= 83598 p= 00005K = 08900 p= 00002) are correlated with phylogeny Furthermore the multivariateregression analysis reveals that skull shape is significantly correlated with centroid size(correlation index 1532 plt 00001) (Fig 4A Table S12)

Ontogenetic trajectories in the PCA morphospaceBased on the PCA results of the original data set (ie including semi-landmarks) theontogenetic trajectories are not uniform (Fig 2 and Table 1) The trajectory of Allosaurus isshort and mainly explained by shape variation captured by PC 1 while that of Tarbosaurusis also short but mainly explained by PCs 1 and 3 The third principal component hasstronger influence on the ontogenetic shape variation in Tarbosaurus based on the length ofits trajectory Compared to Allosaurus and Tarbosaurus the other ontogenetic trajectories


Figure 2 Principal component analysis of the main sample (A) Ontogenetic trajectories of terminaltaxa for PC 1 versus PC 2 (B) Ontogenetic trajectories of terminal taxa for PC 1 against PC 3 (C) Illustra-tion of the main shape changes for the first three principal components Theropod taxa are shown as blackdots while sauropodomorph taxa are shown as grey dots The arrows illustrate the different ontogenetictrajectories in which the arrowhead marks the position of the adult individual

are longer The trajectory ofCoelophysis is mainly explained by the shape variation capturedby PCs 1 and 2 while its slope is opposite to the direction along PC 1 compared to thetrajectories of Allosaurus and Tarbosaurus Based on the angles the ontogenetic trajectoriesofMassospondylus and themegalosaurid taxon are mainly influenced by the shape variationcaptured by PCs 2 and 3 in which the ontogenetic trajectory ofMassospondylus is directed


Table 1 Angles and length of terminal ontogenetic trajectories Angles of ontogenetic trajectoriesagainst PC 1 pairwise angles between ontogenetic trajectories in the PC 1ndashPC 2 and PC 1ndashPC 3morphospace and length of ontogenetic trajectories in the PC 1ndashPC 2 and PC 1ndashPC 3 morphospace(Figs 2A and 2B) Green fields mark pairwise angles in the PC 1ndashPC 2 morphospace and orange fieldsmark that of the PC 1ndashPC 3 morphospace Angles lengths and slopes of ontogenetic trajectories versuslog-transformed centroid size (LogCS) (Fig 4A)

Massospondylus Coelophysis Megalosauridtaxon

Allosaurus Tarbosaurus

Angle (PC 1ndashPC 2) 856492 423458 833216 53228 37406Length (PC 1ndashPC 2) 01761 01174 01414 00332 00403Angle (PC 1ndashPC 3) 632316 101684 650464 185268 605157Length (PC 1ndashPC 3) 00297 00881 00390 00349 00818Massospondylus ndash 734000 1282780 982417 1772841Coelophysis 433033 ndash 548780 1716416 1093159Megalosaurid taxon 23276 409757 ndash 1334803 544379Allosaurus 890280 1323313 913556 ndash 790425Tarbosaurus 980914 1413947 1004190 90634 ndashAngle (LogCS) 33947 48961 46105 02535 15851Length (LogCS) 22815 10636 18147 10657 14016Slope (LogCS) 00593 00857 00806 00044 00277

in the opposite direction along PC 3 to that of the megalosaurid taxon and TarbosaurusHowever the length of the trajectories indicates that the second principal component hasmajor influence on the shape variation in both species during ontogeny

The PCA reveals that the ontogenetic elongation of the snout is primarily related toa relative increase in the length of the maxilla (PCs 1 2) In Massospondylus and themegalosaurid taxon the ontogenetic elongation of the snout is further affected by therelative increase of the length of the premaxilla (PC 3) The relative increase in snoutdepth results mainly from a ventral expansion of the maxilla which is more prominent inAllosaurus and Tarbosaurus than in other taxa (PCs 1 3) In the megalosaurid taxon andAllosaurusmaxillary deepening occurs together with a dorsoventral expansion of the nasal(PC 1) Additionally dorsoventral expansion of the premaxilla is observed in Allosaurusand Tarbosaurus (PC 1) The relative elongation of the snout in Massospondylus themegalosaurid taxon andCoelophysis correlates with a relative increase in the anteroposteriorlength of the antorbital fenestra caused by a posterior shift of the lacrimal and elongationof the maxilla (PCs 1 2) Additionally in Coelophysis the anterior border of the antorbitalfenestra extends anteriorly (PC 1) In bothMassospondylus and the megalosaurid taxon theantorbital fenestra is shifted posteriorly during ontogeny (PC 2) The megalosaurid taxonshows a further dorsal expansion of the antorbital fenestra (PC 3) not seen in the lattertwo taxa Although no relative size changes could be observed in the antorbital fenestraeof Allosaurus and Tarbosaurus the antorbital fenestra of Allosaurus shifts posterodorsallyduring ontogeny whereas that of Tarbosaurus shifts ventrally Inmost trajectories themostanterior point of the antorbital fossa shifts posteriorly during ontogeny (PCs 1ndash3) but arelative decrease in the length of the maxillary antorbital fossa is present in Allosaurus and


Tarbosaurus (PC 1) In the megalosaurid taxon the anterior margin of the antorbital fossashifts ventrally whereas in Coelophysis it shifts anteriorly (PC 1) which correlates with theanterior elongation of the antorbital fenestra in this taxon (see above) Asmentioned abovethe orbit decreases in relative size in all taxa during ontogeny (PCs 1ndash3) In Coelophysisand Massospondylus this is related to a relative shift of the lacrimal posteriorly (PCs 12) In the megalosaurid taxon Allosaurus and Tarbosaurus the relative size reduction iscorrelated with a change in orbital shape from subcircular to oval In the megalosauridtaxon these changes are linked to a posterior shift of the lacrimal (PC 2) and anterior shiftof the postorbital and ascending process of the jugal (PC 3) which is correlated with ananterior extension of the infratemporal fenestra In Allosaurus the ontogenetic changesof the orbit are related to the posterior extension of the lacrimal and anterior shift of thepostorbital and ascending process of the jugal (PC 1) Additionally the orbit of Allosaurusis shifted slightly dorsally In Tarbosaurus these changes result from an anterior extensionof both the postorbital and ascending process of the jugal (PC 3) The orbit of Tarbosaurusbecomes posteriorly constricted by an anterior shift of the ventral process of the postorbitalforming a suborbital process

We examined the differences in the trajectory directions when terminal and ancestralontogenetic series are compared to each other (Fig 3 and Table 2) The significant shapevariation evaluated via the broken stick method is described by the first two principalcomponents (PC 1 5039 PC 2 2079) Both axes are correlated with centroid size (seeTable S12) The ontogenetic trajectory of Coelophysis in mainly influenced by PC 1 whilethat of the megalosaurid taxon Massospondylus and all ancestral trajectories is influencedby both PC 1 and 2 in which the first principal component is found to have a higherimpact on the shape variation during ontogeny In contrast the ontogenetic trajectories ofTarbosaurus and Allosaurus are mainly influenced by PC 2

Ontogenetic trajectories in the regression analysesThe ontogenetic trajectory of Massospondylus is longer than that of the hypotheticalancestor of Saurischia for both shape variables (regression score and Euclidean distance)while the values of the shape variables are significantly lower However the slope ofthe trajectory of Massospondylus based on the regression score is less pronounced thanthat of the saurischian ancestor while it is more pronounced for the Euclidean distance(Figs 4B 4C Tables 3 and 4) In contrast the ontogenetic trajectory of the hypotheticalancestor of Neotheropoda is slightly longer and has a greater slope while the regressionscore and the Euclidean distance of the adult individual are significantly higher thanthat of the saurischian ancestor Coelophysis possesses a longer and steeper ontogenetictrajectory for both shape variables with significantly higher values than the hypotheticalancestor of Neotheropoda (Figs 4B 4C Tables 3 and 4) The ontogenetic trajectoryof the hypothetical ancestor of Orionides is shorter and has a lower slope than that ofthe neotheropod ancestor The regression score of the adult individual is significantlyhigher while the Euclidean distance is lower but not significantly different Comparedto the hypothetical ancestor of Orionides the megalosaurid taxon has a longer andsteeper ontogenetic trajectory with a significantly higher value for both shape variables


Figure 3 Principal component analysis of ontogenetic trajectories (A) Terminal and ancestral onto-genetic trajectories for PC 1 against PC 2 The arrows illustrate the different ontogenetic trajectories inwhich the arrowhead marks the position of the adult individual and the base of the arrow indicates the ju-venile individual (B) Illustration of the main shape changes for the first two principal components

(Figs 4B 4C Tables 3 and 4) In contrast the ontogenetic trajectory of the hypotheticalancestor of Avetheropoda is shorter possessing a lower slope and significantly lowerregression score and Euclidean distance for the adult individual when compared tothe hypothetical ancestor of Orionides The ontogenetic trajectories of Allosaurus andTarbosaurus are longer than that of the hypothetical ancestor of Avetheropoda Bothtrajectories show a slope decrease compared to their common ancestor Interestingly theslope is almost zero when the Euclidean distance is applied as shape variable indicatingonly minor shape changes during the ontogeny as sampled For Allosaurus both shapevalues of the adult individual are higher than that of the ancestor but only the regressionscore is significant In contrast the regression score of the adult individual of Tarbosaurusis significantly lower than that of the hypothetical ancestor of Avetheropoda while theEuclidean distance results in a higher but non statistically significant value (Figs 4B 4CTables 3 and 4)


Table 2 Angles and lengths of terminal and ancestral ontogenetic trajectories Angles of ontogenetic trajectories against PC 1 pairwise angles between ontogenetic tra-jectories in the PC 1ndashPC 2 morphospace and length of ontogenetic trajectories in the PC 1ndashPC 2 morphospace (Fig 3A)

Saurischia Massospondylus Neotheropoda Coelophysis Orionides Megalosauridtaxon

Avetheropoda Allosaurus Tarbosaurus

Angle (PC 1ndashPC 2) 295357 15193 196691 40256 332773 355725 294664 655478 791993

Length (PC 1ndashPC 2) 0082 01372 01202 01162 00879 01571 00429 0044 00735

Saurischia ndash

Massospondylus 143427 ndash

Neotheropoda 98666 44761 ndash

Coelophysis 255101 111674 156435 ndash

Orionides 37416 180843 136082 292517 ndash

Megalosaurid taxon 60368 203795 159034 315469 22952 ndash

Avetheropoda 00693 142734 97973 254408 38109 61061 ndash

Allosaurus 849165 992591 94783 1104266 811749 788797 849858 ndash

Tarbosaurus 71265 856076 811315 967751 675234 652282 713343 136515 ndash

Fothetal(2016)PeerJD

OI107717peerj1589

1641

Table 3 Angles and lengths of terminal and ancestral ontogenetic trajectories Angles lengths and slopes of ontogenetic trajectories from the regression of shape (Re-gression score RS and Euclidean Distance ED) versus log-transformed centroid size (LogCS) (Figs 4B and 4C)

Saurischia Massospondylus Neotheropoda Coelophysis Orionides Megalosaurid taxon Avetheropoda Allosaurus TarbosaurusRegression (RS)Angle (LogCS) 43762 38814 51181 6056 41743 5029 30083 11845 07153Length (LogCS) 11084 22828 13988 10657 13267 18158 09628 10659 14011Slope (LogCS) 00765 00678 00896 01061 00730 00880 00526 00207 00125Regression (ED)Angle (LogCS) 34145 50440 40199 50905 27768 34451 17014 minus01758 minus01087Length (LogCS) 11071 22864 13967 10640 13248 18121 09619 10657 14010Slope (LogCS) 00597 00883 00703 00891 00485 00602 00297 minus00031 minus00019


OI107717peerj1589

1741

Table 4 Overview of heterochronies in saurischian skull shape The differences of the regression scores(1RS) and the Euclidean distances (1ED) between ancestor-descendent relationships of adult individualsfrom the regression analysis (Figs 4B and 4C) and the interpretation regarding heterochrony

1RS 1ED HeterochronySaurischia-Massospondylus minus00262 minus00446 PaedomorphosisSaurischia-Neotheropoda 00629 00733 PeramorphosisNeotheropoda-Coelophysis 00140 00668 PeramorphosisNeotheropoda-Orionides 00146 (minus00079) NAOrionides-megalosaurid taxon 00507 00497 PeramorphosisOrionides-Avetheropoda minus00299 minus00256 PaedomorphosisAvetheropoda-Allosaurus 00153 (00066) NAAvetheropoda-Tarbosaurus minus00145 (00015) NA95 CIs 00078 00098Significance levels (p= 005) 00117 00147

Notes1RS and 1ED values in brackets mark insignificant trendsNA not available

Based on the regression analysis taxa with higher regressions scores tend to haveelongated skulls with long and slender snouts that have a rounded anterior end andpossess anteroposteriorly long antorbital fenestrae oval orbits and a post-rostrum onlyslightly dorsoventrally higher than the snout The maxilla increases in its relative lengthbut also expands ventrally The ascending process of the maxilla the anterior and ascendingprocesses of the jugal and postorbital become more massive In contrast low regressionscores account for skull shapes where these features are less pronounced developed oreven show opposite trends When compared to the regression analyses containing all taxathe relative position length and slopes of the ontogenetic trajectories of the terminal taxais almost identical (Fig 4A) supporting the robustness of the results recovered

DISCUSSIONOntogenetic patternsOur knowledge of the cranial ontogeny of non-avian dinosaurs remains fragmentaryPrevious studies on cranial ontogeny have often been based on single species (GowKitching amp Raath 1990 Carr amp Williamson 2004 Horner amp Goodwin 2006 Huumlbner ampRauhut 2010Campione amp Evans 2011Mallon et al 2011Canale et al 2014 Fredericksonamp Tumarkin-Deratzian 2014) while only a small number of studies have investigated thistopic on the interspecific level (Carr 1999 Evans 2010 Bhullar et al 2012 Mallon Ryanamp Campbell 2015) As is common in other animal groups closely related species oftenundergo similar ontogenetic changes (see Evans 2010 Mallon Ryan amp Campbell 2015)while ontogenetic trajectories become more different with increased phylogenetic distance(see Bhullar et al 2012) or in the case of a single taxon evolving extreme ontogeniescompared to their relatives (Horner amp Goodwin 2009 see also Erickson et al 2004)Despite the large phylogenetic distance between the ontogenetic series sampled herethe present study reveals that the cranial ontogeny of saurischian dinosaurs undergoessome general patterns including the relative elongation and dorsoventrally heightening ofthe preorbital region decrease in orbit size and increase in jugal robustness However thePCA shows that the different ontogenetic trajectories differ strongly in length direction


Figure 4 Centroid size regression analyses for the main sample (A) Regression analysis of all terminaltaxa including ontogenetic trajectories against log-transformed skull centroid size (LogCS) (p lt 00001)(B) Regression analysis of only terminal (solid arrows) and ancestral (dashed arrows) ontogenetic trajecto-ries against log centroid size (p lt 00001) using the regression score as shape variable (C) Equivalent re-gression analysis to (B) using the Euclidean distance as shape variable Theropod taxa are shown as blackdots while sauropodomorph taxa are shown as grey dots The arrows illustrate the different ontogenetictrajectories in which the arrowhead marks the position of the adult individual and the base of the arrowindicates the juvenile individual


and also the location within the morphospace Here the theropod taxa are markedlyseparated from the sauropodomorph Massospondylus which is morphologically verydistinct from other basal sauropod taxa This is especially obvious in the large distancewithin morphospace between Massospondylus and Coelophysis which represent the mostbasal ontogenetic series of each clade indicating a strong diversification of skull shape inthe early evolution of Saurischia This may be related to differentiations along both lines ofSaurischia in terms of ecology including trophic specializations (see Tykoski amp Rowe 2004Barrett amp Rayfield 2006 Langer et al 2010 Sakamoto 2010) The fact that the separationwithin the morphospace already take place among juvenile specimens indicates that thesespecializations might appear very early in ontogenetic development Although the distancesamong such specimens in morphospace are large the trajectories show that both speciesstill share similar trends in cranial development (Figs 2 and 3)

Although occupying a similar area of morphospace the ontogenetic trajectory of themegalosaurid taxon differs markedly from that of Allosaurus and Tarbosaurus showingmore similarity with that of Massospondylus and Coelophysis which share in common therelative elongation of the snout The latter process probably represents a morphologicaltrend within megalosaurids (Therrien amp Henderson 2007 Sadleir Barrett amp Powell 2008)while large-bodied allosauroids and tyrannosaurids tend to have rather deeper than longskulls (see Brusatte et al 2012 Foth amp Rauhut 2013a) However as several medium-sizedtyrannosauroids also have elongated snouts (Li et al 2010 Brusatte Carr amp Norell 2012Luuml et al 2014 Porfiri et al 2014) their ontogenetic trajectories would probably moreclosely resemble that of the megalosaurid taxon One has to take into account that thelength and direction of the ontogenetic trajectories of Allosaurus and Tarbosaurus are likelyinfluenced by the fact that the juvenile specimens are ontogenetically more developedcompared to that of the megalosaurid taxon (see below) Assuming that the hatchlings ofAllosaurus and Tarbosaurus also had short tapering snouts the trajectory would probablybe more similar in length and direction to that of the megalosaurid taxon

Heterochronic patternsPrevious workers have hypothesized that skull shape diversity in theropods andsauropodomorphs was driven by phylogenetic interrelationships dietary preferences(Young amp Larvan 2010 Brusatte et al 2012 Foth amp Rauhut 2013a) functional constraints(Henderson 2002 Foth amp Rauhut 2013a) but also heterochrony (Long amp McNamara1997 Bhullar et al 2012) This study builds on the recent heterochronic analysis of Bhullaret al (2012) who primarily examined derived non-avian theropods and basal avians on thebasis of a great number of ontogenetic trajectories of non-avian coelurosaurs and an extantphylogenetic bracket of crocodylians and birds covering a broader scale of archosauriancraniofacial shape variation However by sampling and comparing ontogenetic trajectoriesof more basal saurischian taxa our data set allows for reevaluation of the conclusionspresented by Bhullar et al (2012)with regards to basal sauropodomorphs allosauroids andtyrannosauroids The current study supports the influence of heterochrony on the cranialevolution of some saurischian lineagesWhen the differences of the regressions scores (1RS)and the Euclidean distances (1ED) in an ancestor-descendant relationship are compared


the significant decrease of the shape values indicates potential paedomorphosis for the skullshape of Massospondylus and the hypothetical ancestor of Avetheropoda while the skullsof Coelophysis the megalosaurid taxon and the hypothetical ancestor of Neotheropodamight be peramorphic Thus the current analyses support a paedomorphosis for basalsauropodomorphs as predicted by Bhullar et al (2012) Due to contradicting resultsregarding shape differences no heterochronic pattern can be inferred for AllosaurusTarbosaurus and the hypothetical ancestor of Orionides Thus the current analyses donot support the predicted cranial peramorphosis for the allosauroids and tyrannosauridlineage (Long amp McNamara 1997 Bhullar et al 2012 Canale et al 2014) while studieson growth (Bybee Lee amp Lamm 2006 Erickson et al 2004) and body size evolution(Dececchi amp Larsson 2013 Benson et al 2014 Lee et al 2014) in theropods indicate sucha trend However this conflict is probably caused by incomplete sampling of ontogenetictrajectories which affects the estimated shape of the hypothetical ancestor of AvetheropodaA further expansion of the sampling of ontogenetic trajectories of saurischian taxa andthe inclusion of an extant phylogenetic bracket (see Bhullar et al 2012) would probablychange some aspects of the analytical outcomes of this study (see below)

The increase in slopes in the ontogenetic trajectories of Neotheropoda Coelophysisand the megalosaurid taxon when compared to their ancestors might show evidencefor peramorphic acceleration However with a few exceptions bone histology of basaltheropods (eg Coelophysis and Syntarsus) is not well studied so that this cannot beconfirmedby growth patterns Several studies on body size evolution support a peramorphictrend showing an increase of size from the hypothetical ancestor of Saurischia overNeotheropoda towards megalosaurids (Irmis 2011 Dececchi amp Larsson 2013) In contrastthe relative decrease in slope in the ontogenetic trajectory of the hypothetical ancestorof Avetheropoda might indicate neoteny But again this cannot be confirmed by bonehistological data at this time Dececchi amp Larsson (2013) and Lee et al (2014) found adecrease of body size from the hypothetical ancestor of Tetanurae towards Avetheropodasupporting a paedomorphic trend in body size For Massospondylus the situation is notentirely clear as our two shape variables led to conflicting results regarding the slopewhen compared with the saurischian ancestor Thus no underlying heterochronic processcan be diagnosed for the paedomorphic skull shape of Massospondylus Although basalsauropodomorphs show a gradual trend towards bigger body size (Sander et al 2010 Irmis2011 Benson et al 2014) and longer accelerated growth (Chinsamy 1993 Erickson Rogersamp Yerby 2001 Klein amp Sander 2007) skull size decreased relatively (Rauhut et al 2011)This relative shrinking might be the reason for the maintenance of a more juvenile skullshape in the early evolution of sauropodomorphs However due to the lack of informationregarding the ontogenetic age of the individuals the deduction of heterochronic processrelated to the slope (ie neoteny and acceleration) has to be considered with caution(see below)

The results of the regression analyses can be further used to interpret evolutionary shapechanges found between hypothetical ancestors and terminal taxa in the ancestral shapereconstruction analyses of the main sample (ie continuous character mapping of theProcrustes-fitted shapes) in terms of paedomorphic or peramorphic trends (Fig 5)


Figure 5 Simplified phylogeny of Saurischia showing the main heterochronic trends of the skullPeramorphosis is colored in green and paedomorphosis in yellow Grey trends indicate uncertain shapetrends Shape of the hypothetical ancestors based on the continuous character mapping of the Procrustes-fitted shapes of the adult terminal taxa from the original data set Blue skulls represent ancestral skullshapes for which ontogeny could not be analysed The heterochronic trends found in the regressionanalyses are visualized by the color of the branches Possible heterochronic trends related to the skullevolution of allosauroids and basal coelurosaurs (see lsquoDiscussionrsquo) are shown as dashed branches


Comparing the skull shape of the hypothetical ancestor of Saurischia to that ofSauropodomorpha indicates a possible initial paedomorphosis in the evolution of thelatter group as shown by the regression analyses which is depicted by a decrease in therelative length of the preorbital region and an increase in the relative orbital size anddepth of the postorbital region As stated above Bhullar et al (2012) already proposeda cranial paedomorphosis for basal sauropodomorphs after finding a strong similaritybetween the skull shape of Eoraptor and the juvenile theropod Coelophysis which hadbeen also highlighted qualitatively by previous authors (eg Ezcurra 2007) In additionFoth (2013) has shown that the skull shape of Eoraptor and Pampadromaeus resembledthat of the juvenile theropods Sciurumimus and Juravenator In Eusauropoda the snoutsbecome more aberrant due to a dorsal shift of the external naris posterodorsal extension ofthe premaxilla elongation of the ascending process of the maxilla and modification of thepostorbital region affecting the relative size of the jugal and postorbital which becomemoregracile (Wilson amp Sereno 1998 Rauhut et al 2011) While the shape changes in the snoutand the shift of the naris were previously presumed to be peramorphic (Long amp McNamara1997) one can assume on the basis of the current observations that the increase of gracilityin the postorbital region of derived sauropods may result from modular paedomorphosisIn this context Salgado (1999) has hypothesized that the reduction of the supratemporalfenestra and fusion of the frontals in diplodocoid sauropods is the result of a peramorphicheterochrony while the loss of contact between squamosal and quadratojugal could bepaedomorphic However these character changes are beyond the scope of the current studydue to the lack of good skull material of juvenile individuals of basal sauropods and thusneed to be analysed in more detail in future studies after the appropriate juvenile materialsare discovered

In contrast the initial evolutionary changes in the skull shape of Theropoda weredriven by peramorphic events as is observed in Coelophysis the megalosaurid taxon andthe hypothetical ancestor of Neotheropoda in the regression analyses These changesinclude the elongation of the snout increase in length of the antorbital fenestra and trendsto a relatively smaller orbit and more robust post-rostral region The basal ceratosaurLimusaurus has a rather small skull with a short snout enlarged subcircular orbit andgracile jugal and postorbital so it is possible that the more robust skull shape (oval orbitmassive jugal and postorbital) of large-bodied ceratosaurs likeCeratosaurus and abelisaurids(eg Carnotaurus andMajungasaurus) could be the result of a secondary peramorphosis asit was proposed for allosaurids and tyrannosaurids (eg Long amp McNamara 1997 Bhullaret al 2012) However due to the poor cranial knowledge and fluctuating phylogeneticrelationships of basal ceratosaurs from the Early and Middle Jurassic (eg Pol amp Rauhut2012 Tortosa et al 2013) the early skull shape evolution of Ceratosauria is not currentlyreproducible In contrast the skull of the hypothetical ancestor of Avetheropoda is probablypaedomorphic with respect to that of Orionides as shown in the regression analyses(Figs 4B and 4C) This trend might extend to the hypothetical ancestor of CoelurosauriaManiraptoriformes and Maniraptora leading to a shorter more tapering snout in lateralview smaller antorbital fenestrae enlarged subcircular orbits and amore gracile postrostralregion resembling the skull shape of the juvenile megalosaurid Sciurumimus These


findings may indicate that the paedomorphic trend hypothesized for Eumaniraptora byBhullar et al (2012) reaches back into the early evolution of Avetheropoda and that basalcoelurosaurs in fact represent lsquolsquominiaturizedrsquorsquo tetanurans conserving juvenile characters inadult individuals A similar trend is found for body size evolution in theropods showinga successive decrease in body size within Avetheropoda (Novas et al 2012 Dececchi ampLarsson 2013 Lee et al 2014) In contrast to this supposed early paedomorphic trend theancestral shape reconstruction reveals that the skulls of allosauroids become secondarilymore robust in relation to the hypothetical ancestor of Avetheropoda supporting cranialperamorphosis (see Canale et al 2014) This might also be the case for large-bodiedtyrannosaurids (see Long amp McNamara 1997 Bhullar et al 2012) although the currentregression analyses could not find such a signal for both groups (see below) Bhullar etal (2012) suggested a multi-step progenetic paedomorphosis for skull shape of Paravesand basal birds with modular peramorphic trends related to beak formation and furtherperamorphic trends for secondarily large-bodied troodontids and dromaeosaurids Theseheterochronic changes were supported by trends regarding body size evolution (Turneret al 2007 Dececchi amp Larsson 2013 Lee et al 2014) and growth patterns (Erickson et al2009) found within Eumaniraptora However as it is the case for Sauropodomorphavarious trends seen in skull shape evolution of theropods need to be verified in the futureregarding possible heterochrony on the basis of new material of both juvenile and adultspecimens

Functional and ecological implicationsThe major differences in cranial shape found here clearly affect dietary preferences andfunctional constraints The robust morphology of the postorbital region and the ovalorbit in peramorphic skulls was previously discussed in relation to the generation ofhigher bite forces (Henderson 2002 Foth amp Rauhut 2013a) However these functionalconstraints go hand in hand with a decrease in cranial disparity (Brusatte et al 2012)Paedomorphic changes in the orbital and postorbital regions were discussed in relation tovisual elaboration and brain enlargement (Bhullar et al 2012) and may have played animportant role in nocturnal activity (Schmitz amp Motani 2011) or the evolution of flightwithin Paraves (Balanoff et al 2013) On the other hand large and circular orbits mightsimply correlate with reduced mechanical stresses during biting (Henderson 2002) whichhave been suggested to also influence size and shape of the external naris antorbital fenestraand infratemporal fenestra (Witmer 1997Witzel amp Preuschoft 2005Witzel et al 2011)

Both ontogenetic and phylogenetic variations in snout shape are likely related to dietarypreferences (Brusatte et al 2012 Foth amp Rauhut 2013a Foth Bona amp Desojo 2015 seeabove) in which the shape of premaxillae and maxillae partly determines the number andsize of teeth (Henderson amp Weishampel 2002) Various examples of ontogenetic changesin the morphology and number of teeth are documented in Saurischia including the basalsauropodomorphMassospondylus coelophysoids (Colbert 1989) basal tetanurans (Rauhutamp Fechner 2005 Rauhut et al 2012) tyrannosaurids (Carr 1999 Tsuihiji et al 2011) andmaniraptorans (Kundraacutet et al 2008 Bever amp Norell 2009) Based on these observationsthe evolutionary increase in the number of teeth has been interpreted as peramorphic


(Bever amp Norell 2009) Tooth morphology however was found to be a stronger indicatorof diet than the shape of the snout itself (see Smith 1993 Barrett 2000 Barrett Butleramp Nesbitt 2011 Zanno amp Makovicky 2011 Foth amp Rauhut 2013a Hendrickx amp Mateus2014) In this context Rauhut et al (2012) hypothesised based on the similarities in thedentition of the juvenile megalosaurid Sciurumimus adult compsognathids (Stromer 1934Currie amp Chen 2001 Peyer 2006) and adult dromaeosaurids (Xu ampWu 2001 Norell etal 2006) that strongly recurved crowns with reduced or no mesial serrations may bepaedomorphic in the latter two taxa This heterochrony probably results from the decreaseof body size observed in coelurosaurs (see above) and indicates an evolutionary shift indietary preferences to smaller prey (see also Zanno amp Makovicky 2011)

LimitationsAs is common in vertebrate paleontology the current study has a limited sample size whencompared with extant neontological data sets (Brown amp Vavrek 2015) The current resultsare necessarily preliminary andmust be viewedwith caution especially because the samplingof ontogenetic trajectories is considerably lower than the sampling of adult individualsFurthermore trajectories are constructed using a single juvenile and adult specimenwith no intermediate forms A single multistage example for Tyrannosaurus presented byBhullar et al (2012) has shown that during ontogeny the trajectory can change its directionconsiderably in a multivariate PCA plot This in turn has an important impact on thelength of the trajectory and its angle in relation to other trajectories However in regressionanalyses the difference with a two-stage approach should be less substantial as multivariateshape information is transformed into a single variable of shape for each stage with respectto its centroid size The poor sample of juveniles is a result of rarity and poor preservation inthe fossil record which seems to be due to a number of factors including preferred huntingof juveniles by predators (Hone amp Rauhut 2010) and a smaller likelihood of preservationdiscovery and collection because juveniles have smaller body sizes and more fragile bonesthan adults (Brown et al 2013) Thus due to small sample sizes the statistical power ofour analyses is generally low (see Cumming Fidler amp Vaux 2007) limiting the explanatorypower of our results On the other hand Brown amp Vavrek (2015) recently demonstratedthat the number of positive and negative allometries is underestimated in smaller samplesin both paleontological and neontological data sets

Another issue affecting our results is that the juvenile individuals sampled hereare all of different early ontogenetic stages The juvenile Massospondylus represents acomposite of several embryos close to hatching (Reisz et al 2010) the megalosauridtaxon (ie Sciurumimus albersdoerferi) is an early juvenile and its exact age could notbe determined (Rauhut et al 2012) the age of the Coelophysis juvenile reconstructed isapproximately one year old (estimated by Colbert 1990 Rinehart et al 2009) the juvenileTarbosaurus specimen is two to three years old (Tsuihiji et al 2011) and the juvenileAllosaurus is likely five to seven years old (estimated based on Bybee Lee amp Lamm 2006Loewen 2009) Thus the different ontogenetic stages of the juvenile specimens and the smallnumber of individuals for each ontogenetic series most likely affected the length but maybealso the slope of the calculated trajectories (and thus the angles between the trajectories)


(see Cardini amp Elton 2007) including that of the hypothetical ancestors Furthermorethe uncertainty regarding the age of the specimens leads to another weak point asspecimen age was not used to characterize the ontogenetic trajectories (see above) whichis a common problem in paleontology (eg McKinney 1986 Klingenberg 1998 Gould2000 Schoch 2010 Bhullar et al 2012) In consequence the applied regression analysesexplored allometry and not heterochrony (see Klingenberg amp Spence 1993 Klingenberg1998) The substitution of age by size however would imply similar growth dynamics(ie proportionality between age and size) between ancestors and descendants whichwould consequently ignore heterochronic processes related to growth rates (ie progenesisand acceleration) Althoughdinosaurs generally have higher growth rates compared to othernon-avian reptiles histological studies reveal that growth rates are not identical (EricksonRogers amp Yerby 2001 Erickson et al 2004 Padian De Ricqlegraves amp Horner 2001 Sander etal 2004 Erickson et al 2009 Grady et al 2014 Werner amp Griebeler 2014) Thereforeallometric patterns cannot be used to infer heterochrony beyond paedomorphosis andperamorphosis as argued by Klingenberg amp Spence (1993) and Klingenberg (1998) Takingthe uncertainties related to the lengths and slopes of the ontogenetic trajectories (due toincomplete ontogenetic series) and statistical uncertainties (due to the small sample size)into account the classifications of underlying heterochronic processes would be misleadingand probably erroneous

In the current study the interpretations of paedomorphosis and peramorphosis rely onthe significant shape differences between adult individuals of the ontogenetic trajectoriesexpressed by shape vectors in the regression analyses for which the multivariate shapedata were transformed into a univariate shape variable These differences are affectedby type of shape variable but more importantly by the ancestral shapes which in turndepend on the phylogenetic relationships the algorithm of time calibration (eg Bapst2014) and the method of reconstruction (eg Martins 1999 Webster amp Purvis 2002)Thus one has to be aware that the application of different methods could result in slightlydifferent ancestral shapes affecting the value of the shape variable However because thecurrent sample covers all major linages of basal saurischians except of crested taxa whichwere found to impact the ancestral shape of the skull roofs significantly (see Fig S5 andTable S6) the results of the ancestral reconstruction of adult individuals are viewed asvalid By using two different shape variables (Regression score and Euclidean distance) itwas possible to confirm significant results through multiple methods

The undefined trend found for Tarbosaurus in relation to the hypothetical ancestorof Avetheropoda illustrates the limitations of our analyses Our result is seeminglycontradictory to previous hypotheses and our ancestral shape reconstruction whichproposed peramorphosis as the main driver of skull evolution in large-bodiedtyrannosaurids (see above Long amp McNamara 1997 Bhullar et al 2012) As stated abovethis result is most likely related to the small sample size of ontogenetic trajectoriesas skulls with elongated and slender snouts are considered to be peramorphic on thebasis of the regression analyses The inclusion of more ontogenetic trajectories of large-bodied theropods would probably change this result in favour of a trend towards adeeper snout Furthermore large-bodied tyrannosaurids like Tarbosaurus descended


from small-bodied coelurosaurian ancestors (Xu et al 2004 Xu et al 2006 Brusatte etal 2010 Rauhut Milner amp Moore-Fay 2010 Benson et al 2014) which means that thehypothetical inclusion of an ontogenetic trajectory of a small-bodied basal coelurosaur(eg Compsognathus Dilong Haplocheirus) and a respective hypothetical ancestorof Coelurosauria would probably change the current results leading to a secondaryperamorphic trend in Late Cretaceous tyrannosaurids as suggested by previous authorsThus this result is very likely an artefact of incomplete sampling In this context thelimited number of ontogenetic series of basal sauropodomorphs results only in a roughtrend regarding the relationship between cranial ontogeny and evolution which cannot beextended to more general patterns in the skull shape evolution of basal sauropods

CONCLUSIONSThe importance of heterochrony in non-avian dinosaur skull evolution is a relativelynew concept (see Long amp McNamara 1997 Bhullar et al 2012) This study quantitativelyassesses the impact of skull heterochrony across early saurischian evolution allowingtesting some of the heterochronic trends proposed by Bhullar et al (2012) and furtherhighlights different vantages of using morphometric data to elucidate heterochronictrends We estimated hypothetical ontogenetic trajectories in Saurischia NeotheropodaOrionides andAvetheropoda using ontogenetic trajectories ofMassospondylusCoelophysisa megalosaurid taxon Allosaurus and Tarbosaurus When compared using PCA theontogenetic trajectories of the terminal taxa show great variation in length and direction butstill follow some very general patterns including a relatively elongated and dorsoventrallydeeper preorbital region decrease in orbit size and increase in jugal robustness Generalperamorphic skulls includemore elongate and slender snouts elongate antorbital fenestraeoval orbits dorsoventrally shallower post-rostral regions andmoremassivemaxillae jugalsand postorbitals Paedomorphic skulls show the opposite features The shape changes fromthe hypothetical ancestor of Saurischia toMassospondyluswere paedomorphic as previouslysuggested by Bhullar et al (2012) In contrast skull evolution of basal theropod taxa wasprobably affected by peramorphic trends However Avetheropoda showed paedomorphicchanges compared to Orionides This might indicate that the paedomorphic trend foundfor Eumaniraptora (see Bhullar et al 2012) may reach back into the early evolution ofAvetheropoda The hypothesized peramorphic evolution for skull shape of allosaurids andtyrannosaurids could not be supported by the current study but this probably resultedfrom the small sample size of ontogenetic trajectories Although our data showed minimaldifferences between our crested-taxa and non-crested taxa data sets and semi-landmark andno semi-landmark data sets it is important to fully evaluate all possible sources of trendsespecially when working with a small data set As stated above our study is hamperedby the preservation of the fossil record (mainly the poor sample of complete juvenilespecimens) and more finds will help to elucidate other evolutionary patterns related toheterochrony With a larger number of taxa comprising juvenile and adult stages it willbe possible to further test heterochronic hypotheses within Saurischia in more detail andeliminate artefacts related to sample size Future studies may also examine ontogenetic


histories of individual taxa that have reasonably complete ontogenetic samples such asCoelophysis to evaluate which factors (dietary preference heterochrony etc) drive shapechange in individual taxa A larger number of studies using geometric morphometrics forindividual taxa as well as a more complete sampling within Saurischia are necessary tomorecompletely assess the importance of heterochronic processes in both sauropodomorphand theropod skull shape In addition it would be of value to explore modularity insaurischian skulls to project the investigation of heterochronic processes to particularskull regions In sum this study demonstrates that heterochrony played an important rolein basal non-avian saurischian skull evolution building upon previous studies (Bhullaret al 2012)

Institutional Abbreviations

BMMS Buumlrgermeister Muumlller Museum Solnhofen Solnhofen GermanyCM Carnegie Museum of Natural History Pittsburgh USAGR Ruth Hall Museum Ghost Ranch USAIVPP Institute of Vertebrate Paleontology and Paleoanthropology Beijing ChinaMCZ Museum of Comparative Zoology Harvard University USA

ACKNOWLEDGEMENTSWe thank Oliver Rauhut (Bayerische Staatssammlung fuumlr Palaumlontologie und GeologieMuumlnchen) Miriam Zelditch (University of Michigan) Johannes Knebel (LudwigMaximilians University Muumlnchen) Stefan Richter (University of Rostock) Walter Joyceand Eduardo Ascarrunz (both University of Fribourg) for discussion and Michel Laurin(Sorbonne Universiteacutes Paris) for comments on an earlier version of the manuscript Wefurther thank Matthew Lamanna (Carnegie Museum of Natural History Pittsburgh) AlexDowns (Ruth Hall Museum Ghost Ranch) David Gillette (Museum of Northern ArizonaFlagstaff) and Xu Xing (Institute of Vertebrate Paleontology and PaleoanthropologyBeijing) for access to collections This study benefitted especially from critical commentsof Jesuacutes Marugaacuten-Loboacuten (Universidad Autoacutenoma de Madrid) and three anonymousreviewers

ADDITIONAL INFORMATION AND DECLARATIONS

FundingCF is supported by a DFG grant to Oliver Rauhut (RA 101212-1) and a postdoctoralfellowship of the DAAD German Academic Exchange Service (No 9154678) BPH issupported by a Benjamin Franklin Fellowship at the University of Pennsylvania MDE issupported by a grant of the DFG Emmy Noether Programme to Richard J Butler (BU25873-1) The funders had no role in study design data collection and analysis decisionto publish or preparation of the manuscript


Grant DisclosuresThe following grant information was disclosed by the authorsDFG RA 101212-1DAAD German Academic Exchange Service 9154678Benjamin Franklin FellowshipDFG Emmy Noether Programme BU25873-1

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Christian Foth conceived and designed the experiments performed the experimentsanalyzed the data contributed reagentsmaterialsanalysis tools wrote the paperprepared figures andor tables reviewed drafts of the paperbull Brandon P Hedrick and Martin D Ezcurra conceived and designed the experimentscontributed reagentsmaterialsanalysis tools wrote the paper reviewed drafts of thepaper

Data AvailabilityThe following information was supplied regarding data availability

All raw data are submitted as Supplemental Information including a MorphoJ andNexus file

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj1589supplemental-information

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Foth C 2013Ontogenetic macroevolutionary and morphofunctional patterns in archosaurskulls a morphometric approach Muumlnchen Ludwig-Maximilians-Universitaumlt

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McNamara KJ McKinneyML 2005Heterochrony disparity and macroevolutionPaleobiology 3117ndash26 DOI 1016660094-8373(2005)031[0017HDAM]20CO2

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Mitteroecker P Gunz P Bookstein FL 2005Heterochrony and geometric morphomet-rics a comparison of cranial growth in Pan paniscus versus Pan troglodytes Evolutionamp Development 7244ndash258 DOI 101111j1525-142X200505027x

Mitteroecker P Gunz PWeber GW Bookstein FL 2004 Regional dissociated hete-rochrony in multivariate analysis Annals of Anatomy 186463ndash470DOI 101016S0940-9602(04)80085-2

Molnar RE 2005 Sexual selection and sexual dimorphism in theropods In CarpenterK ed The carnivorous dinosaurs Bloomington Indiana University Press 284ndash312

Norell MA Clark JM Turner AH Makovicky PJ Barsbold R Rowe TB 2006 A newdroameosaurid theropod from Ukhaa Tolgod (Oumlmnoumlgov Mongolia) AmericanMuseum Novitates 35451ndash51DOI 1012060003-0082(2006)3545[1ANDTFU]20CO2

Novas FE Ezcurra MD Agnoliacuten FL Pol D Ortiacutez R 2012 New Patagonian Cretaceoustheropod sheds light about the early radiation of Coelurosauria Revista del MuseoArgentino de Ciencias Naturales nueva serie 1457ndash81

Padian K De Ricqlegraves AJ Horner JR 2001 Dinosaurian growth rates and bird originsNature 412405ndash408 DOI 10103835086500

Padian K Horner JR 2011 The evolution of lsquolsquobizarre structuresrsquorsquo in dinosaurs biome-chanics sexual selection social selection or species recognition Journal of Zoology2833ndash17 DOI 101111j1469-7998201000719x

Paradis E 2012 Analysis of phylogenetics and evolution with R New York SpringerParadis E Claude J Strimmer K 2004 APE analyses of phylogenetics and evolution in

R language Bioinformatics 20289ndash290 DOI 101093bioinformaticsbtg412Peyer K 2006 A reconsideration of Compsognathus from the Upper Tithonian of

Canjuers southeastern France Journal of Vertebrate Paleontology 26879ndash896DOI 1016710272-4634(2006)26[879AROCFT]20CO2

Piras P Salvi D Ferrara G Maiorino L DelfinoM Pedde L Kotsakis T 2011 The roleof post-natal ontogeny in the evolution of phenotypic diversity in Podarcis lizardsJournal of Evolutionary Biology 242705ndash2720 DOI 101111j1420-9101201102396x

Pol D Rauhut OWM 2012 AMiddle Jurassic abelisaurid from Patagonia and theearly diversification of theropod dinosaurs Proceedings of the Royal Society B2793170ndash3175 DOI 101098rspb20120660

Porfiri JD Novas FE Calvo JO Agnoliacuten FL Ezcurra MD Cerda IA 2014 Juvenilespecimen ofMegaraptor (Dinosauria Theropoda) sheds light about tyrannosauroidradiation Cretaceous Research 5135ndash55 DOI 101016jcretres201404007

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Rauhut OWM 2003 The interrelationships and evolution of basal theropod dinosaursSpecial Papers in Palaeontology 691ndash213

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Rauhut OWM Foth C Tischlinger H Norell MA 2012 Exceptionally preserved juvenilemegalosauroid theropod dinosaur with filamentous integument from the LateJurassic of Germany Proceedings of the National Academy of Sciences of the UnitedStates of America 10911746ndash11751 DOI 101073pnas1203238109

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Sander PM Klein N Buffetaut E Cuny G Suteethorn V Le Loeuff J 2004 Adaptiveradiation in sauropod dinosaurs bone histology indicates rapid evolution ofgiant body size through acceleration Organisms Diversity amp Evolution 4165ndash173DOI 101016jode200312002

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Schoch RR 2009 Life-cycle evolution as response to diverse lake habitats in Paleozoicamphibians Evolution 632738ndash2749 DOI 101111j1558-5646200900769x

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Turner AH Pol D Clarke JA Erickson GM Norell MA 2007 A basal dromaeosauridand size evolution preceding avian flight Science 3171378ndash1381DOI 101126science1144066

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YoungMT LarvanMD 2010 Macroevolutionary trends in the skull of sauropodomorphdinosaursmdashthe largest terrestrial animals to have ever lived In Elewa AMT edMorphometrics for non-morphometricans Berlin Springer 259ndash269

Zanno LE Makovicky PJ 2011Herbivorous ecomorphology and specialization patternsin theropod dinosaur evolution Proceedings of the National Academy of Sciences of theUnited States of America 108232ndash237 DOI 101073pnas1011924108

ZelditchML Swiderski DL Sheets HD 2012Geometric morphometrics for biologists aprimer Amsterdam Elsevier Academic Press


Subjects Biodiversity Evolutionary Studies Paleontology Taxonomy ZoologyKeywords Ontogeny Sauropodomorpha Evolution Theropoda Skull shape DinosauriaHeterochrony Geometric morphometrics

INTRODUCTIONIn an evolutionary context heterochrony describes phenotypic changes due to shifts inthe timing or rate of developmental processes in an organism relative to its ancestorand can lead to significant evolutionary changes in body plans within relatively shortperiods of time (Gould 1977 Alberch et al 1979McNamara 1982 Reilly Wiley ampMeinhardt 1997 Klingenberg 1998McNamara amp McKinney 2005) Two major typesof heterochronic processes are discerned paedomorphosis and peramorphosis Paedo-morphosis occurs when the later ontogenetic stages of an organism retain characteristicsfrom earlier ontogenetic stages of its ancestor due to a truncation of the growth period(progenesis) decrease of the growth rate (neoteny) or a delayed onset of developmentalprocesses (postdisplacement) In contrast a peramorphic organism is ontogeneticallymore developed than the later ontogenetic stages of its ancestor due to the extension ofgrowth period (hypermorphosis) the increase of the growth rate (acceleration) or theearlier onset of developmental processes (predisplacement) (see Gould 1977 Alberch etal 1979 Klingenberg 1998) In practice evidence for heterochronic events in evolutioncan be detected by comparing the ontogenetic trajectories of different taxa under theconsideration of their phylogenetic interrelationships (Alberch et al 1979 Fink 1982)Thus the concept of heterochrony connects two main fields of biological sciencesdevelopmental and evolutionary biology (Gould 1977 Raff 1996) When studyingheterochrony ontogenetic trajectories are characterized by three separate vectors (sizeshape and ontogenetic age) which allows for quantification of heterochronic processeswith slope length and position within a Euclidean space (Alberch et al 1979) In thiscontext geometric morphometrics is a useful method for characterizing shape andsize vectors to investigate heterochrony in organisms within a multivariate framework(Mitteroecker Gunz amp Bookstein 2005)

Documentation of heterochrony in the vertebrate fossil record is limited Preserved fossilontogenetic series covering the whole postnatal development of fossil species are rare due tothe fact that early juvenile specimens are often either lacking or incomplete Furthermoreexact ages of single ontogenetic stages are often not available resulting in the temporalcomponent often being replaced by size which is not an ideal variable for age (Klingenberg1998 Gould 2000) Nevertheless the role of heterochrony has been recognized anddiscussed for the evolution of multiple fossil lineages that do preserve ontogenetic series(Balanoff amp Rowe 2007 Gerber Neige amp Eble 2007 Schoch 2009 Schoch 2010 Schoch2014 Bhullar 2012 Forasiepi amp Saacutenchez-Villagra 2014 Ezcurra amp Butler 2015) includingnon-avian dinosaurs (eg Long amp McNamara 1997 Erickson et al 2004 Guenther 2009Bhullar et al 2012 Canale et al 2014) For example Long amp McNamara (1997) Ericksonet al (2004) and Canale et al (2014) hypothesized that the evolution of large body size incarcharodontosaurids and tyrannosaurids from medium-sized ancestors was the result ofperamorphosis


































































Angle (PC 1ndashPC 2) 295357 15193 196691 40256 332773 355725 294664 655478 791993


Saurischia ndash




Orionides 37416 180843 136082 292517 ndash






OI107717peerj1589

1641




OI107717peerj1589

1741




















































































































































































































































































































Angle (PC 1ndashPC 2) 295357 15193 196691 40256 332773 355725 294664 655478 791993


Saurischia ndash




Orionides 37416 180843 136082 292517 ndash






OI107717peerj1589

1641




OI107717peerj1589

1741























































































































































































































































OI107717peerj1589

1741




















































































































































































































































cranial ontogenetic variation in early saurischians and the role of ... · keywords ontogeny,...

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