Evolutionary Dynamics of Tyrannosauroid Dinosaurs

Home , Eotyrannus, Juratyrant, Kileskus, Maniraptoriformes, Nanuqsaurus, Tyrannosauroidea

Facultat de Ciències Memòria del Treball Final de Grau

Títol del treball:

Estudiant: Laia Garcia Escolà Grau en biologia

Correu electrònic: [email protected]

Tutor: Sandra Heras Mena

Cotutor: Albert Prieto Márquez

Empresa/institució: ICP (Institut Català de Paleontologia)

Vistiplau tutor (i cotutor):

Nom del tutor: Sandra Heras Mena ([email protected]) Nom del cotutor: Albert Prieto Márquez ([email protected])

Empresa/ institució: Institut Català de Paleontologia

Miquel Crusafont

Data de dipòsit de la memòria a secretaria de coordinació: 03/06/2019 Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

Abstract

This study explores the evolutionary dynamics of tyrannosauroid dinosaurs, a successful clade of basal coelurosaur theropods. This is accomplished by estimating rates of evolution using the Claddis R package. Morphological diversity was measured from discrete character data and estimates of evolutionary tempo on current phylogenetic hypotheses of tyrannosauroid relationships.

In this work it is shown the process to obtain the set of necessary documents to obtain the results with the script to finally calculated it with R.

In this set of previous documents are included a matrix character, that gather a series of different characters associated with the different taxa into the clade. It is also added a temporary range of each taxon and a consensus phylogenetic tree made by phylogenetic analysis under parsimony. All of them obtained through different software (Mesquite, TNT and R) and necessaries to run the script to obtain the seek resultants rates.

Evolutionary rates were estimated for different anatomical regions of the tyrannosauroid skeleton, including the skull and mandible, the post cranial body and the whole-body.

These phylogenetic trees include the rate calculation, the mode and tempo of changes produced in each node, to perceive possible acceleration or deacceleration of morphological evolution on the different branches of this clade.

To help with the conclusions and discussions of the study it is assessed a relationship between tyrannosauroid evolution and the body mass of their potential prey, ceratopsians and ornithopods through time.

The results indicate that the mandible was a driver of the increasing mass of the skull in tyrannosauroids, accompanied by an increase of the size of the posterior region of the skeleton and the reduction of the forelimbs. An important conclusion of this study is that the increasing skull size facilitates a greater bite force.

The relationship between tyrannosauroids body mass and that of their potential preys indicates that is boosting, which could be a case of arms race, being a potential cause of this mandible adaptation, which is supported by different studies.

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

Resum

Aquest treball estudia la dinàmica evolutiva dels dinosaures tiranosauroides, un exitós clade basal de teròpodes coelurosaures. Això s’aconsegueix mitjançant l'estimació de les taxes d’evolució utilitzant un paquet estadístic, anomenat Claddis, per al programa R. La diversitat morfològica es mesura a partir de dades de caràcter discret i estimacions del temps evolutiu sobre les hipòtesis filogenètiques actuals de les relacions dels tiranosauroides.

En aquests treball es mostra el procés per a obtenir un conjunt de documents necessaris per a poder obtenir els resultats a través d’un script i que puguin ser finalment calculats amb el programa estadístic R.

En aquest conjunt de documents anteriors s’inclouen una matriu de caràcters, que recull una sèrie de diferents caràcters associats als diferents tàxons del clade. També s’afegeix un rang temporal de cada taxó i un arbre filogenètic consens obtingut a partir d’un anàlisi filogenètic sota parsimònia. Tots ells, necessaris per executar l’script, obtenir les taxes resultants i obtinguts a través de diferents programes (Mesquite, TNT i R).

Les taxes evolutives es calculen per a cada region anatòmica de l’esquelet dels tiranosauroides, les quals es divideixen en el crani i la mandíbula, el crani sense la mandíbula, en el cos post cranial i en el cos sencer.

Aquests arbres filogenètics inclouen el càlcul de la velocitat, el mode i el temps dels canvis produïts a cada node, per percebre una possible acceleració o desacceleració de l’evolució morfològica a les diferents branques d’aquest clade.

Per ajudar amb les conclusions i la discussió sobre l’estudi, s’avalua la relació entre l’evolució de la massa corporal dels tiranosauroides i de les seves preses potencials, ceratopsians i ornitòpodes a través del temps.

Finalment, els resultats indiquen que la mandíbula va ser un dels principals motors en l’augment de la massa del crani en tiranosauroides, acompanyada d’un augment de la mida de la regió posterior de l’esquelet i la reducció de les extremitats anteriors. Una conclusió important d’aquest estudi és que l’augment de la mida del crani facilita una major força de mossegada.

La relació entre la massa corporal dels tiranosauroides i la de les seves preses potencials indica que està augmentant de manera similar, cosa que podria ser un cas d’ “arms race”, sent la causa potencial d'aquesta adaptació de la mandíbula i recolzada en diferents estudis.

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

Resumen

Este trabajo estudia la dinámica evolutiva de los dinosaurios tiranosauroides, un exitoso clado basal de terópodos coelurosaures. Esto se consigue mediante la estimación de las tasas de evolución utilizando el paquete estadístico Claddis para R. La diversidad morfológica se mide a partir de datos de carácter discreto y estimaciones del tiempo evolutivo sobre las hipótesis filogenéticas actuales de las relaciones de los tiranosauroides.

En este trabajo se muestra el proceso de obtención de un conjunto de documentos necesarios para el calculo mediante un script para R.

En este conjunto de documentos anteriores incluyen una matriz de caracteres, que recoge una serie de diferentes caracteres asociados a los diferentes taxones del clado. También se añade un rango temporal de cada taxón y un árbol filogenético consenso obtenido a partir de un análisis filogenético bajo parsimonia. Todos ellos, necesarios para ejecutar el script, obtener las tasas resultantes y obtenidos a través de diferentes programas (Mesquite, TNT y R).

Las tasas evolutivas se calculan para cada región anatómica del esqueleto de los tiranosauroides, las cuales se dividen en el cráneo y la mandíbula, el cráneo sin la mandíbula, en el cuerpo post craneal y en el cuerpo entero.

Estos árboles filogenéticos incluyen el cálculo de la velocidad, el modo y el tiempo de los cambios producidos en cada nodo, para percibir una posible aceleración o desaceleración de la evolución morfológica en las diferentes ramas de esta categoría filogenética.

Para ayudar con las conclusiones y la discusión sobre el estudio, se evalúa la relación entre la evolución de la masa corporal de los tiranosauroides y de sus presas potenciales, ceratopsians y ornitópodos a través del tiempo.

Finalmente, los resultados indican que la mandíbula fue uno de los principales motores en el aumento de la masa del cráneo en tiranosauroides, acompañada de un aumento del tamaño de la región posterior del esqueleto y la reducción de las extremidades anteriores. Una conclusión importante de este estudio es que el aumento del tamaño del cráneo facilita una mayor fuerza de mordida.

La relación entre la masa corporal de los tiranosauroides y la de sus presas potenciales indica que está aumentando de manera similar, lo que podría ser un caso de “arms race”, siendo la causa potencial de esta adaptación de la mandíbula y apoyada en diferentes estudios.

III

Index

Introduction ………….………………………..……….………..…..…… 2

Objectives ……………………………………………….……….…….…… 5

Methodology …………………………………………………………..…. 6

Ethics and sustainability …………..…………………………….… 11

Results ……………………………………………………………………… 11

Discussion ……………………………………………….………………… 20

Conclusion …………………………………………..……………………. 22

Acknowledgment …………………..…………………………….…… 22

References ………………………………………….…………………….. 23

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

Introduction

Tyrannosauroids, are a clade of theropod dinosaurs spanning the Middle Jurassic through the latest Cretaceous (Osborn, 1905; Gauthier, 1986; Brussate et al., 2010). Their fossil record is distributed among Eurasia, the Americas and Australia (Lyson, 2010) (Figure 1). Although is been revealed in recent studies that the distribution of tyrannosauroids could have been cosmopolitan it’s not formally probed, as some authors believed that tyrannosauroids were absent from the most arid paleoenvironments (Holtz, 2004).

Figure 1. Representation map of the tyrannosauroids distribution in an actual Earth map. Colours on the map match with the colours of the geological periods below.

This clade includes some of the most iconic carnivorous dinosaurs, such as Tyrannosaurus rex. Tyrannosauroids have been an iconic clade since the beginning of the twentieth century. (Osborn, 1905). For much of the century, these animals were included within the carnosaur group (Brussate et al., 2010). Carnosaurs included all the large theropods, some of them of gigantic size, like T. rex.

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

Before the advent of cladistics, the relationship of dinosaurs and other fossil organisms followed a Linnaean classification scheme. Subsequently, the implementation of cladistics let to the realisation of numerous monophyletic groups (clades) that did not fit within the Linnaean system.

Currently, some major clades may be assimilated into some Linnaean categories (Table 1). For example, Tyrannosauroidea has a rank of Superfamily, and Tyrannosaridae have a rank of Family (Table 1).

Table 1. Tyrannosauroid classification:

Kingdom Animalia

Phylum Chordata

Clade Dinosauria

Order Saurischia Suborder Theropoda

Subgroup Coelurosauria

Superfamily Tyrannosauroidea

Family Tyrannosauridae

Phylogenetically, tyrannosaurouids lie at the base of Coelurosauria (Figure 2,3), the most diverse subgroup of theropod dinosaurs (Turner et al. 2012).

Figure 2. Single most parsimonious cladogram of the Theropoda found in the present analysis. From Holtz, 1994. Coelurosauria indicated in green and Tyrannosauridae in blue.

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

Figure 3. Coelurosauria tree simplified from Senter, 2007. Coelurosauria indicated in green and Tyrannosauridae in blue.

Within tyrannosauroids, the more derived Tyrannosauridae are popularly known for their relatively massive skulls and undeveloped arms, which has attracted considerable attention from the scientific community (Holtz, 2004; Brusatte and Carr, 2016; Brett-Surman et al. ,2012; Holtz, 1994).

Remarkable tyrannosaurid synapomorphies include a specialized heterodont dentition, a derived squamosal-quadratojugal flange, a pneumatic basicranium and elongate hindlimbs bearing a pinched third metatarsal (Holtz, 2004) (Figure 4).

A C

Figure 4. A. Palatal view of Tyrannosaurus rex. The palatal shelves are used as an identification trait as this anatomical part on tyrannosaurids are more extensive than other large therapods (Holtz. Jr, 2004). B. Example of an heterodont dentition on the tyrannosauridae clade (T. rex) from Hurum and Sabath, 2003. C. Image of a pinched third metatarsal, also called Arctometatarsal.

One of the topics that have generated a considerable debate has concerned the diet of these animals, i.e. the discussion between whether they had a predator or a pure scavenger lifestyle. There is evidence in support of both lifestyles, that they could occasionally scavenge (Erickson et al., 1996; Farlow and Holtz, 2002), but also that they were natural predators with possible pack-hunting habits (Currie, 1998).

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

Even though their ecology is in constant discussion, is it known that tyrannosauroids include some of the largest known theropod taxa and constituted the apex predator of their niche (Benson et al., 2014). However, the basal members of this superfamily were small and svelte dinosaurs (Nesbitt et al., 2019) (Figure 5). This transition is barely numerical demonstrated because, nowadays, there is still existing several gaps in tyrannosauroid evolution as new discoveries are providing new phylogenetic hypotheses of this clade. Thus, for example, the recent discovery of a new mid-Cretaceous tyrannosauroid, Suskityrannus hazelae (Nesbitt et al., 2019) and even some intra−relationships of the Tyrannosauridae had been studied (Loewen et al., 2013), it does not exist a whole phylogenetic tree that grant numerical information about the velocity of the morphological changes in Tyrannosauroidea (Turner et al., 2012).

Figure 5. An example of the transition between a basal member of the clade (Guanlong) and the most recent one (T.Rex). Illustrations modified from Scott Hartman, 2014, and from the Smithsonian website.

In summary, they are a valuable clade for research and one of the most intensively studied extinct dinosaurs. Despite these studies, there are no analyses quantifying the evolutionary dynamics of their skeletal attributes, which may have been key in understanding the evolutionary success of the clade.

Objectives

This project contributes to our understanding of the mode and tempo of morphological evolution of Tyrannosauroidea. Specifically, it focuses on describing quantitatively the changes in the evolutionary rates of the Tyrannosauroidea clade while studying the morphological differences on the skeleton over time and in the different clades.

Those objectives will be fulfilled by implementing numerical techniques of macro-revolutionary analysis, aiming at shedding light into the most significant skeletal changes that led to the evolution of these carnivorous dinosaurs. The analysis also aims at disentangling rates of evolution of different regions of the tyrannosauroid skeleton in a phylogenetic and temporal context.

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

Methodology

The sampled taxa (Table 2) is based on an extensive dataset consisting of 366 discrete anatomical characters scored for the 28 tyrannnosauroids and 4 belonging to the outgroups, Allosaurus (Allosauroidea), Compsognatus (Compsognathidae), Ornithomimos (Ornithomimidae) and Maniraptora (Maniraptoriformes) (Brusatte and Carr, 2016; Brussatte et al. 2014)(Figures 2,3). A dataset obtained from the study of Brussatte and Carr (2016) that includes all valid terminal tyrannosaurid taxa, as this dataset has been updated and critically reviewed, discarding those that are already in our dataset or are invariant, among tyrannosauroids and those that we think are problematic redundant o difficult to understand (Brusatte and Carr, 2016)

Omitted taxa include Coelurus and Tanycolagreus for not having been established convincingly, Bagaaratan for being considered a chimaera and Alectrosaurus, Megaraptorans and Avyatyrannis for not including the wealth of data pertinent (Brusatte and Carr, 2016).

Table 2. Description of the taxa used and the stage age where they belong

TAXA FIRST LAST STAGE AGE SOURCE APPEARANCE APPEARANCE DATUM DATUM Allosaurus 155,7 150,8 Late Jurassic Holtz (1994) (Kimmeridgian- Early Tithonian) Maniraptora 168,3 0 Middle Jurassic Gauthier (1986) (Bathonian) - Holocene Ornithomimos 76.5 66,52 Late Cretaceous Holtz (1994) (Campanian- Maastrichtian) Compsogs 150,8 140 Late Jurassic Wagner (1861) (Tithonian)- Early Cretaceous (Berriasian) Kileskus 165 165 Middle Jurasasic Averianov et al. (2010) (Callovian) Guanlong 160 160 Late jurassic Xu Xing et al. (2006) (Oxfordian) Proceratosaurus 167,7 164,7 Middle Jurassic Von (1932) (Bathonian- Callovian) Yutyrannus 124,6 124,6 Early Cretaceous Xu Xing et al. (2012) (Aptian) Dilong 125 120 Early cretaceous Xu Xing et al. (2004) (Aptian) Sinotyrannus 145 145 Berrasiense Xu Xing et. Al (2004)

Eotyrannus 130 125 Early cretaceous Hutt et al. (2001) (Barremian-

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

Early Hauterivian) Juratyrant 149 149 Late Jurassic Brussatte and Benson (2013) (Tithonian) Stokesosaurus 155,7 150,8 Late Jurassic Madsen (1974) (Kimmeridgian- Tithonian) Xiongguanlong 112 112 Early Cretaceous Li et al. (2010) (Albian) Raptorex 70 70 Late Cretaceous Sereno et al. (2009) (Maastrichtian) Dryptosaurus 70,6 65,5 Early Paleocene Marsh (1877) (Early Danian) Late cretaceous (Maastrichtian) Appalachiosaurus 83,5 76 Late Cretaceous Carr et al. (2005) (Campanian) Albertosaurus 72,8 66,8 Late cretaceous Osborn (1905) (Campanian- Maastrichtian) Gorgosaurus 80 72,8 Late cretaceous Osborn (1905) (Campanian) A_remotus 75 70 Late Cretaceous Kurzanov (1976) (Campanian- Maastrichtian) A_altai 75 70 Late Cretaceous Brussatte, (2009) (Campanian- Maastrichtian) Qianzhousaurus 72 66 Late Cretaceous Lü et al (2014) (Maastrichtian) Daspletosaurus 80 72,8 Late cretaceous Daspletosaurus torosus Russell, (Campanian) (1970) D_n_sp - - - - (Daspletosaurus horneri) Tarbosaurus 70,6 68,5 Late Cretaceous Maleev (1955) (Maastrichtian) Tyrannosaurus 66,8 65,5 Early Paleocene Osborn (1905) (Early Danian) Late Cretaceous (Maastrichtian) Bistahieversor 74,5 74,5 Late Cretaceous Carr et al. (2010) (Campanian) Teratophoneus 77 76 Late cretaceous Carr et al. (2011) (campanian) Lythronax 80,6 79,9 Late cretaceous Loewen et al. (2013) (Campanian) Zhuchengtyrannus 83,5 70,6 Late Cretaceous Hone et al. (2011) (Campanian- Maastrichtian) Nanuqsaurus 69,1 69,1 Late Cretaceous Fiorillo and Tykoski (2014) (Maastrichtian)

Another important consideration was the selection of the outgroup taxa to Tyrannosauroidea. Outgroup taxa help to establish the direction of change of characters in the phylogeny (Lloyd, 2016). Typically, plesiomorphic characters are found in this outgroup taxa from which modifications occur (apomorphies) (Miley, 2011). They do serve an important function for rate analyses that incorporate phylogeny as they are vital to determinate ancestral states reconstructions and counts of character changes on branches.

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

A taxon-character state matrix was prepared (Figure 6). Discrete morphological characters were limited to a maximum of 32 states (Lloyd, 2016). The data may contain missing data, polymorphisms and uncertainties and have specifiable character weights.

…

Figure 6. An exemplar fragment from the 366-character matrix.

Continuous characters were converted to discrete ones. The way to incorporate continuous data is to convert the data into discrete ‘gap-weighted’ characters (Lloyd, 2016).

This character matrix is made with the program Mesquite, with data obtained from the study with a list of 366 different characters between all the specimens (Brusatte and Carr, 2016). These characters are selected according to the different anatomical parts of the body:

• Entire skeleton • Postcranium • Cranial: o Skull (mandible excluded) o Skull + mandible

The resulting matrix was used to infer the phylogenetic relationships of Tyrannosauroidea using Parsimony in the program TNT (Goloboff et al., 2008). The resulting most parsimonious trees were summarized in a strict consensus (Figure 7).

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

This phylogenetic tree, in Newick format, in combination with the dates for the sampled terminal taxa, are two key elements of the evolutionary rates analysis.

(0 ((3 (1 2 ))((5 (6 (4 (7 9 ))))(8 ((12 (10 11 ))(13 (15 (14 (16 (26 ((17 18 )((21 (19 20 ))((28 ((22 23 )(29 (24 25 ))))(27 30 )))))))))))))); proc/;

(Allosaurus, ((Compsogs, (Maniraptora, Ornithomimos )),((Guanlong, (Proceratosaurus, (Kileskus, (Yutyrannus, Sinotyrannus )))),(Dilong, ((Stokesosaurus, (Eotyrannus, Juratyrant )),(Xiongguanlong, (Dryptosaurus, (Raptorex, (Appalachiosaurus, (Bistahieversor, ((Albertosaurus, Gorgosaurus ),((Qianzhousaurus, (A_remotus, A_altai )),((Lythronax, ((Daspletosaurus, D_n_sp ),(Zhuchengtyrannus, (Tarbosaurus, Tyrannosaurus )))),(Teratophoneus, Nanuqsaurus ))))))))))))));

proc/;

Figure 7. Resultant tree from TNT. The first numbers belong to the taxa assigned. The phylogenetic position of the tyrannosauroids was inferred using parsimony. The taxonomic sample included 28 organisms. The data set consisted of 366 equally weighted morphological characters. A heuristic search of 10,000 replicates using random additional sequences was performed, followed by branch swapping by tree-bisection-reconnection holding ten trees per replicate.

A bootstrap analysis was also conducted in TNT to evaluate the repeatability of the inferred phylogenetic hypothesis. Setting the analysis for 5,000 replicates using heuristic searches, in which each search was conducted using random additional sequences with branch-swapping by subtree pruning and regrafting and 25 replicates, which reduces the number of topologies searched (Goloboff et al., 2008).

With the matrix and the consensus tree, we can run the script to obtain the different rates. The resulting rates of evolution are mapped on the consensus tree.

One of the uses of the resulting phylogeny is optimising characters. This consist on the visualization of the evolutionary tree of each character individually. The optimisation allows to study specific character tree’s and their state on every branch.

As mentioned before, rates were calculated in Claddis. Claddis is an R package that allows to perform disparity and rate analyses (Lloyd, 2016). Claddis aims to automate, simplify and supersede a previously made set of scripts specialized in rate analysis. This package allows to take directly NEXUS data for the inputs, a common data format developed to ease scientific

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà reports (Könnecke et al., 2015). For the purpose of this study Claddis is an efficient statistical program fitting because it has implemented a Brussate approach. This approach allows for establishing the calibration of the branches of the tree by using a likelihood approach, the ancestral states, that establishment admits internal nodes and branches to be incomplete as Claddis results depends on tree-based calculations (Lloyd, 2016). The calibration on the resultant tree follows the equal calibration method. This method divides the time between branches equally, which is a more neutral approach than the minimum branch length, a calibration method that calculates the amount of time to be proportional to the number of morphological characters and could result in biased outcomes (Brussate, 2011).

• Assessing the relationship between tyrannosauroid evolution and the body

mass of their potential prey

Additionally, this study investigates a correlation between tyrannosauroid body mass changes and those of potential prey taxa, as a change in the body mass of the latter might have driven similar modifications in the carnivores. It has been demonstrated that an important morphological transformation in tyrannosauroids involved changes the body mass (Hutchinson et al., 2014).

Most known tyrannosauroid taxa are found in the northern hemisphere and, based on this distribution, the potential prey consists of ceratopsians and ornithopods (Holtz, 1994) (Figure 8).

Figure 8. Image representation of the tyrannosauroid potential prey. Ornithopods on the left and ceratopsians on the right. Drawings made by Isis Masshiro and Nobu Tamura.

To facilitate the visualization of body mass changes of the different clades through time, the mass data is distributed in time bins of 10 million years.

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

Table 3. The different intervals used in the time classification of the prey and predator taxa:

Name of the interval. Age range (In Ma) A2 Before 166 A 166-156 B 156-146 B2 146- 116 C 116-106 D 86-76 E 76-66

Ornithopod and ceratopsian body mass data was obtained from Benson and Campione (2014) and that of tyrannosauroids from Lyson et al. (2010).

The lack of body mass information on some taxa is calculated using the equation Log 10 (femur length)-log 10 (body mass) from O’Gorman (2012).

Ethics and sustainability

As one of the objectives of this work is to make a sustainable study and with an ethical way of working, the print of different papers have been limited as the research has been made by computer, no mischief is done or intended to be on the through out of this study as it is recognised all the source of information, neither it is used of any program without the legal licenses on check.

Results

From the resulting 16 trees only four are selected. The selection criteria are based on the calibration technique, choosing the equal calibration method rather than the minimum branch length calibration. The optimal trees to work are the four trees resultants by selecting the node- based results. The node-based results could be more difficult to understand but they respond

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà better the question about to whether an entire clade has faster rates than other clades or the rest of the tree. The likelihood of acceleration (red) or deceleration (blue) in rates of evolution at the nodes of each clade is indicated as pie charts; an event of acceleration or deceleration is supported with a likelihood of 50% of more. The 4 trees belong to different parts of the skeleton. The first (Figure 9) show the evolutionary rates of the whole body, the second (Figure 10) shows the results from the postcranium part and the last ones (Figures 11-12) are from cranial characters.

• Whole skeleton

In the case of the whole body (Figure 9), there is evidence of an evolutionary deacceleration between the selected outgroup and Tyrannosauroidea. Subsequently during tyrannosauroid evolution, there is support for evolutionary accelerations before the splits of the terminal branches and a significant deacceleration on the last node. Exceptions appear to occur in the node of the D_n_sp and Daspletosaurus divergence, where there is not any change rate, neither in the split before Zhuchengtyrannus.

Focusing on the terminal branches there are only two significant rates, a deceleration took place between the split of Gorgosaurus and Albertosaurus, and an acceleration between D_n_sp and Daspletosaurus. The characters involved in these changes can be explained if we look at the other 3 resultant trees.

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

Figure 9. Resultant tree of the whole body. The rates are illustrated with pie charts of the acceleration (red) and deacceleration (blue). Bootstrap values represented with numbers on the tree. Outgroup represented in grey.

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

• Postcranium

No support was found for acceleration nor deceleration of evolutionary rates in the tyrannosauroid postcranium (Figure 10).

Figure 10. Resultant tree of the postcranium. The rates are illustrated with pie charts representing the acceleration (red) and deacceleration (blue). Bootstrap values represented with numbers on the tree. Outgroup represented in grey.

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

• Cranial characters

Evolutionary rate changes are found in the skull and mandible. Comparing both cranial trees (Figures 11 and 12), it is observed that the evolutionary rates are mostly equal. So, a thorough study is made to clarify the differences, counting with all the characters one by one changes, and the outcome is, that even the skull changes are continuous trough time, the driver of this skull changes is the mandible.

Between these trees there is only one distinctive rate, between Gorgosaurus and Albertosaurus split, with a deacceleration caused by the mandible as there is no support for rate changes in the skull tree.

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

Figure 11. Resultant tree of the mandible + skull. The rates are illustrated with pie charts representing the acceleration (red) and deacceleration (blue). Bootstrap values represented with numbers on the tree. Outgroup represented in grey.

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

Figure 12. Resultant tree of the Skull without the mandible. The rates are illustrated with pie charts representing the acceleration (red) and deacceleration (blue). Bootstrap values represented with numbers on the tree. Outgroup represented in grey.

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

• Ratio between Tyranosauroidea and prey body mass of potential prey

The results from the comparison between the body mass on different groups of tyrannosauroid prey, Ornithopoda and Ceratopsidae, and Tyrannosauroidea are established in the adjacent boxplot graphics, where each graphic represents these each of the 3 different groups of taxa (Figures 13-15).

o Tyrannosauridae

It can be observed in this graphic that the predator, tyrannosauroids, started increasing their body mass since the D period (86-76 Ma), same period when the variability of body mass in this group had variance between them, notable in the E period (76-66 Ma), when biggest tyrannosauroids existed (Figure 13).

Interval

Figure 13. Box plot executed with R Studio that represents the relation between the time period (Interval) indicated in the table 3 and the body mass of tyrannosauroids. Body mass in the Y axis and the interval time in the X axis (Table 3).

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

o Ornithopoda

In the case of Ornithopoda a notable increasing of body mass started in the B2 period (146- 116 Ma); however, the variability in this group decreased trough time (Figure 14).

Interval

Figure 14. Box plot executed with R Studio that represents the relation between the time period (Interval) indicated in the table 3 and the body mass of the Ornithopoda clade. Body mass in the Y axis and the interval time in the X axis (Table 3).

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

o Ceratopsidae

Ceratopsian body mass increases in the same period as Tyrannosauroidea, the D (86-76 Ma), and their variability increments on the E interval of time (76-66 Ma) (Figure 15).

Interval

Figure 15. Box plot executed with R Studio that represents the relation between the time period (Interval) indicated in the table 3 and the body mass of the Ceratopsidae clade. Body mass in the Y axis and the interval time in the X axis (Table 3).

Discussion

• Evolutionary rates.

These evolutionary rates on the nodes give a new insight to the morphological changes on this superfamily. The most important confirmation from the resultant trees is that the mandible is the driver of the evolution. Changes on the evolutionary rates of the morphology of the mandible could be caused principally by feeding adaptations.

Observing the last group of Tyrannosauroidea phylogenetic tree, tyrannosaurs, it is observed that their teeth present bear rows of serrations and the cranium appears equally well adapted

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà to resist biting and tearing loading of some of its taxa, like T. rex (Abler, 1992; Rayfield, 2004) . Moreover, the estimated bite-force of T.Rex and tooth mark evidence show that this skull characteristics, of the more recent taxa, allowed to resist bone impacts and a major withstand large bite forces (Erickson, 1996). Traits that could indicate that tyrannosauroids were not specialised into meat slicing which means that the shape of the mandibular corpus does not remain constant in time according to Therrien, 2005. These set of traits and adaptations support the resultant mandible rates, also related to a possible incrementation of the bite force.

• Ratio between Tyranosauroidea and prey body mass of potential prey

Figures 13,14, and 15 show a similar variation trough time between the preys’ group and the predator, meaning that a possible arms race could exist between tyrannosauroids and the potential preys.

Starting with a general low body mass on the time intervals A and B (Table 3). Ornithopods experienced a body mass increase before their predators did, on the interval B2, as tyrannosauroids body mass increase on the interval D along with the other prey grup, Ceratopsidae. Moreover, and although there is no fossil record in the period C on Ceratopsidae, the increase observed in the period D is more extreme than the increase in Tyrannosauroidea. This more extreme and earlier incrementation on Ceratopsidae could an example of an arms race, as the depredator increasing is slower because it is yet not fully adapted to the body mass increasing of their preys, other cause could be an possible change on their diet by turning them to scavengers as the preys get harder to haunt.

At the last period, the depredators have accomplished a higher body mass range than the prey groups.

Considering the graphic results (Figures 13-15) this skull development and body mass increasing could be caused by a body mass gain by the preys or a necessity to expand the prey range.

These changes on the body mass and the skull affects on the morphology of other parts of the body. The increase of the size skull may explain the development of the hindlimb and the miniaturization of the forelimb, since the centre mass of the body must compensate the increasing weight in the front part of the body (Henderson and Snively, 2004). It has been hypothesized that the large hip muscles in tyrannosaurs, and related theropod taxa, had to both retract the femur and balance the cranially positioned centre of mass, causing an incrementation

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà of the hindlimb. Changes on the centre of mass proved to be regular as these were even shifted in ontogeny, lowering the effective mechanical advantage in the hindlimbs (Hutchinson, 2014).

Otherwise, and for further discussion, it is discarded the possibility that a correlation between skull evolution and the intellectual capacity as it has been proved that the intelligence increased at a similar rate than cranial morphological attributes (Brett-Surman, 2012).

This rate study should complement previous studies of these taxa and give insight into the understanding of the mode and tempo of morphological evolution of Tyrannosauroidea.

Conclusion

The implementation of numerical techniques of macroevolutionary analysis made possible to describe changes in the evolutionary rates of Tyranosauroidea.

The mandible is the principal evolutionary driver in Tyrannosauroidea, entailing changes on the skull itself. This cranium size increase, to accomplish a strongest bite as the prey body mass is boosting, causes the body centre mass to cause a weight compensation on the postcranium with a relative reduction of the forelimb and an increase on the hindlimb.

Acknowledgment

To my tutor, Dr. Sandra Heras, to help me when I needed it, to always being interested of how this work was evolving and to give me advice even when something was out of her obligation as a tutor.

The same for my cotutor, Dr. Albert Prieto, from whom I learned a lot of new things about this branch of science that was new to me, as well as Dr. Albert García, who has been a third tutor for me in this work. And all the members of the Institut Català de Paleontologia, who have welcomed me and helped me whenever I needed it.

And as always for my parents and my brother, for the patience, the support and the trust they always have in me.

Finally, to all the teachers who have given me enough bases through my life to carry out this work.

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

References

− Abler, W. (1992). The Serrated Teeth of Tyrannosaurid Dinosaurs, and Biting Structures in Other Animals. Paleobiology, 18(2), 161-183. Retrieved from http://www.jstor.org/stable/2400997

− Averianov, A. O.; Krasnolutskii, S. A.; Ivantsov, S. V. (2010). A new basal coelurosaur (Dinosauria: Theropoda) from the Middle Jurassic of Siberia. Proceedings of the Zoological Institute 314 (1): 42-57.

− Benson, R. B., Campione, N. E., Carrano, M. T., Mannion, P. D., Sullivan, C., Upchurch, P., & Evans, D. C. (2014). Rates of dinosaur body mass evolution indicate 170 million years of sustained ecological innovation on the avian stem lineage. PLoS Biology, 12(5), e1001853. doi: 10.1371/journal.pbio.1001853

− Brett-Surman, Michael K. Holtz, Thomas R. Jnr. & Farlow, James O. (2012) The Complete Dinosaur: Life of the Past, (Second Edition) Indiana University Press

− Brusatte S. L., Carr T. D., Erickson G. M.,. Bever G. S, &. Norell M. A. (2009). A long-snouted, multihorned tyrannosaurid from the Late Cretaceous of Mongolia. Proceedings of the National Academy of Sciences 106(41):17261-17266

− Brusatte, S. L., & Carr, T. D. (2016). The phylogeny and evolutionary history of tyrannosauroid dinosaurs. Scientific Reports, 6, 20252. doi: 10.1038/srep20252

− Brusatte, S. L., Norell, M. A., Carr, T. D., Erickson, G. M., Hutchinson, J. R., Balanoff, A. M., ... & Xu, X. (2010). Tyrannosaur paleobiology: new research on ancient exemplar organisms. Science, 329(5998), 1481-1485.

− Brusatte, S.L. & Benson, R.B.J. (2013). The systematics of Late Jurassic tyrannosauroids (Dinosauria: Theropoda) from Europe and North America. Acta Palaeontologica Polonica, 58(1), 47-54.

− Brusatte, Stephen. (2011). Calculating the Tempo of Morphological Evolution: Rates of Discrete Character Change in a Phylogenetic Context. 10.1007/978-3-642-16271-8_4.

− Carr, T. D., Williamson, T. E., Britt, B. B., & Stadtman, K. (2011). Evidence for high taxonomic and morphologic tyrannosauroid diversity in the Late Cretaceous (Late Campanian) of the American Southwest and a new short-skulled tyrannosaurid from the Kaiparowits formation of Utah. Naturwissenschaften, 98(3), 241–246. doi:10.1007/s00114- 011-0762-7

− Carr, Thomas Williamson &Thomas & Schwimmer, David. (2005). A New Genus And Species Of Tyrannosauroid From The Late Cretaceous(Middle Campanian) Demopolis Formation Of

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

Alabama. Journal of Vertebrate Paleontology [J. Vert. Paleontol.].doi: 25. 119-143. 10.1043/0272-4634(2005)025<0119:angaso>2.0.co;2.

− Currie, P. J. (1998). Possible evidence of gregarious behavior in tyrannosaurids. Gaia, 15, 271-277.

− Erickson, G. M., Van Kirk, S. D., Su, J., Levenston, M. E., Caler, W. E., & Carter, D. R. (1996). Bite-force estimation for Tyrannosaurus rex from tooth-marked bones. Nature, 382(6593), 706.

− Farlow, J., & Holtz, T. (2002). The Fossil Record of Predation in Dinosaurs. The Paleontological Society Papers, 8, 251-266. doi:10.1017/S108933260000111X

− Fastovsky, David E. & Weishampel, David B.. (2005). Evolution and Extinction of the Dinosaurs. (2nd edition). Cambridge University Press.

− Fiorillo, A. R., & Tykoski, R. S. (2014). A Diminutive New Tyrannosaur from the Top of the World. PLoS ONE, 9(3), e91287. doi:10.1371/journal.pone.0091287

− Gauthier, J. 1986. Saurischian monophyly and the origin of birds. Memoirs of the California Academy of Sciences 8: 1–55.

− Goloboff, P.A., Farris, J.S. & Nixon, K.C., (2008). TNT, a free program for phylogenetic analysis. Cladistics 24, 774-786.

− Henderson, D. M., & Snively, E. (2004). Tyrannosaurus en pointe: allometry minimized rotational inertia of large carnivorous dinosaurs. Proceedings of the Royal Society B: Biological Sciences, 271(Suppl_3), S57–S60. doi:10.1098/rsbl.2003.0097

− Holtz, T. R. (2004). The phylogenetic position of the Tyrannosauridae: implications for theropod systematics. Journal of Paleontology, 68(05), 1100–1117. doi:10.1017/s0022336000026706

− Holtz, Thomas Jr. R. (1994).The phylogenetic position of the Tyrannosauridae: implications for theropod systematics. Journal of Palaeontology, 68(05), 1100–1117. doi:10.1017/s0022336000026706.

− Hone, D.W., Wang, K., Sullivan, C., Zhao, X., Chen, S., Li, D., Ji, S., Ji, Q., & Xu, X. (2011). A new, large tyrannosaurine theropod from the Upper Cretaceous of China. Doi :10.1016/j.cretres.2011.03.005

− Hutchinson, J. R., Bates, K. T., Molnar, J., Allen, V., & Makovicky, P. J. (2014). Correction: A Computational Analysis of Limb and Body Dimensions in Tyrannosaurus rex with Implications for Locomotion, Ontogeny, and Growth. PLoS ONE, 9(5), e97055. doi: 10.1371/journal.pone.0097055

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

− Hutt, S., Naish, D., Martill, D.M., Barker, M.J., & Newbery, P. (2001). A preliminary account of a new tyrannosauroid theropod from the Wessex Formation (Cretaceous) of southern England. Cretaceous Research, 22: 227–242.

− Könnecke, M., Akeroyd, F. A., Bernstein, H. J., Brewster, A. S., Campbell, S. I., Clausen, B., … & Wuttke, J. (2015). The NeXus data format. Journal of Applied Crystallography, 48(1), 301–305.doi:10.1107/s1600576714027575

− Kurzanov SM. (1976). A new Late Cretaceous carnosaur from Nogon-Tsav Mongolia. Sovmestnaâ Sovetsko-Mongolskaâ Paleontologiceskaâ Ekspeditciâ, Trudy 3:93–104

− Li, Da-Qing, Norell, Mark, Gao, Ke-Qin, Smith, Nathan & Makovicky, Peter. (2009). A longirostrine tyrannosauroid from the Early Cretaceous of China. Proceedings. Biological sciences / The Royal Society. 277. 183-90. 10.1098/rspb.2009.0249.

− Lloyd, G. T. (2016). Estimating morphological diversity and tempo with discrete character- taxon matrices: implementation, challenges, progress, and future directions. Biological Journal of the Linnean Society, 118(1), 131-151.

− Loewen, M. A., Irmis, R. B., Sertich, J. J. W., Currie, P. J., & Sampson, S. D. (2013). Tyrant Dinosaur Evolution Tracks the Rise and Fall of Late Cretaceous Oceans. PLoS ONE, 8(11), e79420. doi:10.1371/journal.pone.0079420

− Lü Junchang, Yi Laiping, Brusatte Stephen L., Yang Ling, Li Hua & Chen Liu. (2014). A new clade of Asian Late Cretaceous long-snouted tyrannosaurids. Nature Communications 5, Article nº 3788. doi: http://dx.doi.org/10.1038/ncomms4788

− Lyson, Tyler R & Longrich, Nicholas R. (2010). Spatial niche partitioning in dinosaurs from the latest cretaceous (Maastrichian) of North America. doi.org/10.1098/rspb.2010.1444

− Madsen (1974). A new theropod dinosaur from the Upper Jurassic of Utah. Journal of Paleontology 48: 27-31.

− Maleev, Evgeny A. (1955).New carnivorous dinosaurs from the Upper Cretaceous of Mongolia. Doklady, Academy of Sciences USSR 104 (5): 779-783.

− Miley. E. O. (2011). Phylogenetics theory and practice. (2n Edition).

− Nesbitt, S. J., Denton, R. K., Loewen, M. A., Brusatte, S. L., Smith, N. D., Turner, A. H.,.. & Wolfe, D. G. (2019). A mid-Cretaceous tyrannosauroid and the origin of North American end- Cretaceous dinosaur assemblages. Nature ecology & evolution, 1.

− Marsh. O. C. (1877). Notice of a new and gigantic dinosaur. American Journal of Science and Arts 14:87-88

− O’Gorman, E. J., & Hone, D. W. (2012). Body size distribution of the dinosaurs. PloS one, 7(12), e51925. doi: 10.1371/annotation/032ce6c0-22e3-4ae8-997a-40859bcb5609.

Evolutionary Dynamics of Tyrannosauroid Dinosaurs Laia Garcia Escolà

− Osborn, Henry F. (1905). Tyrannosaurus and other cretaceous carnivorous dinosaurs. Bulletin of the AMNH ; v. 21, article 14.g

− Rayfield, E. J. (2004). Cranial mechanics and feeding in Tyrannosaurus rex. Proceedings of the Royal Society B: Biological Sciences, 271(1547), 1451–1459. doi:10.1098/rspb.2004.2755

− Russell, Dale A. (1970). Tyrannosaurs from the Late Cretaceous of western Canada. National Museum of Natural Sciences Publications in Paleontology 1: 1-34.

− Senter, P. (2007). A new look at the phylogeny of coelurosauria (Dinosauria: Theropoda). Journal of Systematic Palaeontology, 5(4), 429–463.doi:10.1017/s1477201907002143

− Sereno P., Tan, L., Brusatte, S.L., Kriegstein, H.J., Zhao, X. & Cloward, K. (2009). Tyrannosaurid skeletal design first evolved at small body size. Science, online September 17. DOI: 10.1126/science.1177428.

− Therrien, F. (2005). Mandibular force profiles of extant carnivorans and implications for the feeding behavior of extinct predators. The Journal of Zoology (London) 267: 249-270.

− Turner, A. H., Makovicky, P. J., & Norell, M. A. (2012). A review of dromaeosaurid systematics and paravian phylogeny. Bulletin of the American museum of natural history, 1-206.

− Vargas. P & Zardoya. R. (2012). El árbol de la vida: sistemática y evolución de los seres vivos. (2nd edition). Madrid.

− Von Huene, F. (1932). Die fossile Reptil-Ordnung Saurischia, ihre Entwicklung und Geschichte. Monographien zur Geologie und Palaeontologie (Serie 1), 4: 1–361.

− Wagner, A. (1861). Neue Beiträge zur Kenntnis der urweltlichen Fauna des lithographischen Schiefers; V. Compsognathus longipes Wagner. Abhandlungen der Bayerischen Akademie der Wissenschaften 9: 30-38.

− Xu, X., Clark, J. M., Forster, C. A., Norell, M. A., Erickson, G. M., Eberth, D. A., … & Zhao, Q. (2006). A basal tyrannosauroid dinosaur from the Late Jurassic of China. Nature, 439(7077), 715–718. doi:10.1038/nature04511

− Xu, X., Norell, M. A., Kuang, X., Wang, X., Zhao, Q. & Jia, C. (2004). Basal tyrannosauroids from China and evidence for protofeathers in tyrannosauroids. Nature 431: 680-684. doi:10.1038/nature02855.

− Xu, Xing Wang, Kebai Zhang, Ke Ma, Qingyu Xing, Lida Sullivan, Corwin Hu, Dongyu Cheng, Shuqing Wang & Shuo. (2012). A gigantic feathered dinosaur from the Lower Cretaceous of China. Nature. 484. 92-5. 10.1038/nature10906.