CHARACTERISING MACROEVOLUTIONARY PATTERNS WITHIN CROCODYLOMORPHA by PEDRO LORENA GODOY A thesis submitted to the University of Birmingham for the degree of DOCTOR OF PHILOSOPHY School of Geography, Earth and Environmental Sciences College of Life and Environmental Sciences University of Birmingham September 2018 University of Birmingham Research Archive e-theses repository This unpublished thesis/dissertation is copyright of the author and/or third parties. The intellectual property rights of the author or third parties in respect of this work are as defined by The Copyright Designs and Patents Act 1988 or as modified by any successor legislation. Any use made of information contained in this thesis/dissertation must be in accordance with that legislation and must be properly acknowledged. Further distribution or reproduction in any format is prohibited without the permission of the copyright holder. Abstract Crocodylians today comprise only 24 recognised species, and are often regarded as morphologically conservative. However, the fossil record of crocodylomorphs, which includes the extinct relatives of crocodylians, is much richer and extends over the last ~220 million years. This great biodiversity is reflected in their morphological disparity, with crocodylomorph species occupying a much wider range of ecological niches. Research effort has concentrated mostly on the description of new taxa and on placing them within the crocodylomorph evolutionary tree, and has greatly contributed to our understanding of crocodylomorph phylogeny and diversity. Nevertheless, another fundamental aspect of crocodylomorph macroevolution, morphological disparity, has only recently been the subject of quantitative scrutiny, with the focus often limited to specific subgroups rather than the entire clade. In this thesis, crocodylomorph morphological disparity is quantitatively assessed using distinct types of data. Body size patterns, characterised via a model-fitting approach, provide new insights into the adaptive landscape of crocodylomorphs. Patterns of cranial shape variation suggest an important link between ecological diversification and morphological disparity. Finally, the action of heterochrony, underlying remarkable cranial modifications in the crocodylomorph clade Notosuchia, is tested using geometric morphometrics. Together, these results represent a significant contribution to better understanding crocodylomorph phenotypic evolution. Aos meus pais. Acknowledgements I am deeply grateful to my supervisor Richard Butler, who offered me the opportunity to develop a project on the research field I always dreamed of, and was a constant source of support, advice and insights throughout my entire PhD. Richard will certainly be my inspiration if I am to become a supervisor in the future. I also thank my internal co- supervisors, Ivan Sansom and James Bendle, and especially my external co-supervisor, Roger Benson, for their ideas, discussions and comments on parts of this thesis. I am thankful to CAPES (Coordenação de Aperfeiçoamento de Pessoal em Nível Superior) and the University of Birmingham for jointly funding my PhD project. I also thank the financial support from Universitas 21, the Palaeontological Association, and the “Doris O. and Samuel P. Welles Research Fund”, from the University of California's Museum of Paleontology. I acknowledge the access to fossil specimens provided by Lorna Steel (NHMUK, London, UK), Zoltán Szentesi (MTM, Budapest, Hungary), Attila Ősi (MTM), Eliza Howlett (OUMNH, Oxford, UK), Matthew Riley (CAMSM, Cambridge, UK), Ronan Allain (MNHN, Paris, France), Rainer Schoch (SMNS, Stuttgart, Germany), Erin Maxwell (SMNS), Marisa Blume (HLMD, Darmstadt, Germany), Eberhard Frey (SMNK, Karlsruhe, Germany), Oliver Rauhut (BSPG, Munich, Germany), Max Langer (LPRP/USP, Ribeirão Preto, Brazil), Sandra Tavares (MPMA, Monte Alto, Brazil), Fabiano Iori (MPMA), Thiago Marinho (CPP, Peirópolis, Brazil), Jaime Powel (PVL, San Miguel de Tucumán, Argentina), Rodrigo Gonzáles (PVL), Martín Ezcurra (MACN, Buenos Aires, Argentina), Stella Alvarez (MACN), Alejandro Kramarz (MACN), Patricia Holroyd (UCMP, Berkeley, USA), Kevin Padian (UCMP), William Simpson (FMNH, Chicago, USA), Akiko Shinya (FMNH), Paul Sereno (UCRC, Chicago, USA), Tayler Keillor (UCRC), Mark Norell (AMNH, New York, USA), Carl Mehling (AMNH), Judy Galkin (AMNH), Alan Turner (SUNY, Stony Brook, USA), Liu Jun (IVPP, Beijing, China), Corwin Sullivan (IVPP), Zheng Fang (IVPP), Amanda Millhouse (USNM, Washington, D. C., USA). I thank all my colleagues from the Paleobiology research theme of the University of Birmingham, specially Dan Cashmore, Emma Dunne, Andy Jones and Juan Benito Moreno, for their help, assistance, and friendship. Further thanks to my Brazilian palaeontologist colleagues Julio Marsola, Gabriel Ferreira, Mario Bronzati, Felipe Montefeltro, Bruno Vila Nova, and Max Langer, who not only have been friends for many years, but also contributed to parts of this thesis. I also thank Trina Du, Louise Meunier and Hans Larsson, who provided me with an enjoyable and fruitful period at the Redpath Museum (McGill University). I express special appreciation to the many Brazilian friends that lived or are still living in Birmingham, including Carlos, Carol, Lais, Tupá, Julio, Dalila, Camila, Douglas, Jamila, José Carlos, Pedro, Tati, Mario, Mari, Samara, Vítor, Elis, Valter, Giana, Ravenna, David, Renata, Willians, Emily, Serginho, Paula, Walter, Rubens, and Glauco, as well as those living in London (Giu, Tarso and Victor) and Sheffield (Ligia and Matheus). Special thanks to my dearest friend Matheus, for his incredible companionship over more than 10 years. Finally, my sincere and immense gratitude to my family, Solange, João and Lucas, whose unconditional love and support were surely crucial for my engagement in research and ultimately led me to finish this thesis. And I extend my gratitude to Mariana, the most recent member of the family, for her affection and (intense) support, particularly during the last months before handing the thesis. Thank you, my love. Table of Contents Chapter 1: Introduction _____________________________________________________ 1 1.1. Taxonomic diversity versus morphological disparity in macroevolutionary studies _______ 2 1.2. The study group: Crocodylomorpha ____________________________________________ 4 1.3. Objectives ________________________________________________________________ 8 Chapter 2: Crocodylomorph body size evolution ________________________________ 9 2.1. Background _______________________________________________________________ 9 2.2. Material and Methods ______________________________________________________ 14 2.2.1. Proxy for body size ____________________________________________________ 14 2.2.2. Phylogenetic framework ________________________________________________ 17 2.2.3. Time-calibration ______________________________________________________ 21 2.2.4. Macroevolutionary analyses _____________________________________________ 23 2.2.5. Correlation with abiotic factors ___________________________________________ 29 2.3. Results __________________________________________________________________ 31 2.3.1. Comparative model-fitting analyses _______________________________________ 31 2.3.2. Appraising the SURFACE model fits ______________________________________ 33 2.3.3. Describing the body size macroevolutionary patterns in Crocodylomorpha _________ 39 2.3.4. Investigating the modes of body size evolution within Notosuchia and Crocodylia___ 48 2.3.5. The influence of palaeolatitude and palaeotemperature ________________________ 51 2.4. Discussion _______________________________________________________________ 56 2.4.1. The adaptive landscape of crocodylomorph body size evolution _________________ 56 2.4.2. Ecological diversification and its implications for crocodylomorph body size distribution _______________________________________________________________ 61 2.4.3. Cope’s rule cannot explain the evolution of larger sizes in Crocodylomorpha _______ 65 2.4.4. Correlation of crocodylian body size with global cooling ______________________ 68 2.4.5. Body size selectivity and diversification across Mesozoic boundaries _____________ 69 2.5. Conclusions ______________________________________________________________ 73 Chapter 3: Crocodylomorph cranial shape disparity _______________________________ 75 3.1. Background ______________________________________________________________ 75 3.2. Material and Methods ______________________________________________________ 78 3.2.1. Sampling and data collection_____________________________________________ 78 3.2.2. Phylogenetic framework ________________________________________________ 80 3.2.3. Geometric morphometric analyses ________________________________________ 82 3.2.4. Estimating disparity ____________________________________________________ 88 3.3. Results __________________________________________________________________ 91 3.3.1. Geometric morphometric analyses ________________________________________ 91 3.3.2. Disparity through time and between groups ________________________________ 105 3.4. Discussion ______________________________________________________________ 113 3.4.1. Assessing the different methods to minimise the effects of interobserver error _____ 113 3.4.2. Crocodylomorph cranial shape variation ___________________________________ 115 3.4.3. Crocodylomorph cranial shape disparity ___________________________________ 117 3.4.4. Ecological diversity and crocodylomorph