Imperial College of London Department of Earth Sciences and Engineering An Appraisal of the ‘Living Fossil’ Concept Dominic John Bennett Submitted in part fulfilment of the requirements for the Degree of Philosophy in the Department of Earth Sciences and Engineering of Imperial College London The copyright of this thesis rests with the author and is made available under a Creative Commons Attribution Non- Commercial No Derivatives licence. Researchers are free to copy, distribute or transmit the thesis on the condition that they attribute it, that they do not use it for commercial purposes and that they do not alter, transform or build upon it. For any reuse or redistribution, researchers must make clear to others the licence terms of this work. Bennett © 2017 ii “When I use a word,” Humpty Dumpty said, in rather a scornful tone, “it means just what I choose it to mean – neither more nor less.” ‘Through the Looking Glass’ by Lewis Carroll iii ABSTRACT Although the term ‘living fossil’ has been around for over 150 years, it remains scientifically undefined and contentious. Generally, it refers to any taxon that is evolutionarily unique, species-poor and exhibits traits closely resembling those of extinct taxa. This interpretation, however, is not universal. Other interpretations of the term include species that are evolutionary dead-ends, taxa that were first discovered in the fossil record and/or lineages that have undergone no (sic) morphological change. In addition to the confusion over definition, many have argued against the concept on the grounds that it is either not feasible, that it may not delineate a true category of biodiversity or that it recalls defunct Victorian scientific ideas. Despite these objections, it is evident that the concept of the living fossil can play an important role in our understanding of evolution over large timescales. In recent years there has been renewed interest in the concept of the living fossil thanks to the development of genomic techniques that are revealing previously hidden rates of molecular change in well-known living fossils. Additionally, many species that have been described as living fossils are threatened with extinction and there exists a risk that their unique evolutionary history is being lost. In this thesis, I attempt a re-appraisal of the living fossil concept. Firstly I test whether the concept of the living fossil can be made scientifically sound. Secondly I develop a new quantitative definition of the living fossil. I show that the concept is robust as it can be used to distinguish lineages that have experienced different rates of evolution. In addition I demonstrate that it is possible to devise a quantitative definition, which I use to identify living fossils and their traits across a wide range of taxonomic groups. iv CONTENTS 1. Introduction ........................................................................................................... 1 2. Testing the Living Fossil with a Tree-Growth Model ............................................. 36 3. Testing the Living Fossil with the Fossil Record .................................................... 65 4. Developing New Metrics for the Living Fossil ........................................................ 98 5. Identifying Shared Ecological Characteristics of the Living Fossil ......................... 120 6. Coding the Living Fossil ...................................................................................... 151 7. Conclusions ........................................................................................................ 178 References ................................................................................................................ 187 Appendix ................................................................................................................. 216 v ACKNOWLEDGEMENTS I wish to thank all those who have made the realisation of this thesis possible. To my mother and father for their proofreading, patience and quiet abode. I am grateful to Francisco ‘Pancho’ Reyes Leiva, Rebekah ‘Becky’ Thorne and Christian ‘Oh Stupid Big Feet’ Potiszil for all the climbing and board games – I would not have survived so many of those slow days of non-progress otherwise. I am thankful to Denis Vega and Peipei Wang, witnesses of my amazing throwing skills. I would also like to thank all those at the zoo who helped me, offered words of advice and a friendly ear. Jessica ‘Gibbon Girl’ Bryant for crosswords, cats and crisps. Simon ‘Lion Man’ Dures and Gaby ‘a-Dormouse’ Peniché for falafel Fridays and fun. James ‘Elephant Bird King’ Hansford for the oo-ing and R-ing, the beer-ing and the tea-ing. Also a big thanks to Jon Bielby for the chats, tea and having the faith in me to hold your baby, Freya. Also to Susy Echeverría-Londoño thanks for the coffees and cakes (but not always the cinema). Finally, many thanks to both my supervisors, Mark Sutton and Sam Turvey, both of whom devised this PhD topic. You both had the faith in me to pursue the topic as I saw fit and provided the help and support whenever I needed it. vi FOREWORD This thesis is entirely my own work but with substantial help and suggestions from my supervisors, Mark Sutton and Sam Turvey. Any content that is not my own is properly referenced. This thesis has been written as a single continuous piece of work, it should, however, be noted that large sections of chapters two and six have been published in peer-reviewed journals. Refer to references Bennett et al. (2017a) and Bennett et al. (2017b). Additionally, chapter four is currently under review for publication. The appendix contains supplementary materials in the form of tables, figures and additional text. Supplementary tables and figures are indicated with ‘S’ before the figure/table number. Supplementary text is indicated to the reader by the main document’s text. Supplementary data too large for textual representation are stored electronically in the attached CD; see files ‘chapter_4.zip’ and ‘chapter_6.zip’. vii ABBREVIATIONS AIC …………………… Akaike Information Criterion ANOVA …………………… Analysis of Variance DE …………………… Dead End Scenario ED …………………… Evolutionarily Distinct EDBMM …………………… Evolutionary Distinctness Biased Markov Model Eph …………………… Ephemeral Scenario EPI …………………… Evolutionary Performance Index ERMM …………………… Equal Rates Markov Model ES …………………… Equal Splits FP …………………… Fair Proportion GAM …………………… General Additive Model GLS …………………… Generalised Least Squares Hyd …………………… Hydra Scenario International Union for the Conservation of IUCN …………………… Nature LF …………………… Living Fossil LMEM …………………… Linear Mixed Effects Model MY …………………… Millions of Years MYA …………………… Millions of Years Ago NCBI …………………… National Center for Biotechnology Information Pan …………………… Panchronic Scenario PD …………………… Phylogenetic Diversity PE …………………… Pendant Edge pEPI …………………… Proximate Evolutionary Performance Index PF …………………… Phylogenetic Fuse Scenario PSV …………………… Phylogenetic Species Variability viii LIST OF TABLES Table 1.1 Living fossils Are Not Well Studied ...................................................................................................... 3 Table 1.2 Examples of Living Fossils ....................................................................................................................... 6 Table 1.3 Living Fossil Synonyms .......................................................................................................................... 13 Table 1.4 Separating the Paleaobiotic and the Neobiotic ............................................................................ 25 Table 1.5 Estimated Evolutionary Distinctnesses .......................................................................................... 31 Table 2.1 Tree Shape Statistics ............................................................................................................................... 51 Table 2.2 Clade Shape Statistics ............................................................................................................................. 53 Table 3.1 Epoch-Epoch Midpoints ......................................................................................................................... 76 Table 3.2 Linear Models of EDt1~EDt0 ................................................................................................................. 84 Table 3.3 Non-Linear Models of EDt1~EDt0 ....................................................................................................... 85 Table 3.4 Expected Linear Models of EDt1 .......................................................................................................... 87 Table 4.1 Top pEPI Living Fossils ........................................................................................................................ 108 Table 4.2 Top EPI Living Fossils ........................................................................................................................... 111 Table 4.3 Species Counts by Group ..................................................................................................................... 113 Table 5.1 Factors Affecting Extinction ............................................................................................................... 123 Table 5.2 Factors Affecting Speciation .............................................................................................................. 124 Table 5.3 Assembled Variables ............................................................................................................................