The evolution of echolocation in bats: a comparative approach Alanna Collen A thesis submitted for the degree of Doctor of Philosophy from the Department of Genetics, Evolution and Environment, University College London. November 2012 Declaration Declaration I, Alanna Collen (née Maltby), confirm that the work presented in this thesis is my own. Where information has been derived from other sources, this is indicated in the thesis, and below: Chapter 1 This chapter is published in the Handbook of Mammalian Vocalisations (Maltby, Jones, & Jones) as a first authored book chapter with Gareth Jones and Kate Jones. Gareth Jones provided the research for the genetics section, and both Kate Jones and Gareth Jones providing comments and edits. Chapter 2 The raw echolocation call recordings in EchoBank were largely made and contributed by members of the ‘Echolocation Call Consortium’ (see full list in Chapter 2). The R code for the diversity maps was provided by Kamran Safi. Custom adjustments were made to the computer program SonoBat by developer Joe Szewczak, Humboldt State University, in order to select echolocation calls for measurement. Chapter 3 The supertree construction process was carried out using Perl scripts developed and provided by Olaf Bininda-Emonds, University of Oldenburg, and the supertree was run and dated by Olaf Bininda-Emonds. The source trees for the Pteropodidae were collected by Imperial College London MSc student Christina Ravinet. Chapter 4 Rob Freckleton, University of Sheffield, and Luke Harmon, University of Idaho, helped with R code implementation. 2 Declaration Chapter 5 Luke Harmon, University of Idaho, helped with R code implementation. Chapter 6 Joseph W. Brown, University of Idaho, and Rich FitzJohn, University of British Columbia, helped with R code implementation. 3 Abstract Abstract The evolutionary history of echolocation in bats is poorly understood, as fossils provide little direct evidence, and most studies into echolocation have taken an ecological approach. Bats use a wide variety of echolocation call structures despite facing similar sensory challenges, and it is not clear how and why these echolocation call types evolved, or what impact they have on other aspects of the evolution of bats. Here, I use phylogenetic comparative methods and newly-collated echolocation call data from 410 species in 120 genera and all 19 families to investigate the origination and evolution of echolocation in bats (Chiroptera). I construct an updated phylogenetic supertree of the bats using source phylogenies from the literature between 1970 and 2009. I ask three main questions: (1) Are echolocation call structures really a product of present- day ecological conditions, or are they much more constrained by evolutionary history than is currently thought? (2) What did the first echolocation calls sound like? (3) Are echolocation calls ‘key innovations’ that promote diversification? I found that early divergences and subsequent constraints in evolutionary history have resulted in a greater variety of bat call structures than appear to be functionally necessary. The structure of the first echolocation calls was predicted to be short duration, multi- harmonic, and narrowband, suggesting that the proto-bat was a slow and manoeuvrable flier with an opportunistic and omnivorous diet, and may have used a perch-hunting foraging strategy. Finally, some echolocation call types were found to correlate with higher diversification rates such that they may be considered key innovations, but, unexpectedly, the most rapidly diversifying clades were those in which species either did not use echolocation at all (Pteropodidae), or where less sensory reliance was placed on echolocation (Stenodermatinae: Phyllostomidae). 4 Acknowledgements Acknowledgements Firstly I would like to thank my supervisors: Kate Jones, who provided endless (!) advice and encouragement, and whose door was always open for scientific discussions and supportive chats. Helen Chatterjee, who, in particular, provided much-needed pastoral care throughout my PhD and championed my cause with UCL and NERC when Lyme Disease became too much. And Gareth Jones, who kept me thinking about the bats behind the comparative methods, and provided extremely useful comments on my drafts. Fundamental to all the analyses in my PhD were over 6,000 recordings of bat calls, made by the members of the ‘Call Consortium’ over a combined 150 years of bat-detecting. I am incredibly grateful to all of these bat scientists for giving me access to their hard-won echolocation calls. I hope EchoBank will go on to be the basis for many more studies of echolocation. In particular, I would like to thank David Jacobs for hosting me in South Africa, and for stimulating discussions about bat ecology whilst chasing his dog up Cape Town’s mountains. I also want to thank the interns who worked on EchoBank: Daniel Simmons, Huma Pearce, and Guo-Heng Chin, and fellow PhD student Charlotte Walters, whose contribution to EchoBank is substantial. Jen Crees, your contribution to my sanity was invaluable. Equally important was the bat supertree. Huge thanks to Olaf Bininda-Emonds who coached me through the supertree construction process, sent me Perl scripts, and gave up computing power to run the analysis. And was unfailingly kind and helpful throughout it all. Christina Ravinet also helped with supertree construction and I am very grateful for her contribution. I would also like to thank the following people for advice, inspiration and R help: Luke Harmon, Graham Slater, Rob Freckleton, Joe Szewczak, Kamran Safi, Rich FitzJohn, Bernd Brandt, Joseph Brown and Natalie Cooper. Thanks to NERC and CEE for funding the PhD. 5 Acknowledgements Finally, thank you to my unofficial supervisor, and fiancé, Ben Collen, for support, encouragement, methodological discussions, and indulging my concerns over my examiners’ opinions on everything from supertrees to split infinitives. 6 Table of Contents Table of Contents Declaration 2 Abstract 4 Acknowledgements 5 Table of Contents 7 List of Tables 9 List of Figures 11 1 Chapter 1: General Introduction 17 1.1 Introduction 17 1.2 Thesis aims and outline 32 2 Chapter 2: General Methods 35 2.1 Introduction 35 2.2 Call consortium 35 2.3 Recording echolocation calls 37 2.4 Digitisation 46 2.5 Field methods 47 2.6 The EchoBank database 50 2.7 Parameterisation 52 2.8 Echolocation data from the literature 59 2.9 Echolocation data for analyses 61 2.10 Conclusions 64 3 Chapter 3: A new supertree of bats (Chiroptera) 66 3.1 Abstract 66 3.2 Introduction 66 3.3 Methods 71 3.4 Results and Discussion 77 3.5 Conclusions 114 4 Chapter 4: Evolutionary constraint in echolocation call structure 116 4.1 Abstract 116 4.2 Introduction 117 4.3 Methods 122 4.4 Results 127 4.5 Discussion 157 7 Table of Contents 4.6 Conclusions 168 5 Chapter 5: The origin of echolocation in bats: what did the first echolocation calls sound like? 170 5.1 Abstract 170 5.2 Introduction 171 5.3 Methods 179 5.4 Results 183 5.5 Discussion 206 5.6 Conclusions 215 6 Chapter 6: Are echolocation call structures ‘key innovations’ that promote diversification? 216 6.1 Abstract 216 6.2 Introduction 217 6.3 Methods 224 6.4 Results 231 6.5 Discussion 243 6.6 Conclusions 253 7 Chapter 7: General Conclusions 255 7.1 The Evolution of Echolocation in Bats 255 8 Appendices 264 8.1 Appendix A: Species list: EchoBank and literature 264 8.2 Appendix B: References for echolocation data from the literature 283 8.3 Appendix C: References for bat supertree and list of source trees 292 8.4 Appendix D: Nodal support for bat supertree 312 8.5 Appendix E: Fossil calibration dates for supertree 334 8.6 Appendix F: Species list: Analyses 337 8.7 Appendix G: Species list and references for vocalisations 393 9 References 395 8 List of Tables List of Tables Table 1.1 Diversity of bat echolocation signals across families. 21 Table 2.1 Sound libraries containing bat echolocation call recordings. 36 Table 2.2 Contributors to the EchoBank Call Consortium. 37 Table 2.3 Detectors, recording devices and microphones used to make recordings stored in EchoBank. 39 Table 2.4 Explanations for release types of recordings stored in EchoBank. 46 Table 2.5 Species caught during fieldwork in Papua New Guinea and Australia in 2009. 50 Table 2.6 Metadata collected and stored in EchoBank. 51 Table 2.7 Parameters taken by SonoBat for each echolocation call. 57 Table 2.8 The echolocation call parameters selected for analysis. 62 Table 2.9 The transformations used for the parameter data analysed in subsequent chapters. 64 Table 3.1 Comparison of date estimates at major nodes between trees in the recent literature. 81 Table 4.1 The impact of variation in the three major components of echolocation call structure on functionality. 118 Table 4.2 The diversity of echolocation calls in bats: a comparison between the categories of Jones and Teeling 2006, and proposed new categories. 139 Table 4.3 The relative weights for the corrected Akaike Information Criterion scores for the three competing evolutionary models. 156 Table 4.4 The relative weights for the Bayesian Information Criterion scores for the competing evolutionary models.157 Table 5.1 Discrete categories used in ancestral character estimation. 182 Table 5.2 Estimated ancestral values at the root node for each of the echolocation call parameters. 193 9 List of Tables Table 5.3 Loadings of the eight call parameters onto the first three principal components. 196 Table 5.4 The reconstructed PCA scores at the root node using four ancestral reconstruction methods. 197 Table 5.5 Summary of the ancestral character estimates at the root node for the discrete echolocation call types. 200 Table 6.1 Speciation and extinction rates designated as either possible (p) or impossible (i).