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Phylogeny and Extinction Risk in Mammals Luis Darcy Verde Arregoitia

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Phylogeny and Extinction Risk in Mammals Luis Darcy Verde Arregoitia Phylogeny and extinction risk in mammals Luis Darcy Verde Arregoitia A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2014 School of Biological Sciences 1 Abstract Detailed knowledge of the evolutionary relationships between species can inform studies in ecology and conservation. This phylogenetic information is becoming a recognized basis for evaluating conservation priorities. However, associations between species risk of extinction and the properties of a phylogeny such as diversification rates and phylogenetic lineage ages remain unclear. Limited taxon-specific analyses suggest that species in older lineages are at greater risk. Extinction due to chance events is more likely over time, or groups may become more specialized over time, reducing their potential to adapt to new conditions. This thesis has four main parts. The first aims to identify evolutionary characteristics that predict the fates of species, by testing for associations between lineage age, clade size, diversification rates, evolutionary distinctiveness and extinction risk for terrestrial mammals. There were no significant global or regional associations, and three significant results within two taxonomic groups. Extinction risk increases for evolutionarily distinct primates and decreases with lineage age when lemurs are excluded. Lagomorph species (rabbits, hares and pikas) that have more close relatives are less threatened. The second part of this thesis investigates why primate species in both younger and evolutionarily distinct lineages are more likely to be threatened. This section aims to identify the immediate causes of extinction risk (e.g. factors such as hunting and habitat loss and their variation in space) and how they relate to evolutionary history and species biology. The relationships between phylogeny and extinction risk are mediated by the evolutionary trend of increasing body size through time. Evolutionarily distinct primate species are smaller- bodied and thus more susceptible to the effects of habitat fragmentation. Species in younger lineages generally have larger body sizes. Larger species are preferentially hunted and reproductively less resilient. The third section of the thesis examines why lagomorph species with fewer close relatives are more likely to be threatened. The non-random extinction of small clades disproportionately threatens genetic diversity and phylogenetic history. This section explores the lagomorph phylogeny to test if differences in lagomorph evolution, biogeography and ecology explain current patterns of diversity and threat. Diversification was unrelated to climate, topography, geographic range size or geographic isolation. For lagomorphs in general, extinction risk was ii positively correlated with increasing human population density and negatively correlated with occurrence in anthropogenically modified habitat. Habitat generalists were less likely to be threatened, and paleoendemic species with few close relatives tend to be habitat specialists. The fourth and final section of the thesis expands on the use of phylogenies in ecology and conservation. This chapter aims to quantify ecological similarity between rodent species in order to compare it with phylogenetic relatedness. Results are related to ecological theory on ecological character displacement, and to conservation in the context of competition between introduced and native species. Morphological data can identify species with high probabilities of competing with invasive rats and house mice. The findings of this thesis contribute to our understanding of the patterns of threat to evolutionary history. The results in each section incorporate spatially explicit data on threats to mammals, and a process-based approach to interpreting the patterns of diversity. The inclusion of paleobiogeographic data provides more information on the origins of diversity and how to best preserve it. These research outputs can assist in planning and implementing actions to mitigate threats and conserve multiple measures of diversity. iii Declaration by author This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis. I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my research higher degree candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly stated which parts of my thesis, if any, have been submitted to qualify for another award. I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the General Award Rules of The University of Queensland, immediately made available for research and study in accordance with the Copyright Act 1968. I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis. iv Publications during candidature Peer-reviewed papers Verde Arregoitia, L.D., Blomberg, S.P. & Fisher, D.O. (2013) Phylogenetic correlates of extinction risk in mammals: species in older lineages are not at greater risk. Proceedings of the Royal Society B: Biological Sciences, 280, 20131092. Murray, K.A., Verde Arregoitia, L.D., Davidson, A., Di Marco, M. & Di Fonzo, M.M.I. (2014) Threat to the point: improving the value of comparative extinction risk analysis for conservation action. Global Change Biology, 20, 483-494. Publications included in this thesis Chapters 2-5 are included as papers in the format in which they were submitted for publication as encouraged by the University. Their supplementary materials appear at the end of each chapter. The text in these chapters is consistent with its published or submitted format. I use the plural first-person pronoun “we” because each chapter is a collaborative multi-authored paper. While efforts have been made to minimise the level of information overlap between papers, repetition of some material can be expected. Pages are numbered consecutively throughout the thesis for ease of use and a single bibliography is provided for brevity. All co-authors consented to the manuscripts being included in the thesis. In Chapters 1 and 6, where the body of the thesis is introduced, interpreted and summarised, the singular first-person pronoun “I” is used and chapters are referred to by chapter number. This format is consistent with the fact that Chapters 1 and 6 are the Candidate’s work while Chapters 2-5 are collaborative papers. v CHAPTER 2: Verde Arregoitia, L.D., Blomberg, S.P. & Fisher, D.O. (2013) Phylogenetic correlates of extinction risk in mammals: species in older lineages are not at greater risk. Proceedings of the Royal Society B: Biological Sciences, 280, 20131092. Contributor Statement of contribution Luis D. Verde Arregoitia (Candidate) Designed study (70%) Analysed data (80%) Wrote and edited paper (90%) Diana O. Fisher Designed study (30%) Wrote and edited paper (10%) Simon P. Blomberg Analysed data (20%) CHAPTER 3: Verde Arregoitia, L.D., Blomberg, S.P. & Fisher, D.O. Body size and threatened evolutionary history in primates (in preparation for submission) Contributor Statement of contribution Luis D. Verde Arregoitia (Candidate) Designed study (80%) Analysed data (70%) Wrote and edited paper (80%) Diana O. Fisher Designed study (20%) Wrote and edited paper (10%) Simon P. Blomberg Analysed data (30%) Wrote and edited paper (10%) vi CHAPTER 4: Verde Arregoitia, L. D., Leach, K., Reid, N., & Fisher, D.O. Diversity, extinction, and threat status in Lagomorphs (accepted pending major revisions, Ecography) Contributor Statement of contribution Luis D. Verde Arregoitia (Candidate) Designed study (85%) Analysed data (60%) Collected data (75%) Wrote and edited paper (70%) Katie Leach Analysed data (40%) Collected data (25%) Wrote and edited paper (10%) Neil Reid Designed study (15%) Wrote and edited paper (10%) Diana O. Fisher Wrote and edited paper (10%) CHAPTER 5: Verde Arregoitia, L. D. & Fisher, D.O. Likelihood of competition between invasive and native rodents revealed by global comparisons of morphological, ecological and phylogenetic similarity (in review, Journal of Mammalian Evolution) Contributor Statement of contribution Luis D. Verde Arregoitia (Candidate) Designed study (100%) Collected and analysed data (100%) Wrote and edited paper (60%) Diana Fisher Wrote and edited paper (40%) vii Contributions by others to the thesis Chapters 1 and 6 were written by the Candidate, with editorial advice from Diana Fisher. Simon Blomberg provided statistical advice for Chapters 4 and 5. Statement of parts of the thesis submitted to qualify for the award of another degree None viii Acknowledgements I am grateful for the excellent supervision from Diana Fisher, Simon Blomberg and Kerrie Wilson. Throughout the whole process they gave me guidance when I needed it, but they also trusted
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