The Role of Biome Shifts in Lineage Diversification Esther Elizabeth Dale Submitted in fulfilment of the requirements for the degree of Doctorate of Philosophy Department of Botany, University of Otago November 2018 II Abstract This thesis examines the role of biomes in lineage diversification. It explores whether biome conservatism, the tendency to remain in ancestral biomes, constrains diversification, and tests whether biome shifts are linked to characteristics of particular biomes, clades or traits. This work focuses on a series of radiations in Australia and New Zealand. Using the hyper-diverse genus Acacia in Australia, Species Distribution Models (SDM) were used to predict distributions and niche traits of 481 species in 19 clades across two biome typologies. Diversification was not constrained to any biomes, with most species (94%) occupying multiple biomes, but diversification was greatest in those biomes currently occupying larger areas. New Zealand groups (Poaceae, Melicytus, Myrsine and Pseudopanax) with small scale radiations (< 25 species) were then investigated in relation to occupancy of the three main biomes (Forest, Open and Alpine). A temporal sequence of biome availability in New Zealand allowed an examination of diversification in the context of the directional transition from forest to more open biomes. A combination of methods including SDM, biogeographical models, and trait measurements of plants grown in a common garden were utilised to explore the importance of biome shifts during diversification, the relationship between trait shifts and biome shifts, and ask if biome conservatism was prevalent in the different clades. Biome conservatism did not constrain diversification in New Zealand lineages. Biome shifts were generally frequent and more closely related to extrinsic biome factors like biome age, biome availability and relative environmental similarity between biomes, rather than to intrinsic features of lineages, such as clade size, diversification rate or age. Traits of species differed predictably by biomes occupied, and biome shifts between highly contrasting biomes (Forest and Alpine) were accompanied by biologically important trait changes. An intermediate number of biome shifts promoted maximum diversification, while low and very high biome shift frequencies dampened diversification. Diversification in New Zealand lineages typically started in Forest, before shifting into different biomes. Multiple biome occupancy and cross-biome diversification were common features of these lineages. Biome conservatism, based on the proportion of taxa occupying the ancestral III biome, was evident in many lineages, despite more recent shifts into different biomes. Current methods for assessing biome conservatism are methodologically problematic in lineages that contain species that occupy multiple biomes. A new biome conservatism index is proposed, based on calculating the proportion of taxa that occupy the ancestral biome. This work demonstrates that biomes are a useful habitat scale for examining eco-evolutionary processes shaping the diversification of lineages. IV Acknowledgements Thanks to my team of supervisors. Bill Lee, for so many great conceptual conversations and keeping me focused on the big questions. Steve Higgins for getting me started and reminding me to think globally. David Orlovich for stepping in when I needed a new Botany supervisor and encouraging comments. Matt Larcombe for stepping in, in particular with assistance with the TTR modelling, and always giving detailed comments. Andrew Tanentzap and Javi Igea for having me visit to work on Chapter 3, and for teaching me a bunch of useful analyses. Also, the rest of the Ecosystems and Global Change group and the Forest Ecology and Conservation group at University of Cambridge for being so welcoming during my visit. Thanks to Ben Potter for constructing the phylogenies in Chapters 3 and 4. Thanks to the Manaaki Whenua – Landcare Research and GNS Dunedin site community for fostering a great research environment, all the interesting tearoom conversations and words of wisdom. In particular, my office mates, Gretchen and Hayley, for encouragement and help with a variety of things from the technical to the practical. Angela for sourcing the colonisation dates for Poaceae clades and many helpful conversations. In the Department of Botany, thanks to my office mates; Hadley O’Sullivan for assistance with the freezer system (especially the 90s computer!) and server; Vicky Tomlinson and Rebecca Macdonald for help with sourcing equipment for the electrolyte leakage measurements; Susan Mackenzie for assistance with the experimental plants; Stewart Bell for help in the field; Kath McGilbert and Michelle McKinlay for assistance with various forms and orders crucial to keeping the science going. A huge thanks to Auckland Botanic Gardens, Dunedin Botanic Gardens, Otari Wiltons Bush, Manaaki Whenua-Landcare Research Lincoln, University of Auckland, V Acknowledgements Ribbonwood Native Plant Nurseries, The Department of Conservation, Emma Bodley, Kate Caldwell, Bev Clarkson, Jim Clarkson, Shannel Courtney, Peter de Lange, Rewi Elliot, Peter Heenan, Peter Johnson, Finn Michalak, Greg Nelson, Louise van der Salm, and Ines Schönberger for access to plant material and/or help with collecting material. Also, the Peter Bannister Student Field Grant for a grant towards field work. Peter Bellingham, Bruce Clarkson, Peter de Lange, Peter Johnson, Kelvin Lloyd, and Chris Lusk provided helpful advice on the biomes occupied by the NZ lineages examined. Daphne Lee, Bruce Hayward, and Dallas Mildenhall provided information on macrofossils and pollen records. Thanks to Jocelyn Dale for proof-reading. Thank you to the holders of National Vegetation Survey data that permitted me to use their data sets, including Hugh Wilson, the Otago Peninsula Biodiversity Group and the LUCAS programme programme for the Ministry for the Environment. In addition, I acknowledge Ngāti Hei, Ngāti Kuri, and Ngāti Wai for allowing me to use data previously collected within their rohe. To my friends and family, both in Dunedin and further afield, people of Leith, thanks for meals, care packages, coming to visit and words of encouragement, you’re the best! Thanks to Mum and Dad for instilling in me a love of learning and all the different ways you, along with Alwyn, Meredith and Godfrey, have been supportive of this. VI Contents Abstract .......................................................................................................... III Acknowledgements ......................................................................................... V General introduction: What is a biome shift? ........................ 1 1.1 What are biomes? ........................................................................................ 1 1.2 What is biome occupancy? .......................................................................... 2 1.3 What are biome shifts? ................................................................................ 3 1.4 What is biome conservatism? ..................................................................... 5 1.5 Why Australasia? ......................................................................................... 7 1.6 Thesis outline .............................................................................................. 10 Diversification is decoupled from biome conservatism in Australian Acacia ........................................................................................... 13 2.1 Introduction ................................................................................................ 13 2.2 Methods ....................................................................................................... 16 2.2.1 Biome concepts ...................................................................................... 16 2.2.2 Clade selection ....................................................................................... 17 2.2.3 Modelling species distributions ............................................................. 18 2.2.4 Biome occupancy ................................................................................... 19 2.2.5 Diversity, niche size and biome relationships ........................................ 20 2.2.6 Phylogenetic signal in biome occupancy ............................................... 21 2.2.7 Specialisation to soil .............................................................................. 21 2.3 Results ......................................................................................................... 22 VII Contents 2.3.1 Species biome specialisation.................................................................. 22 2.3.2 Clade biome specialisation .................................................................... 23 2.3.3 Diversification in relation to biomes...................................................... 24 2.3.4 Sampling effort of presence points ........................................................ 27 2.3.5 Specialisation to soil .............................................................................. 29 2.4 Discussion ................................................................................................... 29 2.5 Conclusion .................................................................................................. 36 Biome shifts and diversification of New Zealand Poaceae .. 37 3.1 Introduction...............................................................................................