From trait patterns to species lifetimes: Effects of niche differentiation on coexistence and community structure by Rafael D’Andrea Rocha A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy (Ecology and Evolutionary Biology) in The University of Michigan 2016 Doctoral Committee: Associate Professor Annette M. Ostling, Chair Professor Bradley Cardinale Professor Deborah E. Goldberg Professor Mercedes Pascual c Rafael D’Andrea Rocha 2016 All Rights Reserved Acknowledgements Annette Ostling, who tirelessly coached and supported me as a PhD student. Annette made a point to be always available for feedback on my work, even when she had tons of other things to do, which was all the time. She pushed me on when I faltered but was always friendly and never talked down to me. We collaborated closely—and intensely—on the papers we co-wrote. Her academic and financial support made possible my participation at numerous events that advanced my PhD career, including nine conferences, two courses and workshops, and two visits during her sabbatical year. She hired me twice as a GSI for her General Ecology class, which was an important learning experience, and also great fun. She introduced me to other ecologists, including James O’Dwyer, whose lab I will be joining after completing my PhD. Besides being there as my mentor and advisor, Annette doubled down as a friend and confidante. I am immensely grateful for the considerable amount of time and effort Annette dedicated to helping me during my five or six years at EEB. I would not be here without her. Mercedes Pascual, Deborah Goldberg, and Brad Cardinale, who generously agreed to join my committee and provided valuable guidance to improve the dissertation. Gyuri Barabás, my colleague, role model, collaborator, and good friend. Gyuri is an inspiration: devoted to science, incredibly smart, humble, and a heck of a great guy! I was lucky to join Annette’s lab when Gyuri was there. Rosalyn Rael, who was a postdoc in the lab when I joined. We collaborated on papers, enjoyed Indian food together, and had lots of laughs as ESA travel companions. John Vandermeer, for believing in my application to EEB despite my scant background in biology. Douglas Futuyma, whose Evolutionary Ecology course at Stony Brook started it all, and who suggested U of M. Jane Sullivan and Cynthia Carl, EEB Grad Coordinators who made my PhD life so much easier. NSF, EEB, and Rackham, for the funding. ii The University of Michigan, which provided me with so many resources as a graduate student. I feel privileged to have come here. Ann Arbor. I had a fantastic time in this exceptional town. I love it here, and I hope to come back often. All the great places I was able to visit in my travels for conferences, courses etc, including Austin, Portland, Minneapolis & St Paul, Sacramento, Baltimore, Ft Lauderdale, Miami, Berkeley, San Francisco, Maine, Wisconsin, Montreal, Quebec, Sao Paulo, Denmark, and Sweden. These were amazing experiences made possible by being an EEB PhD student in the Ostling lab. All the incredible people I met in Ann Arbor, especially Jordan Bemmels, John Guittar, Susan Cheng, and Sahar Haghighat. My family, for their unconditional love and support. Braeden, for his love, patience, and affection. iii Table of Contents Acknowledgements ::::::::::::::::::::::::::::::::::::: ii List of Figures ::::::::::::::::::::::::::::::::::::::::: vii List of Appendices :::::::::::::::::::::::::::::::::::::: ix Abstract :::::::::::::::::::::::::::::::::::::::::::: xi Chapter 1. Introduction ....................................1 1.1 Background . .1 1.2 Dissertation structure . .3 1.3 Publication status . .5 2. Challenges in linking trait patterns to niche differentiation ........7 2.1 Introduction . .7 2.2 Early trait pattern research: rise and fall of limiting similarity . .9 2.3 New perspectives and prospects on limiting similarity . 11 2.4 Recent empirical approaches in the context of past criticisms . 13 2.4.1 Is evenness to be expected? . 14 2.4.2 Identifying niche axes and multidimensionality . 16 2.4.3 The null model . 18 2.5 Further elements to be considered in trait research . 19 2.5.1 Emergent clusters . 20 2.5.2 Spatial scales . 22 2.5.3 Intraspecific variation . 23 2.6 Toward a theory of trait patterning under niche differentiation . 24 2.7 Conclusions . 26 2.8 Glossary . 27 2.9 Box 1: Trait-based metrics . 29 iv 2.10 Figures . 33 3. Species packing in nonsmooth competition models ............. 38 3.1 Introduction . 39 3.2 Background . 42 3.2.1 Models of competition around equilibria . 42 3.2.2 The fragility of continuous coexistence solutions . 44 3.3 Demonstrating robust continuous coexistence under kinked kernels 45 3.4 Kinked kernels and robust continuous coexistence . 46 3.5 How do kinked competition kernels emerge? . 50 3.5.1 Discontinuous utilization curves lead to kinked kernels . 50 3.5.2 Mechanisms inhibiting discontinuous resource utilization 52 3.6 Discussion . 54 3.7 Figures . 59 4. Revising the tolerance-fecundity tradeoff; or On the consequences of discontinuous resource use for limiting similarity, species diversity, and trait dispersion ................................... 64 4.1 Introduction . 64 4.2 The tolerance-fecundity tradeoff model . 67 4.2.1 Original formulation . 67 4.2.2 Revised formulation . 68 4.3 Comparisons between continuous and discontinuous tolerance function . 71 4.3.1 Tight packing . 71 4.3.2 Species diversity . 72 4.3.3 Trait dispersion . 74 4.4 Relation to competition kernel and generalization to other models . 75 4.5 Discussion . 77 4.6 Figures . 79 5. Niche differentiation does not guarantee higher species diversity, longer lifetimes, or lower extinction rates ....................... 84 5.1 Introduction . 84 5.2 Methods . 86 5.3 Results . 89 5.4 Discussion . 91 5.5 Figures . 93 v 6. Trait pattern under stochastic niche assembly: are species clusters a general phenomenon? ............................... 96 6.1 Introduction . 96 6.2 Methods . 98 6.3 Results . 101 6.4 Discussion . 104 6.5 Figures . 109 7. Can clustering in genotype space reveal niches? ............... 115 7.1 Introduction . 115 7.2 The Jeraldo et al. test . 117 7.3 Limitations of Jeraldo et al.’s null hypothesis . 118 7.3.1 The effect of mutations . 118 7.3.2 Immigration . 119 7.3.3 The gut microbiome . 120 7.4 Discussion . 121 7.5 Figures . 124 8. Dissertation summary and closing thoughts .................. 127 8.1 Dissertation summary . 127 8.2 Closing thoughts . 128 Appendices :::::::::::::::::::::::::::::::::::::::::: 131 Bibliography ::::::::::::::::::::::::::::::::::::::::: 195 vi List of Figures Figure 2.1 The d=w niche overlap rule . 33 2.2 Multidimensionality may mask species differences . 34 2.3 Emergent clusters . 35 2.4 Niche mechanisms and spatial scales . 36 2.5 Effect of intraspecific variation on competition . 37 3.1 Equilibrium patterns under a Gaussian competition kernel . 59 3.2 Equilibrium patterns under smooth nonanalytic competition kernels . 60 3.3 Equilibrium patterns under kinked competition kernels . 61 3.4 The effect of increasing perturbation size on model with kinked kernel . 62 3.5 Utilization curves of two species with traits x1 and x2 ............ 63 4.1 Visual representation of the tolerance-fecundity tradeoff ........... 79 4.2 Robust tight packing . 81 4.3 Kinked and smooth kernels lead to vastly different outcomes . 82 5.1 Neutral v. niche dynamics: local persistence times, richness, and extinction rates . 93 5.2 Baseline v. variant scenarios . 94 5.3 Effect of niches-to-species ratio . 95 6.1 Simulaton outcomes of MacArthur-Levins stochastic niche assembly with immigration . 109 6.2 Average standard score of the gap statistic across MacArthur-Levins scenarios110 6.3 Simulation outcomes of other niche mechanisms . 111 6.4 Average standard scores of gap statistic across other niche mechanisms . 112 6.5 Species lifetimes v. regional abundance, medoids . 113 6.6 Average standard score of established trait pattern metrics, CV trend . 114 7.1 Conceptual illustration of random and clustered genotype space . 124 7.2 Effect of mutation . 125 7.3 Effect of immigration . 126 I.1 Kinked v. smooth results in the competition-colonization tradeoff ..... 158 J.1 Species local persistence times v. local abundances . 159 J.2 Finite v. circular axis . 160 J.3 Fast v. slow niche sorting . 161 vii J.4 Species local persistence times v. local abundances . 163 J.5 Low v. high immigration . 164 J.6 Parabolic v. random intrinsic growth rate . 165 J.7 Niches-to-species ratios influence number of residents . 166 M.1 Simulation outcomes of all scenarios . 179 M.2 Gap curves of all scenarios . 180 M.3 Species lifetimes v. regional abundance for all scenarios . 181 M.4 CV trend, all scenarios . 182 M.5 Deterministic immigration-free outcomes . 183 M.6 Resource-consumer scenarios: low v. high resource depletion . 184 M.7 Effect of immigration on slow-sorting MacArhtur-Levins scenario . 185 P.1 Distribution of distances to nearest modal genotype driven by neutral drift and mutation . 194 viii List of Appendices Appendix A. Niche mechanisms and spatial scales: life history tradeoffs and example plant traits . 132 B. Existing research on the role of intraspecific variation to coexistence . 134 C. Two-species coexistence under smooth and kinked kernels . 136 D. Competition kernel as an overlap between sensitivities and impacts . 140.