Cold Comfort Diversification and Adaptive Evolution across Latitudinal Gradients By Stephanie Alexandra Stuart A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Integrative Biology in the Graduate Division of the University of California, Berkeley Committee in charge: Professor David D. Ackerly, Chair Professor Todd E. Dawson Professor Chelsea D. Specht Fall 2011 Abstract Cold Comfort Diversification and Adaptive Evolution across Latitudinal Gradients by Stephanie Alexandra Stuart Doctor of Philosophy in Integrative Biology University of California, Berkeley Professor David D. Ackerly, Chair Angiosperms originated during a prolonged climatic greenhouse, and their early fossil record comes exclusively from low paleolatitudes. Thus, the ancestral ecological niche of flowering plants was most likely tropical. Tropical origins have shaped the subsequent ecological boundaries and evolutionary opportunities faced by descendents of these ancestors. This has had profound consequences for the subsequent diversification and ecology of this large and important group. Here, these consequences are explored from three different points of view, and at three different scales, with the goal of understanding the evolution of freezing-tolerant clades and the traits that facilitate their survival. Chapter 1 begins with a broad view of angiosperm evolution, encompassing the entire clade at a global scale. It uses phylogenetically independent contrasts to test the relative contributions of area, latitude, and climate to diversification patterns through time. The analysis shows that expansions in latitudinal range, rather than expansions in total area, are the strongest correlate of increased diversification through the history of this clade. Phylogenetically independent results are then compared with present-day patterns. The present-day latitudinal diversity gradient is demonstrated to be the result of a tropical origin rather than intrinsically higher speciation rates in the tropics. The origin of the pattern seen in Chapter 1 is explored in Chapter 2, by examining whether greater functional diversity occurs in wet tropical environments, which are the putative ancestral niche of flowering plants, or through adaptation to seasonal environments. Three different rainforest sites in Australia are studied. A wet tropical community is contrasted with two seasonal communities: one which is seasonally dry, and another which is seasonally cold. A link between seasonality and increased functional diversity is demonstrated for traits relating to water use and cold tolerance. A new method is presented for testing the relative contribution of phylogenetic niche conservatism to shifts in trait means between communities. This method is used to demonstrate that, in these three forests, traits relating to successional status are conserved, while traits relating to water used and cold tolerance are evolutionarily labile. In Chapter 3, a specific hypothesis about the origins of cold tolerance is presented. It is argued that seasonally dry environments could provide an evolutionary stepping stone between wet tropical and 1 temperate environments, based on a known link between molecular mechanisms of drought and freezing acclimation. Individuals from seven eudicot clades are collected from the same system of wet tropical, dry tropical, and temperate forests used in Chapter 2. On being subjected to a controlled freezing profile, plants from the dry tropical forest show considerably more resistance to damage than their relatives from the wet tropical environment. This demonstrates that acclimation to drought is a plausible pathway for the evolution of tolerance to freezing. The latitudinal gradient from high species diversity in the tropics to lower diversity at near the poles is often attributed to the intrinsically stressful nature of growing in a seasonal environment. The work presented here refutes this point of view, showing how stress from one perspective can be seen as selective pressure from another. The selective pressures that resulted from transitions into temperate environments in angiosperms have led to more species, increased functional diversity, and greater resistance to unexpected conditions. 2 Table of Contents List of Figures ...................................................................................................................................................... iv List of Tables ........................................................................................................................................................ v Acknowledgements ............................................................................................................................................. vi Introduction .......................................................................................................................................................... 1 Earth’s history and the origin of modern-day temperate environments ................................................. 2 Flowering plant evolution in the context of past climates ......................................................................... 3 The evolutionary history of tolerance to cold ............................................................................................. 5 Chapter 1: Latitudinal span is a stronger predictor of species richness than area: Variety is the spice of life ........................................................................................................................................................................... 6 Introduction ...................................................................................................................................................... 6 Climate .......................................................................................................................................................... 6 Area ............................................................................................................................................................... 7 Time .............................................................................................................................................................. 7 Latitude and phylogenetic niche conservatism ....................................................................................... 7 Inverse gradients in diversification: temperate radiations ..................................................................... 8 What this chapter tests ............................................................................................................................... 8 Methods ............................................................................................................................................................ 8 Phylogeny and focal clade selection ......................................................................................................... 8 Family range mapping ................................................................................................................................ 9 Area, latitude, and longitude ...................................................................................................................... 9 Climate ........................................................................................................................................................ 10 Principal components analysis ................................................................................................................ 10 Phylogenetic methods ............................................................................................................................... 11 Phylogenetically independent contrasts for geographic data .............................................................. 12 Linear Model Analysis .............................................................................................................................. 13 Results ............................................................................................................................................................. 14 Results of the principal components analyses....................................................................................... 14 Latitude is the best predictor of diversification .................................................................................... 15 Discussion ....................................................................................................................................................... 17 Temperate, not tropical clades, have higher diversification rates ...................................................... 17 Latitude is a better predictor of species richness than area................................................................. 18 Time-for-diversification best accounts for the latitudinal gradient in species richness .................. 18 Conclusions .................................................................................................................................................... 19 Chapter 2: Functional diversification under contrasting seasonality in three Australian rainforest communities ........................................................................................................................................................ 20 Introduction ...................................................................................................................................................