The Pennsylvania State University The Graduate School GENETIC AND PHENOTYPIC SPATIAL VARIATION AMONG PLANT POPULATIONS A Dissertation in Plant Biology by Victoria Lynn DeLeo 2020 Victoria Lynn DeLeo Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy December 2020 The dissertation of Victoria Lynn DeLeo was reviewed and approved by the following: Jesse R. Lasky Assistant Professor of Biology Dissertation Advisor Chair of Committee John E. Carlson Professor of Plant Science and Ecosystem Science and Management Professor of Molecular Genetics and Director, Schatz Center for Tree Molecular Genetics Tanya Renner Assistant Professor of Entomology Liana T. Burghardt Assistant Professor of Plant Science Dorothy Foehr Huck & J. Lloyd Huck Early Career Chair Teh-hui Kao Distinguished Professor of Biochemistry and Molecular Biology Chair of the Intercollege Graduate Degree Program in Plant Biology iii ABSTRACT Evolution acts at the level of populations. From differences in allele frequencies or trait frequencies among populations, we can make inferences about the forces that are most important in selection and gene flow at a specific point in time for specific systems. In this dissertation, I used Arabidopsis thaliana and tropical trees to investigate variation in response to abiotic pressures across populations. I considered two of the biotic pressures that constrain abiotic adaptation: life history traits and animal dispersers. I modeled phenotypic change across a continent through time in response to understand how phenotypes vary in response to climate. Next, I modeled genetic phenological traits within and among populations and compared to phenological variation in the wild to examine the source of this potentially adaptive variation. Finally, I compared population structure between Metopium toxiferum and Bursera simaruba to investigate the importance of an abundant avian disperser in moving seeds across the landscape. I found regional differences in Arabidopsis response to abiotic pressures and evidence that some phenotypic change is constrained by axes of life history variation. I showed that genetic traits explain phenology trait distributions in the wild. I discovered that the large differences in population genetics between two tropical trees was not clearly related to the nesting behavior of an avian disperser. The patterns of variation we see across populations and along environmental gradients are likely shaped both by trait covariation within species and by community interactions. I argue that phenology has played a role in both of these factors and is an important consideration in plant adaptation at the population level. iv TABLE OF CONTENTS LIST OF FIGURES ................................................................................................................. vii LIST OF TABLES ................................................................................................................... xvi ACKNOWLEDGEMENTS ..................................................................................................... xviii Chapter 1 Introduction ............................................................................................................ 1 Chapter 2 Effects of two centuries of global environmental variation on phenology and physiology of Arabidopsis thaliana ................................................................................. 3 Abstract ............................................................................................................................ 3 Introduction ...................................................................................................................... 4 Materials and Methods ..................................................................................................... 10 Samples .................................................................................................................... 10 Leaf traits ................................................................................................................. 11 Phenology ................................................................................................................. 12 Statistical analysis .................................................................................................... 13 Results .............................................................................................................................. 17 Distribution of samples through time and space ...................................................... 17 Correlations among phenotypes (question 1) ........................................................... 19 Spatial variation in long-term average phenotypes (questions 2 and 3) ................... 19 Temporal change in phenotypes ............................................................................... 22 Phenotype associations with spatiotemporal climate gradients (questions 2 and 3) ....................................................................................................................... 24 Discussion ........................................................................................................................ 27 Intraspecific variation in life history and physiology shows little coordination along a single major axis (question 1) .............................................................. 28 Arabidopsis life history and physiology vary across spatial environmental gradients, suggesting adaptive responses to long-term environmental conditions (question 2) ..................................................................................... 29 Physiology, lack of correspondence to the Leaf Economic Spectrum ..................... 30 Phenology, high variation across space .................................................................... 32 Changes in Arabidopsis life history and physiology over the last two centuries track climate, suggesting adaptive responses (question 3) ............................... 32 Our approach, technical limitations in herbaria data to surmount in future studies ............................................................................................................... 35 Conclusion ................................................................................................................ 36 Acknowledgements .......................................................................................................... 36 References ........................................................................................................................ 37 Chapter 3 Genetic variation in phenology describes observed phenological variation in wild Arabidopsis thaliana populations ............................................................................ 38 Abstract ............................................................................................................................ 38 v Introduction ...................................................................................................................... 39 Materials and Methods ..................................................................................................... 43 Phenology data in the literature ................................................................................ 43 Additional flowering time and dormancy measurements ......................................... 44 Wild phenology ........................................................................................................ 45 Modelling collection day from genetic phenology ................................................... 46 Prediction of flowering time across native range with Generalized Additive Models .............................................................................................................. 47 Comparison of models ............................................................................................. 49 Flowering time distribution across native range ...................................................... 50 Maternal source effects ............................................................................................ 50 Results .............................................................................................................................. 51 Covariation in genetic phenology traits.................................................................... 51 Modelling wild phenology from genetic phenology values: .................................... 52 Genetic flowering time predicted by landscape flowering time ............................... 55 Does variance in genetic phenology in a region predict the variance of wild flowering times? ............................................................................................... 56 Discussion ........................................................................................................................ 61 Genetic variation in flowering time and dormancy can weakly predict variation in wild phenology among populations ............................................................. 63 Variation in genetic phenology can predict variation in wild phenology within populations ....................................................................................................... 64 Conclusion ................................................................................................................ 67 Acknowledgements .........................................................................................................