The genetics, biogeography and local adaptation of intraspecific variation in defense traits of Arabidopsis thaliana

Wild plant populations employ a variety of defense strategies to cope with the multitude of herbivorous and microbial pests that threaten their survival and reproduction each successive generation. Since these biotic threats can influence plant fitness and vary greatly across different environments, a geographic selection mosaic could result in population differentiation and local adaptation of defenses to regional pest cohorts at variable scales. Understanding how wild plant populations balance their natural defenses through space and time can aid in the development of crops optimally defended for the environments in which they will be cultivated, which is especially important for plants that are grown without pesticides or antibiotics. Unfortunately, little is currently known in regards to the scale and extent of local adaptation of plant defenses in wild relatives of crops, especially in terms of how multiple defense traits are balanced in natural populations. In this thesis, I investigate the spatial and temporal scale of natural variation in two important defenses of the Brassicaceae, glucosinolate concentrations and trichome density. Through a combination of genome-wide association mapping, genomic scans for signatures of selection, and analysis of field fitness data, I present evidence supporting local adaptation of constitutive defenses in the genetic model species Arabidopsis thaliana..;First, I examined the potential for local adaptation of the glucosinolate profiles of A. thaliana in vegetative tissues. I found that the 4- and 5-carbon chain, aliphatic glucosinolates were highly concentrated in accessions from the mild, oceanic climates of Western Europe, particularly in France and the United Kingdom, and the major epistatic loci associated with natural variation in their concentrations, GS-OH, GS-AOP and GS-ELONG, displayed strong signatures of natural selection in the genomes of the Arabidopsis Regional Mapping (RegMap) panel. Analysis of common garden field experiments in France revealed that local progoitrin concentrations and GS-OH alleles both positively influenced fitness in the field. Next, I examined the glucosinolate profiles of flowers and siliques to determine if glucosinolate concentrations of reproductive phase tissues follow different patterns of population differentiation or genetic associations. These reproductive tissues exhibited greater overall concentrations of glucosinolates but similarities with rosettes in their patterns of variation, with the short-chain alkenyl and hydroxyalkenyl glucosinolates displaying similar genetic associations and population differentiation across Europe, suggesting that glucosinolate profiles across different developmental phases are locally adapted in Western Europe through enhanced accumulation of alkenyl and hydroxyalkenyl glucosinolates. Finally, I examined the relationship between trichomes and glucosinolates, which are both constitutive defenses against herbivores that operate via different mechanisms of action: physical vs. chemical inhibition. I found that the hydroxyalkenyl glucosinolates and abaxial trichome density were positively correlated in a broad sample of accessions across Europe, with accessions from the Western range exhibiting the highest expression of both defenses. Utilizing a multi-trait mixed model association method, I found that SNP variation around an R2R3 MYB transcriptional regulator, ETC2, exhibits a common effect on trichome density and progoitrin concentration, suggesting that multiple anti-herbivore defenses are coordinately controlled by pleiotropic transcriptional regulators. Together these results highlight the importance of herbivore resistance in shaping the evolution of natural populations of A. thaliana and provide detailed evidence for local adaptation of constitutive defenses in Western Europe.;All the mapping panels and data used in this thesis are available as supplementary files.