The origin and maintenance of diversity in British Euphrasia (Orobanchaceae)

Plant species exhibit extensive diversity due to various evolutionary processes such as speciation, polyploidisation, hybridisation, and shifts in mating system, which can rapidly generate novelty. The maintenance of this diversity subsequently depends on both biotic and abiotic factors that may lead to population expansion or extinction. The taxonomically complex genus Euphrasia in Britain and Ireland, with its great diversity in ploidy, mating systems, and ecology, serves as an ideal system to address fundamental questions about the origins and maintenance of plant diversity. The overarching aim of this thesis is to elucidate the evolutionary mechanisms driving diversity in this rapid radiation at both inter- and intra-species levels. First, we use genotyping-by-sequencing and spatially-aware clustering methods to investigate genetic structure across 378 populations spanning 18 British Euphrasia species, including diploids and tetraploids with varying mating systems (Chapter 2). The rest of the thesis performs more focused comparisons of the distinct selfing species E. micrantha and the mixed-mating species E. arctica. This includes a phylogeographic analysis using chloroplast and nuclear ribosomal DNA (Chapter 3), and an assessment of the impact of mating systems on genetic structure using nuclear SNP data (Chapter 4). Finally, a common garden experiment investigates ecological adaptation by measuring plant performance in different soil pH and host conditions (Chapter 5). The population genetic study reveals permeable species boundaries, with genetic clustering largely by geography rather than species identity. Notably, only northern Scottish populations of E. micrantha show clear genome-wide divergence from other species. Incongruence between plastid and nuclear ribosomal genomes within E. micrantha reveals different evolutionary histories. While cpDNA indicates postglacial expansion with distinct East and West dispersal in Scotland, nrDNA suggests ongoing hybridisation with other species, signifying local hybridisation. Nuclear SNP data show high inbreeding coefficients and many runs of homozygosity in both E. micrantha and E. arctica, showing of the profound genomic consequences of self-fertilisation in Euphrasia. However, occasional outcrossing may rescue the long-term loss of diversity and result in evolutionary novelty. From an ecological perspective, the common garden study found that soil pH significantly influenced the performance of Euphrasia species. Notably, E. micrantha displayed a narrower pH tolerance compared to E. arctica, highlighting the importance of edaphic specialisation, which may play a role in Euphrasia speciation. These findings offer insights into the complex evolutionary pressures shaping Euphrasia’s diversity and highlight the need to study how the interactions between selfing, hybridisation, polyploidy and edaphic specialisation impact speciation in other plant lineages