1 2 Genus-wide comparison reveals divergence and evolution of the four sections within the 3 genus Claviceps are the result of varying mechanisms driving genome evolution and host 4 range 5 6 Abstract: 16 Background: 17 The genus Claviceps has been known for centuries as an economically important fungal 18 genera for pharmacology and agricultural research. Despite this little is known about its 19 evolution. Only recently have researchers begun to unravel the evolutionary history of the genus, 20 with origins in South America and classification of four distinct sections through ecological, 21 morphological, and metabolic features (Claviceps sects. Citrinae, Paspalorum, Pusillae, and 22 Claviceps). The first three sections are additionally characterized by narrow host range, while 23 sect. Claviceps is considered evolutionarily more successful and adaptable as it has the largest 24 host range and biogeographical distribution. However, the reasons for this success and 25 adaptability remain unclear.26Results: 27 Our study elucidates these factors by sequencing and annotating 50 Claviceps genomes, 28 representing 21 species, for a comprehensive comparison of genome architecture and plasticity 29 in relation to host range potential. Our results show the trajectory from specialized one-speed 30 genomes (C. sects. Citrinae and Paspalorum) to adaptive two-speed genomes (C. sects. Pusillae 31 and Claviceps) through co-localization of TEs around predicted effectors and loss of RIP 32 resulting in unconstrained tandem gene duplication coinciding with increased host range 33 potential and speciation.34 Conclusions: 35 Alterations of genomic architecture and plasticity can substantially influence and shape 36 the evolutionary trajectory of fungal pathogens and their adaptability. Furthermore, our study 37 provides a large increase in available genomic resources to propel future studies of Claviceps in 38 pg. 3 pharmacology and agricultural research, as well as, research into deeper understanding of the 39 evolution of adaptable plant pathogens. 40 41