Subtelomeric regions are often under-represented in genome sequences of eukaryotes. One of the best known examples of theuse of telomere proximity for adaptive purposes are the bloodstream expression sites (BESs) of the African trypanosomeTrypanosoma brucei. To enhance our understanding of BES structure and function in host adaptation and immune evasion, theBES repertoire from the Lister 427 strain ofT. bruceiwere independently tagged and sequenced. BESs are polymorphic in sizeand structure but reveal a surprisingly conserved architecture in the context of extensive recombination. Very small BESs doexist and many functioning BESs do not contain the full complement of expression site associated genes (ESAGs). Theconsequences of duplicated or missingESAGs, includingESAG9,anewlynamedESAG12, and additional variant surfaceglycoprotein genes (VSGs) were evaluated by functional assays after BESs were tagged with a drug-resistance gene.Phylogenetic analysis of constituentESAGfamilies suggests that BESs are sequence mosaics and that extensive recombinationhas shaped the evolution of the BES repertoire. This work opens important perspectives in understanding the molecularmechanisms of antigenic variation, a widely used strategy for immune evasion in pathogens, and telomere biology.