Greater genetic and regulatory plasticity of retained duplicates in Epichloë endophytic fungi

Gene duplicates can act as a source of genetic material from which new functions arise. Most duplicated genes revert to single copy genes and only a small proportion are retained. However, it remains unclear why some duplicate genes persist in the genome for an extended time. We investigate this question by analysing retained gene duplicates in the fungal genus Epichloë, ascomycete fungi that form close endophytic symbioses with their host grasses. Retained duplicates within this genus have two independent origins, but both long pre‐date the origin and diversification of the genus Epichloë. We find that loss of retained duplicates within the genus is frequent and often associated with speciation. Retained duplicates have faster evolutionary rates (Ka) and show relaxed selection (Ka/Ks) compared to single copy genes. Both features are time‐dependent. Through comparison of conspecific strains, we find greater evolutionary rates in coding regions and sequence divergence in regulatory regions of retained duplicates than single copy genes, with this pattern more pronounced for strains adapted to different grass host species. Consistent with this sequence divergence in regulatory regions, transcriptome analyses show greater expression variation of retained duplicates than single copy genes. This suggest that cis‐regulatory changes make important contributions to the expression patterns of retained duplicates. Coupled with supporting observations from the model yeast Saccharomyces cerevisiae, these data suggest that genetic robustness and regulatory plasticity are common drivers behind the retention of duplicated genes in fungi.