Indel driven rapid evolution of core nuclear pore protein gene promoters

Abstract

Nuclear pore proteins (Nups) prominently are among the few genes linked to speciation from hybrid incompatibility in Drosophila. It was previously found that neuronal wiring underlying the female post-mating response induced by male-derived sex-peptide requires channel Nup54 functionality. A hot spot for rapid evolution in the promoter of Nup54 suggests a critical role for regulatory elements at the onset of speciation. Systematic analysis of Nup coding and promoter regions using Drosophila phylogenomics reveals that polymorphism differences between closely related Drosophila species in Nup coding regions do not generally evolve rapidly. Consistent with findings for Nup54, additional channel Nups 58 and 62 promotors are also hotpots for rapid accumulation of insertions/deletions (indels). Examination of Nup upstream regions reveals that core nuclear pore complex gene promoters accumulate indels rapidly. Since changes in promoters can have dominant effects (effects which directly impact gene expression of associated genes), these results indicate an evolutionary mechanism driven by indel accumulation in core Nup promoters. Compensation of such deleterious changes could lead to altered neuronal wiring, rapid fixation of adaptive traits and subsequently the rise of new species. Hence, the nuclear pore complex may act as a nexus for species-specific changes via nucleo-cytoplasmic transport regulated gene expression.