Most models of speciation by sexual selection assume that reproductive isolation is driven by divergence in female mating preferences.  However, we still know little about the evolvability of preference functions, whether they exhibit constraint, and how their specific properties evolve.  Thus, I imposed artificial selection on Drosophila athabasca (WN), utilizing no-choice mating trials on females accepting divergent Inter-Pulse-Interval (IPI) male courtship songs, a key target of species recognition.  Response to selection resulted in increased female acceptance of low and high IPI songs by 30 and 26% in only 10 generations, respectively.  Females selected to mate in the presence of high IPI songs akin to its sibling D. mahican (EA) increased their matings to the same level as with their conspecific IPI songs.  In contrast, females selected to accept low IPI songs relaxed choosiness; increasing acceptance of both low and high IPI songs with no evidence of peak preference shift.  These divergent responses to selection suggest that choosiness and peak preference can both evolve.  Finally, selection was mostly driven by dominant alleles, supporting “Haldane’s sieve” and raising the question of their maintenance.  Overall, these results imply that sexual selection systems can be easily destabilized in nature.