Complementary neural systems for the experience-dependent integration of mate-choice cues in European starlings

Choice of a particular mate phenotype may arise out of experience with the very phenotypes under consideration. Female European starlings (Sturnus vulgaris) prefer males that sing predominantly long-bout songs over males that sing predominantly short-bout songs, and thus, song-bout length is a phenotypic parameter instrumental in releasing the female's mate choice. The preferred long-bout songs induce higher expression of the immediate early gene (IEG) ZENK in the female auditory telencephalon than short-bout songs do, but this sensitivity to song length depends on the female's recent song experience. Here, we compared the experience-dependent modulation of ZENK with that of another IEG, FOS, and report that ZENK and FOS expression in the caudomedial mesopallium and caudomedial nidopallium show different modulation properties that complement natural variation in song-bout length. As reported previously, ZENK expression was greater in response to novel long-bout than to novel short-bout songs following a 1-week experience with long-bout but not short-bout songs. In contrast, FOS expression was greater in response to novel long-bout than to novel short-bout songs following a 1-week experience with short-bout but not long-bout songs. Thus, the ZENK and FOS signaling pathways are made sensitive to variation in song length by experiences with songs at opposite ends of the starling song-variation continuum, suggesting the presence of complementary neural systems made sensitive in register with the natural axis of phenotypic variation fundamental to the female's mate choice.