A neural basis for password-based species recognition in an avian brood parasite

Obligate avian brood parasites are raised by heterospecific hosts and, therefore, lack crucial early exposure to relatives and other conspecifics. Yet, young brood parasites readily recognize and affiliate with others of their own species upon independence. One solution to this social recognition paradox is the ontogenetic 'password' mechanism used by obligate parasitic brown-headed cowbirds (Molothrus ater), whereby conspecific identification is initially mediated through the cowbird chatter: a non-learned vocal cue. We explored the neural basis of such password-based species recognition in juvenile and adult male cowbirds. We found that cowbird auditory forebrain regions express greater densities of the protein product of the immediate-early gene ZENK in response to the password chatter call relative to control sounds of mourning dove (Zenaida macroura) coos. The chatter-selective induction of ZENK expression occurs in both the caudal medial nidopallium (NCM) and the caudal medial mesopallium (CMM) in adults, but only within the NCM in juveniles. In contrast, we discovered that juvenile cowbirds exhibit neural selectivity to presentations of either conspecific or heterospecific songs, but only in CMM and only after recent experience. Juvenile cowbirds that did not have previous experience with the song type they were exposed to during the test period exhibited significantly lower activity-dependent gene expression. Thus, in juvenile male cowbirds, there is early onset of species-specific selective neural representation of non-learned calls in NCM and recently experienced song in CMM. These results suggest that NCM is evolutionarily co-opted in parasitic cowbirds to selectively recognize the password chatter, allowing juvenile cowbirds to identify adult conspecifics and avoid mis-imprinting upon unrelated host species. These ontogenetic comparisons reveal novel insights into the neural basis of species recognition in brood parasitic species.