Prostaglandin F_2α drives female pheromone signaling in cichlids, revealing a basis for evolutionary divergence in olfactory signaling.

Abstract

Pheromones play essential roles in reproduction in many species. Prostaglandin F_2α (PGF_2α) acts as a female reproductive hormone and as a sex pheromone in some species. An olfactory receptor (OR) for PGF_2α was recently discovered in zebrafish, but this signaling pathway is evolutionarily labile. To understand the evolution of signals that attract males to fertile females, we used the African cichlid <i>Astatotilapia burtoni</i> and found that adult males strongly prefer fertile female odors. Injection of a prostaglandin synthesis inhibitor abolishes this attractivity of fertile females, indicating these hormones are necessary for pheromonal signaling. Unlike zebrafish, <i>A. burtoni</i> males are insensitive to PGF_2α, but they do exhibit strong preference for females injected with PGF_2α. This attractiveness is independent of the PGF_2α hormonal receptor Ptgfr, indicating that this pheromone signaling derives from PGF_2α metabolization into a yet-undiscovered pheromone. We further discovered that fish that are insensitive to PGF_2α lack an ortholog for the OR Or114 that zebrafish use to detect PGF_2α. These results indicate that PGF_2α itself does not directly induce male preference in cichlids. Rather, it plays a vital role that primes females to become attractive via an alternative male OR.