Prostaglandin F2α drives female pheromone signaling in cichlids, revealing a basis for evolutionary divergence in olfactory signaling

Pheromones play essential roles in reproduction in many species. Prostaglandin F-2 alpha (PGF(2 alpha)) acts as a female reproductive hormone and as a sex pheromone in some species. An olfactory receptor (OR) for PGF(2 alpha) 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 Astatotilapia burtoni 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, A. burtoni males are insensitive to PGF(2 alpha), but they do exhibit strong preference for females injected with PGF(2 alpha). This attractiveness is independent of the PGF(2 alpha) hormonal receptor Ptgfr, indicating that this pheromone signaling derives from PGF(2 alpha) metabolization into a yet-undiscovered pheromone. We further discovered that fish that are insensitive to PGF(2 alpha) lack an ortholog for the OR Or114 that zebrafish use to detect PGF(2 alpha). These results indicate that PGF(2 alpha) 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.

Automated summary

Pheromones, such as PGF(2 alpha), are vital in reproductive processes in multiple species. The hormones are necessary for pheromone signaling, however, the specific signaling pathways can be different across species. Our study using Astatotilapia burtoni found that adult males strongly prefer odors of fertile females and the attractiveness is mediated through a yet-undiscovered pheromone derived from PGF(2 alpha) metabolism. Unlike zebrafish, A. burtoni males do not exhibit sensitivity to PGF(2 alpha), but prefer females injected with PGF(2 alpha), indicating a different signaling mechanism.