Electrophysiological Measures of Olfactory Sensitivity Suggest That Goldfish and Other Fish Use Species-Specific Mixtures of Hormones and Their Metabolites as Pheromones

Abstract

Twenty years ago Kittredge et al. (1971) speculated that aquatic organisms may have evolved to use hormonal metabolites as sex pheromones. Their reasoning was simple: these compounds are pre-adapted for this function because they are naturally released to the environment in synchrony with important reproductive (endocrinological) events and their recognition might only require a simple mutation by which endocrine receptors are expressed on chemosensory tissue. Ten years later, Colombo et al. (1980) found that a fish, the male black goby (Gobius jozo) produces and releases a conjugated reduced androgen to water where it attracts ovulated females. Soon thereafter, Van den Hurk and Lambert (1983) reported that a mixture of two conjugated steroids, testosterone glucuronide and estradiol glucuronide, attracts male zebra danio (Brachydanio rerio). These exciting findings prompted us to test whether goldfish (Carassius auratus) also use hormonal metabolites as pheromones. Using electrophysiological measures of olfactory sensitivity (the electro-olfactogram or EOG) as a bioassay we discovered that goldfish are extremely sensitive to the steroidal maturation hormone 17α,20β-dihydroxy-4-pregnen-3-one (17,20βP) (see Sorensen, 1992). Subsequently we discovered that 17,20βP is released to the water where if functions as a preovulatory “primer” pheromone, increasing male gonadotropin (GtH) and milt (sperm and seminal fluid) production. Knowing that ovulated goldfish also release a pheromone which stimulates male behavior, we continued our pursuit of hormonal pheromones wing EOG recording to screen putative hormonal pheromones. We subsequently discovered that metabolites of prostaglandin F_2α (PGF_2α ) are likely released by recently ovulated fish to function as a postovulatory ‘releaser’ pheromone. A preliminary account of these findings was presented at Chemical Signals in Vertebrates V (Sorensen and Stacey, 1990), along with predictions that many other fish use hormonal metabolites as pheromones.