Electrophysiological evidence for detection and discrimination of pheromonal bile acids by the olfactory epithelium of female sea lampreys ( Petromyzon marinus )

Abstract

Electro-olfactograms were used to determine sensitivity and specificity of olfactory organs of female sea lampreys ( Petromyzon marinus) to four bile acids: 3-keto petromyzonol sulfate and 3-keto allocholic acid from spermiating males and petromyzonol sulfate and allocholic acid from larvae. Spermiating male bile acids are thought to function as a mating pheromone and larval bile acids as a migratory pheromone. The response threshold was 10(-12) mol l(-1) for 3-keto petromyzonol sulfate and 10(-10) mol l(-1) for the other bile acids. At concentrations above 10(-9) mol l(-1), the sulfated bile acids showed almost identical potency, as did the non-sulfated bile acids. The two sulfated bile acids were more potent than the two non-sulfated ones. In addition, 3-keto petromyzonol sulfate and water conditioned with spermiating males induced similar concentration-response curves and response thresholds. Cross-adaptation experiments demonstrated that the sulfated and non-sulfated bile acids represent different odors to the olfactory epithelium of females. Further exploration revealed that 3-keto petromyzonol sulfate represents a different odor than petromyzonol sulfate, while 3-keto allocholic acid and allocholic acid represent the same odor. Results indicate that male-specific bile acids are potent and specific stimulants to the female olfactory organ, supporting the previous hypothesis that these bile acids function as a pheromone.

Odorant organization in the olfactory bulb of the sea lamprey

“…During spawning migration, sea lampreys encounter a mixture of bile acid steroids released from larval sea lamprey in the streambed, and these larval odours have an important role in identifying a suitable river for spawning and larval rearing (Li et al, 1995;Sorensen and Vrieze, 2003). Once a spawning location is found, spermiated male sea lampreys release steroid pheromones, which induce movement/searching and spawning behaviours in ovulated female sea lamprey (Li et al, 2002;Siefkes et al, 2003;Siefkes and Li, 2004;Johnson et al, 2005Johnson et al, , 2009. Physiological studies have also investigated olfactory function in the sea lamprey.…”

“…Basic amino acids and a variety of steroid bile acids (including the lamprey pheromones) stimulate olfactory sensory responses from the main olfactory epithelium (e.g. Li et al, 1995Li et al, , 2002Li and Sorensen, 1997;Siefkes and Li, 2004;Sorensen et al, 2005;Johnson et al, 2009). However, the peripheral olfactory organ also houses abundant tubular diverticula known as the accessory olfactory organ (Hagelin and Johnels, 1955).…”

Bile acids as potential pheromones in pintado catfish Pseudoplatystoma corruscans (Spix & Agassiz, 1829): eletrophysiological and behavioral studies

“…Recently, it has been shown that bile acid profiles of lake trout (Salvelinus namaycush) are largely influenced by sex and maturation stage (Zhang et al, 2001) and that bile of female Rainbow trout (Oncorhynchus mykiss) contains a pheromone (Vermeirssen & Scott, 2001). Moreover, malespecific bile acids of sea lamprey (Petromyzon marinus) are potent and specific stimulants to the female olfactory organ (Siefkes & Li, 2004). Furthermore, electrophysiological studies demonstrated that an odotopic map of responses to bile acids and amino acids are represented in different regions of olfactory bulbs of chars (Salvelinus alpinus) and graylings (Thymallus thymallys) (Doving et al, 1980).…”

Olfactory sensitivity to bile fluid and bile salts in the European eel (Anguilla anguilla), goldfish (Carassius auratus) and Mozambique tilapia (Oreochromis mossambicus) suggests a `broad range' sensitivity not confined to those produced by conspecifics alone

“…Many species of fish have been shown to have an acute olfactory sensitivity to bile salts (Døving et al, 1980;Siefkes and Li, 2004;Zhang et al, 2001). Although the biological function of this phenomenon is unclear, with the notable exception of the sea lamprey Petromyzon marinus (Li et al, 2002;Polkinghorne et al, 2001;Sorensen et al, 2005), the stability and water solubility of the bile salt molecule makes it an ideal candidate for a role in chemical communication (Rosenthal and Lobel, 2006).…”

“…For example, behavioural evidence has shown that prey fish are able to recognise potential predators by olfaction (Kristensen and Closs, 2004;Rosenthal and Lobel, 2006). Furthermore, migration could involve olfactory detection of bile salts (Siefkes and Li, 2004).…”