Multiple functions of a multi‐component mating pheromone in sea lamprey Petromyzon marinus

Abstract

The role of the C24 sulphate in the mating pheromone component, 7α,12α,24-trihydroxy-5α-cholan-3-one 24-sulphate (3kPZS), to specifically induce upstream movement in ovulated female sea lampreys Petromyzon marinus was investigated. 7α,12α-dihydroxy-5α-cholan-3-one 24-oic acid (3kACA), a structurally similar bile acid released by spermiated males, but lacking the C24 sulphate ester, was tested in bioassays at concentrations between 10(-11) and 10(-14) molar (M). 3kACA did not induce upstream movement in females or additional reproductive behaviours. In contrast, spermiated male washings induced upstream movement, prolonged retention on a nest and induced an array of nesting behaviours. Differential extraction and elution by solid-phase extraction resins showed that components other than 3kPZS + 3kACA are necessary to retain females on nests and induce nest cleaning behaviours. All pheromone components, including components in addition to 3kPZS + 3kACA that retain females and induce nest cleaning behaviours were released from the anterior region of the males, as had been reported for 3kPZS. It is concluded that the sea lamprey male mating pheromone has multiple functions and is composed of multiple components.

Evidence for partial overlap of male olfactory cues in lampreys

“…Components of complex signals can have different underlying functions and be shaped by different selective pressures (Candolin, 2003). In P. marinus, the major pheromone component 3kPZS elicits long-distance mate search (Siefkes et al, 2005;Johnson et al, 2009), while minor components probably facilitate close-proximity courtship behaviours (Johnson et al, 2012). Most pheromones identified in fish are released at relatively low rates, are likely to guide close-proximity spawning synchronization rather than mate search, and are hypothesized to represent receiver adaptations (Stacey, 2015).…”

“…In many insects, reproductive isolation is partially maintained through species-specific components, component ratios, or antagonists in pheromone blends (Symonds and Elgar, 2008). The importance of ratios in species-specific pheromone blends in vertebrates is generally poorly understood, but female P. marinus respond to the male pheromone when the blend is incomplete and when components are presented at various ratios (Johnson et al, 2009(Johnson et al, , 2012, although some ratios appear to be more effective Brant et al, 2016a). Likewise, our results, together with field observations of heterospecific spawning (Cochran et al, 2008), indicate that even partial overlap in lamprey odours may result in attraction to heterospecific odours.…”

“…Similarly, the physiological ability to detect an odour, such as that determined by EOG recordings, does not directly indicate that the odour elicits a behavioural response. For example, P. marinus sensitivity to 3-keto allocholic acid (Siefkes and Li, 2004) does not translate into a behavioural response (Johnson et al, 2012). Hence an alternative to the hypothesis that release of male pheromone components is partially shared among species is that commonly released compounds are not active pheromones in any species and that the compounds released by male I. unicuspis, I. fossor, I. castaneus and L. appendix that attracted female P. marinus in behavioural assays are not released by male P. marinus.…”

“…The major component 7α, 12α, 24-trihydroxy-5α-cholan-3-one-24-sulfate (3-keto petromyzonol sulfate, 3kPZS) guides female movement over long distances to the nest (Li et al, 2002;Siefkes et al, 2005;Johnson et al, 2009). Additional minor components that retain females in the area of the nest and elicit nesting behaviours remain unidentified (Johnson et al, 2012), but may include 3,12-diketo-4,6-petromyzonene-24-sulfate (DkPES; Li et al, 2013;Brant et al, 2016a) and petromyzestrosterol .…”

“…The odours of stream-resident larvae guide adult P. marinus during the migration into spawning streams (Teeter, 1980;Vrieze and Sorensen, 2001). Upon reaching the final stages of sexual maturation, males construct nests and signal with an odour that elicits upstream movement and nesting behaviours in females (Li et al, 2002;Siefkes et al, 2005;Johnson et al, 2012). The major component 7α, 12α, 24-trihydroxy-5α-cholan-3-one-24-sulfate (3-keto petromyzonol sulfate, 3kPZS) guides female movement over long distances to the nest (Li et al, 2002;Siefkes et al, 2005;Johnson et al, 2009).…”