Olfactory cues provide critical information for spatial orientation of fish, especially in the context of anadromous migrations. Born in freshwater, juveniles of anadromous fish descend to the ocean where they grow into adults before migrating back into freshwater to spawn. The reproductive migrants, therefore, are under selective pressures to locate streams optimal for offspring survival. Many anadromous fish use olfactory cues to orient toward suitable streams. However, no behaviorally active compounds have been identified as migratory cues. Extensive studies have shown that the migratory adult sea lampreys (Petromyzon marinus), a jawless fish, track a pheromone emitted by their stream-dwelling larvae, and, consequently, enter streams with abundant larvae. We fractionated extracts of larval sea lamprey washings with guidance from a bioassay that measures in-stream migratory behaviors of adults and identified four dihydroxylated tetrahydrofuran fatty acids, of which (+)-(2S,3S,5R)-tetrahydro-3-hydroxy-5-[(1R)-1-hydroxyhexyl]-2-furanoctanoic acid was shown as a migratory pheromone. The chemical structure was elucidated by spectroscopies and confirmed by chemical synthesis and X-ray crystallography. The four fatty acids were isomer-specific and enantiomer-specific in their olfactory and behavioral activities. A synthetic copy of the identified pheromone was a potent stimulant of the adult olfactory epithelium, and, at 5 × 10−13 M, replicated the extracts of larval washings in biasing adults into a tributary stream. Our results reveal a pheromone that bridges two distinct life stages and guides orientation over a large space that spans two different habitats. The identified molecule may be useful for control of the sea lamprey.
|Original language||English (US)|
|Number of pages||6|
|Journal||Proceedings of the National Academy of Sciences of the United States of America|
|State||Published - Aug 21 2018|
Bibliographical noteFunding Information:
ACKNOWLEDGMENTS. We thank Soo Kyun Hur, Joey Riedy, Ethan Buchinger, Skye Fissette, Zak Smillie, Hayley O’Meara, Trevor O’Meara, and Zach Johnson for their assistance in field assays or fractionation; staff members of the US Geological Survey Hammond Bay Biological Station for access to that facility and for assistance in collection of and extraction of washings of larval sea lamprey; and the US Fish and Wildlife Service (Ludington Biological Station and Marquette Biological Station) and the Department of Fisheries and Oceans Canada (Sea Lamprey Control Centre) for supplying animals. This study was mainly funded by grants from the Great Lakes Fishery Commission (to W.L., K.L., C.O.B., and M.H.). G.M. received support from National Science Foundation Grant CHE-1404730, and T.R.H. received support from National Institute of General Medical Sciences Grant GM-65597.
- Anadromous migration
- Animal behavior
- Chemical ecology