Fish courtship pheromone uses the brain's smell pathway

May 30, 2016, RIKEN
PGF2α activates two ventromedial glomeruli in the zebrafish olfactory bulb, as revealed by neural activation marker (pERK: red). Green: GFP-expressing olfactory axons, blue: glomerular structure visualized with anti-SV2 antibody. Credit: RIKEN

Research at the RIKEN Brain Science Institute in Japan has revealed that a molecule involved in fish reproduction activates the brain via the nose. The pheromone is released by female zebrafish and sensed by smell receptors in the noses of the males. The neural pathway and brain areas involved in transforming this molecular messenger into courtship behavior in fish were also identified and reported in Nature Neuroscience on May 30.

Prostaglandin F2α (PGF2α) is a reproductive hormone in female and mammals that is involved in ovulation and uterine contraction. In fish, it is also pheromone—a social and sexual signaling molecule used to attract the opposite sex—that is secreted by females in their urine. Males will normally swim toward even small concentrations of the molecule, but the researchers, led by Yoshihiro Yoshihara, found that male fish without a sense of smell were indifferent when PGF2α was added to their tank.

PGF2α synchronizes reproductive behaviors between female and male zebrafish, but how this happens was unknown. Having confirmed that sensory tissue responsible for smelling was needed for males to sense PGF2α, researchers then found that the only type of neurons activated by it are ciliated . The team then searched for the receptor within these neurons that detects PGF2α.

Contrary to expectations, the key players were not prostaglandin receptors. Molecular labeling revealed that PGF2α only bound to two specific olfactory receptors. These olfactory receptors are evolutionarily quite different from prostaglandin receptors, and the same or corresponding olfactory receptor genes are present in other fish and mice, which indicates that a similar mechanism for reproductive communication might be present within other species.

PGF2α activates a ventromedial glomerulus in the zebrafish olfactory bulb, as revealed by neural activation marker (pERK: red). A neighboring glomerulus is negative for pERK. Green: GFP-expressing olfactory axons, blue: DAPI staining. Credit: RIKEN

The researchers also found that through these olfactory receptors, PGF2α activates a direct, dedicated to the areas of the brain that are responsible for eliciting courtship behavior in male fish. The ciliated olfactory sensory neurons send their signals to specific regions called glomeruli in the of the brain, which in turn relay them to distinct forebrain areas. This "labeled line", in which circuits only transmit information about particular stimuli from a limited number of receptors, is also how the sense of taste functions. Hardwired pathways like this are common for innate behaviors, says Yoshihara, and it may have been an evolutionary accident that the PGF2α molecule was well-matched to certain olfactory receptors, facilitating the use of the "smell pathway" for reproductive purposes.

Finally, the researchers tested the response to PGF2α in male fish that were lacking the genes for one of the they had identified. These fish weren't drawn to PGF2α in their tank, spent less time chasing female fish, and were less successful at spawning. A smell receptor thus seems to be the gateway for PGF2α into the brain. Pheromone signaling works hand in hand with other senses like vision to bring about the courtship dance that increases a fish's chances of mating.

Male zebrafish are attracted to the pheromone PGF2α, which is released by female zebrafish during courtship. As proof that males are attracted to the pheromone itself, males swarm to it when it is placed into their tank (upper right). Credit: RIKEN

Explore further: Odor alternative: 'Olfactory necklace' detects scents in a way contrary to neurobiology dogma

More information: Yabuki Y, Koide T, Miyasaka N, Wakisaka N, Masuda M, Ohkura M, Nakai J, Tsuge K, Tsuchiya S, Sugimoto Y, Yoshihara Y (2016) Olfactory receptor for prostaglandin F2α mediates male fish courtship behavior. Nat Neurosci. DOI: 10.1038/nn.4314

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betterexists
not rated yet May 30, 2016
GENE EDITING: Why not add Flying Fish Feature to Other Fish ALSO?
betterexists
not rated yet May 30, 2016
Why NOT Add Flying Snake Feature to some other Snakes ALSO?
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