RIKEN BRAIN SCIENCE INSTITUTE (RIKEN BSI)

Male fish need a sense of smell to get it on

Courtship behavior initiated by pheromone

May 31, 2016

Amanda Alvarez
Cross-posted from Neurographic

PGF2α activates two ventromedial glomeruli in the olfactory bulb of the zebrafish brain. Red: neural activation marker pERK. Green: olfactory axons expressing green fluorescent protein. Blue: the structure of the glomeruli visualized with anti-SV2 antibody. Image: Yoshihiro Yoshihara/RIKEN Brain Science Institute

Prostaglandin F2α can hardly be described as an alluring perfume. The odorless pheromone is released in the urine of ovulating female zebrafish, and males are drawn to it, well, like a fish to water. Prostaglandin F2α, or PGF2α, sets off a chain of courtship behaviors in the males, who chase, touch, and encircle the females before mutual spawning takes place. The instinctual romance aside, no one knew how PGF2α sets off these behaviors in the male brain. A new study published in Nature Neuroscience has revealed how this happens, and it turns out it all depends on the sense of smell.

Besides fish, prostaglandin F2α is also in lots of other animals, including mammals, where it acts hormonally to synchronize reproductive cycles. When it’s excreted by fish, it’s no longer a hormone within the body but a pheromone in a watery plume that leads males to reproductively ready females. Prostaglandins are lipid-type molecules that normally bind to their own prostaglandin receptors in body tissues. Not so with PGF2α and the male zebrafish.

Anosmic male zebrafish — that is, without a sense of smell — were indifferent to concentrated PGF2α in their tank, while their normal counterparts zoomed over as soon as it was poured in, as the video below demonstrates.

The olfactory epithelium, the location of primary “smelling” cells, is clearly necessary for PGF2α to have its effect on males. Within this tissue, only one kind of cell was activated by PGF2α: ciliated olfactory sensory neurons, long cells that send their outputs from the periphery of the body to the brain. With hairy surface protrusions, these neurons can pick up lots of odorants the nose might come into contact with.

But PGF2α is quite picky. It only binds to two kinds of olfactory receptors in these neurons and no others, the researchers found. These receptors have the very catchy names OR114–1 and 114–2, and PGF2α fits into them like a key into a lock. Though PGF2α is not a “smell” in the strict sense, it takes advantage of the 114 olfactory receptor pair’s affinity for carboxylic acids with a long hydrocarbon chain. In fact it appears that these olfactory receptors aren’t activated by any other prostaglandins or odorants.

Through these receptors, the PGF2α signal has a privileged path straight into the forebrain of the fish. From the olfactory sensory neurons, the researchers deduced, the neural signals pass into the olfactory bulb, a stopover point that creates a 2D map of smell inputs, after which they are transmitted to forebrain areas like the telencephalon and the preoptic nucleus. Those brain areas are directly responsible for setting off the fish’s courtship behavior.

“Smelling” PGF2α thus makes normal zebrafish males much more successful at spawning than fish missing the gene that makes the 114–1 olfactory receptor. These knockout fish spend much less time chasing and circling females and generally seem to have an impaired mating experience. How and why PGF2α came to “hijack” the smell pathway isn’t clear, but it obviously gave zebrafish a reproductive advantage. Because the 114 olfactory receptor genes are present in other fish with known attraction to PGF2α, and very similar receptors are found also in mice, the researchers think sex pheromones might make use of olfaction-based reproductive communication in many species.

 

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. Nature Neuroscience, DOI: 10.1038/nn.4314

 

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 RIKEN Press Release: Fish courtship pheromone uses the brain’s smell pathway