Garter Snake Vibes: A Tale of Pheromones and Mating

GarterSnakeCoverEvery spring, red-sided garter snakes in Manitoba, Canada emerge from hibernation in an intense quest to mate. Female snakes emerge with high levels of circulating estrogen, resulting in pheromones strong enough to set male snakes in a frenzy. Up to 100 male snakes frantically and simultaneously court a single female in a tangled, writhing mating ball. In the size of the average living room, there could easily be 100,000 snakes breeding at one time.

Bob Mason, Professor of Integrative Biology at Oregon State University and renowned garter snake researcher, explains his fascination with the system as a graduate student.

“What struck me when I was a young pup – everything that we were working on regarding reproduction had to do with pheromones. If the female didn’t produce them or the male didn’t detect them, all reproduction came to a halt,” Mason commented.

A pheromone is a chemical produced by one individual that effects a change in the physiology or behavior of other members of the same species. But why use snakes to study pheromones?

Mice, the popular girl in the room when it comes to biological research models, also use pheromones to help facilitate mating. Scientists can manipulate mice pheromone systems using specific gene knockout breeds, resulting in a total inability to produce or detect pheromones. However, even without the use of pheromone signaling, mice are still able to mate. Biologically clever, mice have evolved all kinds of redundant systems to facilitate mating even when one cue goes missing – great for them, bad for researchers trying to understand mating cues. Snakes, on the other hand, are easy to manipulate and yield much more pronounced effects.

“Evolutionarily, snakes haven’t evolved redundant systems. So that makes it a really powerful tool to study reproductive biology,” said Mason.

Mason’s recent research is examining how pheromone signals are received and transduced into behavioral effects.

Garter snakes are covered with a thin layer of fatty lipids that prevent subcutaneous water loss and keep them from drying out. Pheromones are part of those skin lipids on the surface of female snakes, which send signals of their reproductive status to the males. Pheromones are detected by the males via tongue flicking, and then activate a cascade of events in the brain to affect mating behavior.

Now, we all know oil and water don’t mix. Mason and his colleague, Mimi Halpern, were interested in understanding how lipid-based pheromones could travel through a water-based organism to elicit their effects. They looked to the harderian gland, the largest cephalic gland in vertebrates, yet not well understood. They discovered that, in snakes, this gland is the source of fluid containing binding proteins that pick up pheromone molecules on the tongue and carry them into the volmeronasal organ for sensing. If the harderian glands were surgically removed from snakes, mating was abolished.

An observant undergraduate student in Mason’s lab noticed that snakes with the harderian glands removed weren’t feeding normally – usually devouring worms immediately, these snakes would only eat worms that were dangled in front of them. To their surprise, the removal of the harderian glands had also rendered the snakes incapable of chemically detecting food.

Mason emphasized, “Here we have one system – the harderian gland and its binding proteins – that serves as the linchpin for the two most important life history events for this animal: breeding and feeding.”

What’s more is that snakes with harderian glands removed eventually regenerated these structures and regained the ability to detect chemical cues. Mason added, “Very few organs regenerate. These glands are so important that they regenerated – and quickly!”

Mason’s research group is starting to utilize transcriptomics and the fully sequenced garter snake genome to answer further questions about this system. Now, Mason only wishes he could discover the fountain of youth – “Science being done now is spectacular. Huge scientific questions are going to be answered in this decade. It’s a fantastic time to be involved.”

Bob Mason received the Oregon State University F.A. Gilfillan Memorial Award for Distinguished Scholarship in Science in October, and will be giving a featured lecture at OSU in the spring – stay tuned!

By Keely Corder