Every spring, the Interlake region of Manitoba, Canada, is the scene of a mating frenzy. Lured by female sex pheromones, ‘Tens of thousands of red-sided garter snakes bubble out of the ground’, says chemical ecologist Rocky Parker. ‘Male mate choice comes down to a matter of tongueflicks. But we don’t know what triggers pheromone production.’ Parker teamed up with Robert Mason of Oregon State University to decode the secrets of chemical signalling in red-sided garter snakes. Knowing that the hormone oestrogen activates sexual signal expression in birds, and given that snakes and birds are closely related, Parker and Mason wondered whether oestrogen triggers the production of a snake sexual signal: the garter snake sex pheromone (p. 723).
The pair reasoned that, if oestrogen was the key to their puzzle, exposing male snakes to oestrogen should make them smell like females and therefore irresistible to other males. To find out, they collected male red-sided garter snakes in Manitoba and brought them back to Oregon, where they surgically inserted oestrogen implants into the males’ body cavities. The next spring, they took the snakes back to Manitoba to test whether oestrogen had made them alluring. Placing the altered males in an outdoor arena, the pair was delighted to see that wild males courted the implanted males. But, seeing that the altered males tried to avoid their love-struck suitors, Parker and Mason devised an additional test. Starting a mating ball composed of a female surrounded by courting males, they placed an altered male near the mating ball and counted how many males lost interest in the female and began wooing the altered male instead. Again, wild males were keen to court implanted males; they believed that they were pursuing females. Parker and Mason also found that the effects were entirely reversible, as wild males were no longer fooled by altered males once their implants were removed. The hormone functions as an ‘on/off switch’ for female pheromone production.
So far, Parker and Mason’s suspicions had been confirmed. But when they laid scent trails in a Y-maze – by rubbing male and female snakes’ bellies along the maze’s arms – they were astonished to find that implanted males were more attractive than small females. ‘Longer females have more babies, so it’s best to court large females’, says Parker. ‘For some reason, oestrogen made males as alluring as large females.’
To find out why, the pair collected altered males’ skin lipids and examined their pheromone composition using mass spectrometry. Garter snake sex pheromones are made up of light and heavy methyl ketones, with large females producing mostly heavier ketones. When Parker and Mason plotted the pheromone profiles, they saw that altered males had a heavy pheromone composition, just like large females. ‘It turns out that oestrogen triggers the production of the heaviest, and therefore sexiest, methyl ketones’, Parker concludes.
So, in red-sided garter snakes, oestrogen triggers female pheromone production. This may offer an explanation for the puzzling existence of ‘she-males’ – wild males who naturally produce female sex pheromone but have negligible circulating oestrogen levels. ‘Exposure to oestrogen-mimicking pollutants could explain the presence of she-males’, says Parker; bad news for a species whose reproduction depends solely on chemical cues. ‘But the good news is that the changes are at least reversible’, he adds.