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Cross-dressing in the Snake World

Some male garter snakes in Manitoba's Interlake region imitate females in the spring. The reason for this strange behaviour has been a mystery since its discovery 15 years ago. But now Rick Shine, an evolutionary biologist from the University of Sydney, and his colleagues from Oregon State University, Corvallis, think they have worked out the evolutionary strategy behind the behaviour.

The team observed red-sided garter snakes which had recently emerged from hibernation in Manitoba's famous snake dens about 100 kilometres north of Winnipeg. The males of this snake species routinely form 'mating balls', where several suitors coil themselves around one female. But over a quarter of the mating balls were actually centred on a 'she-male.'

When the researchers studied these impostors, they found that they were fatter than their male counterparts and crawled more slowly. Their courtship behaviour was suppressed and they were less likely to couple with females. "Males that produced female skin lipids became female in behaviour as well as attractiveness," says Shine.

To check that the snakes were not getting their hormonal disguise from contact with females, the researchers rubbed males against females. Males treated in this way failed to excite other males. However, when they removed the snakes' male pheromones by washing them with a solvent and adding female lipids, the snakes became attractive to males. These 'artificial' she-males also lost interest in sex.

But to the researchers' surprise, when these she-males were captured and tested a day later, they had become the most vigorous suitors of all. At the same time their attractiveness to males had decreased. The situation seemed inexplicable, until Shine realized that the hormonal 'cross-dressing' was a temporary phase that all males went through upon awakening from hibernation.

Shine and his colleagues suggest that she-maleness suppresses the snakes' urge to court females while they are still weak from hibernation, preventing them from wasting valuable energy on courting when they are likely to fail. Masquerading as females also confuses other males, distracting them from true females.

"We call this kind of behaviour 'spite'," says Morris Gosling, an evolutionary biologist at the University of Newcastle. "The she-males diminish the costs of courtship at the same time as duping other males."