Male fruit flies dampen the libido of sexual rivals with smelly pheromone.
The struggle to reproduce and leave behind a genetic legacy has seen the evolution of a variety of weird and wonderful mating features. While male birds such as the peacock don fancy feathers and conduct elaborate courtship dances to outcompete rivals, male fruit flies employ a far less savoury tactic.
For the fruit fly Drosophila melanogaster, the tiny workhorse of the genetics lab, mating isn’t a guarantee of reproductive success. A male who has successfully mated with a female could still be outdone if a rival comes along and mates with his partner after he has wandered off in post-coital bliss. Sperm from both males will compete for the ultimate prize of fertilising the female’s egg.
One way that male fruit flies try to keep their sexual conquests to themselves is by offering their lover a smelly pheromone perfume as a parting gift to repel further would-be suitors.
How this intriguing system evolved is the subject of study published this week in the Proceedings of the National Academy of Sciences, USA. Sexual selection – where species evolve features that enhance their chances of reproducing, but not necessarily their survival – was first described by Darwin in his 1859 book, Origin of the Species. Darwin suggested that the peacock’s feathers, the lion’s mane, and the deer’s antlers were all examples of female preferences driving the evolution of male appearance. In some cases, the appearance is used as a proxy for females to determine the genetic quality of their potential partners.
It was once thought that the female preference for a particular trait — ever longer tail feathers or ever more elaborate mating dances — and the male traits themselves, sprung forth more or less simultaneously and co-evolved over time. However, since the early 1990s, researchers have identified cases where females have a natural proclivity towards a particular trait, even when the males of their species lack that characteristic. For example, female platyfish will shun male platyfish with plain tails in favour of males with artificially attached plastic swordtails, even though these males don’t occur naturally. The females simply have a sensory bias for the more fancy tail.
In such cases, the evolutionary stage is set for an evolutionary process called sensory exploitation. This seems to be what has happened with the Drosophila pheromones, although the sensory bias that is being exploited is that of the male, not the female.
To tease out the evolutionary origins of the smelly sex pheromone, known as CH503, researchers lead by Joanne Yew at the National University of Singapore compared the pheromone in eight species of Drosophila fruit fly. Five species produced identical versions of CH503, whereas three species did not produce the anti-aphrodisiac. The researchers tested how males responded to the pheromone by presenting virgin males with a virgin female perfumed with the stinky substance. Males from the three species unable to produce CH503 were repelled by the smell just as males from the five species who do produce the chemical. This indicates that the aversion to the scent predates the evolution of the pheromone in five of the species.
The researchers then tested how strong this aversion was between the different species. Species that produce the pheromone were less repelled by the smell than non-producer species, suggesting that over time, species that employ the anti-aphrodisiac in their mating strategy become habituated to the chemical over evolutionary time. This is the first time that sensory exploitation has been described as a mechanism for the evolution of pheromones used in male-male competition.
Ng SH, Shankar S, Shikichi Y, Akasaka K, Mori K & Yew JY. 2014. Pheromone evolution and sexual behavior in Drosophila are shaped by male sensory exploitation of other males. Proceedings of the National Academy of Sciences, USA. Published ahead of print: doi:10.1073/pnas.1313615111