In the Evolution of a Signal, What Comes First: The Signal or the Response?

Finding and attracting a mate is tricky business for most species. It can be quite helpful then to have a species-specific signal that is sent and received by members of your own species, but not perceived as well by predators. Chemical signals (those we perceive through smell and taste) are among the most diverse and specific signals produced in the animal kingdom, so they make good candidates for these species-specific mating signals. Sex pheromones are chemical compounds released by an animal that attract animals of the same species but opposite sex. They are often so specific that other species can't smell them at all, which makes them useful as a secret communication line for just that species. But this specificity raises an intriguing question: When a new species evolves and uses a new pheromone signaling system, what comes first: the ability to make the pheromone or the ability to perceive it?

Here is the conundrum: Among species that use pheromonal signaling systems to attract mates, individuals that are detecting and responding to the scent (the receivers) are using the specificity of the signal as a measure of whether the individuals emitting the scent (the senders) are in fact the right species. Any individuals that make a new and different scent would then be perceived by the receivers as being the wrong species and they won't attract any mates. If you don't attract mates, you can't pass on your new genes for your new scent. This produces a strong pressure to make a scent that is as similar as the scent produced by everyone else as possible (this is called stabilizing selection). With this intense pressure to be like everyone else, how did the incredible diversity of species-specific pheromones come to be?

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A German research group recently shed light on this question with a study of jewel wasps. There are four species of jewel wasps, and the males of all four species produce two chemicals (called RS and MQ) for pheromonal communication. However, males of one of these species, called Nasonia vitripennis, produces a third unique chemical compound called RR. The combination of RS and MQ produces a scent that attracts females of all four species, but the addition of RR produces a scent that is irresistible only to the Nasonia vitripennis females (females of the other species didn't seem to care if RR was added to the scent). Interestingly, none of the females respond at all to the scent of RR alone.

The researchers then performed chemical and genetic analyses of the RS, MQ and RR scent components. It turns out, the chemical structure of RR is almost identical to RS, with just one minor difference. This one difference is due to the presence of enzymes that are created in response to just three genes.

Based on this evidence, the researchers concluded that the male evolutionary ancestors of these jewel wasps produced pheromones consisting of RS and MQ compounds and the females responded to that scent. Somewhere along the divergence of the Nasonia vitripennis, a few males developed a genetic mutation that resulted in the conversion of some of the RS component into a new RR component. But at this point, the females either didn't smell this new component or didn't care. As the RR genes started spreading through the population by random chance, female Nasonia vitripennis started to detect and prefer pheromones that contained the RR component. And voilà! A new pheromonal system is born!

This doesn't necessarily mean that this is how all new communication systems come to be. There is evidence that in some cases the genes for the production of the signal and the perception of the signal are close to one another on the DNA and can thus be passed along together. In other cases, a few genes may influence both the production and the perception of the signal. But in this case, it looks like the signal evolved before the response to it. The evolution of communication systems is inherently difficult to study, but this research points our noses in the right direction.

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Further reading:
Lassance, J. and Löfstedt, C. Chemical communication: A jewel sheds light on signal evolution, Current Biology, 23(9), R346-R348 (2013). DOI: 10.1016/j.cub.2013.03.055.

Niehuis, O., Buellesbach, J., Gibson, J.D., Pothmann, D., Hanner, C., Mutti, N.S., Judson, A.K., Gadau, J., Ruther, J. and Schmitt, T. Behavioural and genetic analyses of Nasonia shed light on the evolution of sex pheromones, Nature, 494, 345-348 (2013). DOI:10.1038/nature11838.

Image Credits:
Nasoniavit.jpg is by M.E. Clark at Wikimedia Commons.