Elton Prize shortlisted Article

This blog post is provided by Colin Donihue and tells the #StoryBehindThePaper for the article “Rapid and Repeated Divergence of Animal Chemical Signals in an Island Introduction Experiment”. Colin has been shortlisted for the 2020 Elton Prize for this article.

Colin is a postdoctoral fellow at the Institute at Brown for Environment and Society. He is interested in understanding the causes and consequences of contemporary evolution. Much of his work focuses on determining the drivers of functional trait changes in lizards and the cascading effects of those trait changes on ecosystems.

Despite being the most ancient and pervasive means of animal communication, the evolution of chemical signals has never been experimentally investigated in the wild. Visual and auditory communication modalities have received more than a century of thorough study, but only recently have technical advances enabled scientists to begin deciphering the eco-evolutionary drivers that dictate the evolution of chemical signals.

In 2014, we captured 100 Podarcis erhardii lizards from a large, predator-rich island in the Greek Aegean Sea called Naxos, and evenly distributed them to five replicate predator-free islets.

In the years since, the population densities have increased by more than 500%, which has resulted in extreme intraspecific competition among the islet populations. This predator-free and intensely competitive ecological context is predicted to both decrease survival selection pressure and increase sexual selection pressure, resulting in a dramatic two-pronged push for rapid chemical signal evolution. We hypothesized that this novel selective context would drive the rapid divergence of chemical signal design in these experimental lizard populations.

With help from lizard chemical communication experts, Drs. Simon Baeckens and José Martín, we’ve taken a look at the chemical signals of the males on the experimental islands. Lo and behold, these chemical signals have shifted, and even more importantly, all five experimental populations have shifted in the same way. In other words, these lizards, translocated to experimental islands, have rapidly and repeatedly developed new “love languages” now that they don’t have to worry about predators and are intent on signaling their quality.

A bit more background: Here’s a picture of a beautiful Podarcis erhardii male. A few things to notice: see those large pores on the underside of the legs? Those are “femoral pores” – specialized glands that the lizard uses to exude a special waxy cocktail of chemicals.

These exudates are a great way for a lizard to communicate with other lizards. We’re still working on decoding the messages being sent, but we think several of them advertise “male quality” and perhaps immune function both to other males (stay away!) or females (come hither!).

There’s a problem though: lizards aren’t the only ones paying attention to these waxy scent-marks. Predators, particularly snakes, are excellent at sniffing them out when looking for a tasty snack. There’s a tradeoff then: on the one hand, a male lizard wants to let the world know how great he is (so he can attract mates), while at the same time keeping a low profile to avoid becoming lunch.

Naxos, the site of origin for the experimental populations, has lots of snakes that love to eat lizards. Accordingly, the lizards on Naxos have a relatively “buttoned-up” chemical signal design. When those populations were translocated to the islets though, after only a few generations those chemical signals had really cut loose! No longer having to worry about eavesdropping snakes, and intent on staking their claims, the experimental island populations have significantly more diverse cocktails of chemical signals and are spiking several “flags” of male quality (oleic acid, octadecanoic acid, and α-tocopherol).

One of the particularly important findings of this study is that all five of the experimental populations shifted in the same manner. This suggests to us that chemical signals can shift between populations in a deterministic, predictable way, according to changes in their ecology.

Thanks to incredible help in the field from Claire Santoro, Anne-Claire Fabre, Kinsey Brock, and Menelia Vasilopoulou-Kampitsi.