Butterflies, or butterlies?

Most of us rely on our sense of sight to identify the people around us. So, if your roommate were to try and fool you into thinking that she was your boyfriend, she’d have to go to fairly epic, award-winning-special-effects-makeup-level lengths to fool you. In nature, however, organisms can often fool members of entirely different species into thinking they are related using methods that are analogous to simply putting on your boyfriend’s cologne.

The vast majority of organisms use chemical signals to identify – and trick– each other. Chemical mimicry is the process of synthesizing the pheromones of another species so that members of that species will think that you are one of them.  Indeed, while we have little experience with non-humans dressing up and fooling us into thinking they are our neighbor or family member, chemical mimicry is a very common phenomenon in nature. And, due to our long tradition of using mistaken identities as a comedic device, and our general impulse to view the actions of organisms as willful choices instead of non-emotional instincts produced by millennia of evolution, the stories of chemical mimicry are often hilarious.

One story about chemical mimicry involves an endangered species of butterfly, the rare and beautiful Phengaris rebeli (formerly Maculinea rebeli, which someone thought sounded too much like “masculine rebel” and needed changing). While sure to make you laugh, P. rebeli’s chemical mimicry story also helps us to understand why this butterfly is so threatened and informs how we think about conserving its habitat.

P. rebeli, native to the Alps and other areas in southern Europe, is a social parasite of red ants named Myrmica schencki.  The story of its deception of these unwitting ants begins with the flowering plant Gentiana cruciata. P. rebelifemales lay their eggs specifically on the leaves of this plant. When the larvae hatch, they get their first meal from the plant. After a period of feeding on these leaves, the larvae fall to the ground (cue strangely loud  plopping noise of the wiggly larvae falling a few inches onto the soil below). This happens during the early evening, which is exactly the time of night that Myrmica red worker ants are out-and-about looking for food and, as it happens, any misplaced ant larvae.

When the ants  encounter the P. rebeli larvae, from here-on called caterpillars, they ask “who is this?” by swabbing the caterpillars’ grubby bodies with their antennae, which is the way the ants can get a whiff of the chemicals there.Researchers have studied the process of Myrmica ants interacting with the caterpillars to understand this key interaction more deeply. They analyzed the surface chemicals the larvae produce, and whether these chemicals closely mimic the preferred host–Myrmica schencki– or mimic pheromones found in most Myrmica species. They discovered that the chemicals secreted by the caterpillars are highly similar to those present on Myrmica schencki ant larvae and workers. Rather than synthesizing one or a just a handful of important pheromone compounds, the caterpillars’ chemicals are instead a complex mixture, a subtle perfume built from many different volatile and non-volatile hydrocarbons, including limonene, which is a terpene that smells like citrus fruits. Upon encountering this lovely perfume of ant larvae, the Myrmica ants are fairlyconvinced: it takes the ants much longer to actually pick up the caterpillars compared to larvae of their own species, and many ants even place their caterpillars on the rubbish heap, before changing their minds and removing the caterpillars from the pile of ant trash. Eventually, most of the caterpillars end up safe and sound amongst the ant larvae, or “brood.”

Once amongst the ant brood, things get even stranger. Having secreted their own fairly convincing ant-larvae perfume, the caterpillars become even more convincingly “ant-like” through the process of chemical camouflage. Through physical  contact with ants and their built environment, the caterpillars pick up even more ant scents. The researchers used a scoring system, named “Nei’s distance,”  to measure the degree of similarity between the chemical profiles of extracts of caterpillars and ants, where 1 is identical and 0 is no chemicals in common. The score for the caterpillars freshly plopped onto the ground from their eggs compared to the adult ant workers was 0.3. After adoption by the ants, the score jumps to 0.85. The treatment of the caterpillars by the ants reflects this change: once fully ingrained into ant society and camouflaged by ant compounds, the caterpillars are treated so well that in times of stress, the ants will actually feed the caterpillars the chopped up bodies of ant larvae and eggs. If you think about it, this is pretty messed up.  

Living amongst the ants over the course of one to two years, the caterpillars grow from 1 mg to about 100 mg in size, which is about one-hundred times larger than an ant, making us wonder how the gig isn’t up for the caterpillars once they’ve grown so remarkably giant compared to their hosts. After their long co-habitation with the ants, the caterpillars emerge as butterflies, their chemical charade a success. The strategy of P. rebeli to parasitize ants in such a lengthy and integrated manner is a strategy to gain resources, including food and safety from predators, and deal with ants as competitors for those resources at the same time. Other species of butterflies have altogether different ideas for how to deal with the ants, including agitating ants or simply throwing in the towel and feeding and appeasing them with gifts of sugar and amino acids.

Chemical mimicry is found throughout nature, and can involve insect-insect interactions (such as that between P. rebeli and M. schencki) as well as plant-insect interactions. For example, orchids produce the female sex hormones of pollinators, and these chemicals are carried by the wind to seduce male pollinators to the flower. Finally, our review of the chemical mimicry of the large blue butterflies P. rebeli points to the specificity of its lifestyle: the eggs are deposited on specific flowers, and the larvae fall to the ground at the peak foraging time of red ants, one species of which will be fooled into taking the caterpillars into their colony. This high degree of specificity during multiple stages of its lifetime points to the fragility of its habitat, and suggests that protecting the butterfly means protecting Gentiana cruciata and M. schencki, too.

- CAB