Crickets are nothing if not noisy, but populations on two Hawaiian islands have embraced silence by rapidly losing sound-producing wing structures to avoid infestation by deadly fly larvae.
In Current Biology today, researchers show that a silent form of the oceanic field cricket (Teleogryllus oceanicus) evolved independently – and quickly, in evolutionarily terms – on two neighbouring Hawaiian islands.
“What is quite unique here is the nearly simultaneous appearance of this trait on both islands,” Nathan Bailey, a biology researcher at St Andrews University in the UK and one of the study’s authors, said. “The fact that this seems to have happened so recently and so rapidly is very intriguing.”
The benefits of staying silent
To attract females to mate with them, male crickets scrape together two wing structures known as the plectrum and file to produce their distinctive song.
But singing also attracts unwanted visitors. On several Hawaiian islands where the cricket is an introduced species, the parasitoid fly Ormia ochracea will acoustically locate male crickets and deposit larvae on them.
These larvae burrow into host crickets and emerge around a week later, killing the cricket.
This behaviour produces a major selection pressure, and in the early 2000s crickets on the island of Kauai evolved an unusual avoidance strategy. A form of male appeared that, due to a genetic mutation, had lost the wing structures necessary for producing song.
These non-singing males – known as flatwings – are harder to locate in the dark, offering protection from the parasitoid flies.
“Far fewer flatwings get infested compared with normal males,” Dr Bailey said. “That’s the advantage of being silent.”
The downside to this adaptation is that male crickets can no longer attract mates, so instead they position themselves close to singing males and intercept females as they approach.
Flatwings are now the dominant cricket form on Kauai, making up 96% of the island’s population.
Two years after their appearance on Kauai, flatwings were observed on the nearby island of Oahu. Many researchers assumed the crickets had simply dispersed onto the neighbouring island.
Different paths, same destination
To put this theory to the test, the researchers genetically analysed normal and flatwing crickets from each island population.
“The basic idea is we chopped the cricket genome into tiny pieces, sequenced a subset of those pieces, and detected genetic markers that were associated with the flatwing phenotype,” Dr Bailey said.
These genetic markers, known as single-nucleotide polymorphisms (SNPs), indicate which genetic mutations are linked to the flatwing form.
“These SNPs are basically like fingerprints,” Therésa Jones from the University of Melbourne explained. “If they appeared at roughly the same places on the genome in the two different populations then this flatwing trait probably arose on one island, and then spread to another.
"But they’re not the same at all – they’re very different.”
This suggests that flatwings are an example of convergent evolution. Faced with similar selection pressures, crickets on each island underwent different mutations to reach the same outcome: silence.
Evolution in the blink of an eye (comparatively)
Although our understanding of rapid evolution is growing, most known examples have occurred in laboratory settings. Observing it in the field is far less common.
“A close example is perhaps that of the Italian wall lizard, where we saw massive morphological changes over a period of 36 years,” Dr Jones said. “As with the crickets, this took place in an island population, and I think that’s one of the key factors in allowing for this very rapid evolutionary change.”
Robin Tinghitella from University of Denver, who has studied the flatwings, believes that a genetic bottleneck may have primed both island populations to evolve the trait so rapidly.
“In other locations where the crickets live, like Australia, females are quite choosy and flatwing males would be selected against,” she said.
“But imagine you’re a female cricket and you land on an island with very few mates to choose from. If you’re extremely choosy you may never find an acceptable mate, which means the end of your genetic line.
"In other words, small founding populations may favour females who are lax in their mating decisions.”
This means that less choosy females on small islands may be more tolerant of flatwing males, allowing them to mate enough times that the survival benefits of not singing outweigh the sexual costs.
“There is absolutely no doubt that singing is a beneficial trait,” Dr Jones said, “but the selective pressure from parasitism is so strong that it is pushing the species away from acoustic communication, and very rapidly.
"That is what’s so cool about this study. It’s rare to be able to watch evolution unfold in your lifetime – rare and beautiful.”