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Sound of silence: crickets rapidly evolved to hide from deadly flies

Crickets are nothing if not noisy, but populations on two Hawaiian islands have embraced silence by rapidly losing sound-producing…

Crickets on the Hawaiian islands of Oahu (pictured) and Kalau have evolved to keep quiet. Trey Ratcliff/Flickr, CC BY-NC-SA

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.

A flatwing cricket. Nathan Bailey, CC BY

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.

A comparison of flatwing and normal wings. Nathan Bailey/, CC BY-NC-SA

“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.”

The Italian wall lizard underwent rapid evolution on the island of Pod Mrčaru. Alexandre Roux/Flickr, CC BY-NC-SA

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.”

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5 Comments sorted by

  1. Paul Prociv

    ex medical academic; botanical engineer at University of Queensland

    Fascinating work! But what happens when all the normal, sound-producing males vanish, assuming them all to be susceptible to the parasitic larvae? How will females then be able to locate their partners? Will it mean extinction?

    1. Andrew Katsis

      Editor at The Conversation

      In reply to Paul Prociv

      Hi Paul. Your question actually came up in my interview with Nathan Bailey, and he said it was still a mystery.

      It's possible that flatwing males will adapt a new mating strategy, perhaps by spending more time wandering around in search of females.

      It's also possible that frequency-dependent (or balancing) selection will prevent singing males from disappearing entirely. That is, if there are very few singing crickets, then those individuals may gain enough matings to compensate for their higher mortality, pushing their numbers back up (at least temporarily).

      It's certainly an interesting research question!

    2. Mark Bean


      In reply to Paul Prociv

      Wonderful article! In terms of balancing selection, perhaps it will be that there becomes such a large group of non-singing males positioned close to a singing male that the singing male will be afforded some protection. Perhaps a fly may land on one of the non-singers by accident. So interesting!

  2. Jeremy Culberg

    Electrical Asset Manager at Power Generation

    I can recall a similar line on a species of fish - sexual selection preferred a highly decorative male, however highly decorated males were eaten (poor camouflage). So depending on where the species was inhabiting, predatory pressure or sexual selection pressure dominated. Remove the predator from the equation, and within a few generations the male population is swinging back to being highly decorative.
    In this case, it seems to have gone one step further, requiring a mutation, rather than simply a level of expression of existing genes.

  3. Rod Andrew

    Editor, teacher, engineer

    Thanks for a great article.
    Evolution by natural selection is such a wonderful, elegant explanation for why living things are the way they are.
    Wallace and Darwin would have been pleased to see this evidence.