How Hawaiian field crickets evolved silence and mature faster

Hawaiian field crickets faced an apparently impossible decision: continue singing to attract mates and risk death at the hands of a parasitic fly, or become silent and find another means of reproducing.

Evolution provided a solution. Within a few decades, silent males spread quickly across the islands, having lost their courtship song through several different mutations affecting their wings.

A new study has now uncovered another advantage that helped make the transformation possible.

Silent males become adults around a week before their singing rivals, giving them more time to find mates despite losing the song that once drew females to them.

When Hawaiian field crickets’ singing turns deadly

Male crickets produce their song by scraping one wing against the other. In most parts of the world, females use that rasping sound to find them in the dark. On the Hawaiian Islands, however, the same song comes at a deadly price.

A parasitic fly hunts by sound, following the chirp to its source before depositing newly hatched larvae on the male. The larvae burrow into his body and consume him over the days that follow.

This pressure rapidly changed the crickets. Silent males, known as the flatwing form, were first recorded on Kauai in 2003.

Making themselves invisible

As one early study documented, researchers found that over 90 per cent of males on the island had lost their ability to sing in roughly 20 generations.

A flatwing male is undetectable to the fly by sound, but he is also silent to the females he needs to reach.

Jae Walker, a PhD student at the University of St Andrews in the UK who led the new research into these field crickets (Teleogryllus oceanicus), described their escape in simple terms.

“It’s like these crickets have the acoustic equivalent of invisibility powers!” said Walker.

Since then, silence has spread from Kauai to crickets on the other south-eastern Hawaiian Islands.

A faster path to adulthood

The loss of song appeared to be a serious disadvantage, and for years the obvious question was how silent males could reproduce at all.

Walker’s team found part of the answer in the crickets’ development, rather than in their wings.

The researchers reared the insects and monitored their growth. Ordinary singing males, they found, took about a week longer to become adults than silent males and also took longer than females of either type.

Reaching maturity sooner gives silent males a longer period of adult life. The extra nights offer more opportunities to reach a female, either by walking towards males that are still singing or by waiting nearby.

That head start appears to compensate for some of the disadvantage of silence.

Walker sees it as a trade-off. “They aren’t able to attract female mates with their song, but they develop faster so have more time to seek out female mates using other methods,” he said.

The genetics behind silence

Researchers have yet to establish why the two types develop at different rates.

Using microscopy and sequencing genes active in developing wing tissue, the team identified a master gene called doublesex as a likely contributor. The gene helps direct the formation of male and female bodies.

Previous research had already connected the flatwing trait to a section of the genome containing that same gene.

The new study suggests that doublesex acts within a broader network of genes responsible for forming wing veins, and that small changes to this network can each result in a silent male.

Silence evolves again and again

Flatwing is no longer the only form in which these crickets have become quiet. Walker’s team has been cataloguing several distinct silent forms, each caused by its own mutation and each preventing the male from calling in a different way.

In one form, called curlywing, the edges of the wings curl upwards. In another, smallwing, the wings are reduced to around half their usual size.

The latest form, known as defiled, damages the very vein a male would rub to produce sound. Different genetic starting points continue to lead to the same result.

That pattern reflects an earlier paper showing that flatwing itself evolved more than once on separate islands, through different mutations that silenced the wings in similar ways.

Complete silence is not the only means of escape. Some male Hawaiian crickets have adopted a quieter, purring song that the fly largely ignores but females can still hear.

“This parallel evolution toward silenced song reveals similar but independent solutions to the same problem, leading us to ask how this variety of changes occurred,” said Walker. Every newly discovered form makes that question broader.

Nature changing before our eyes

The crickets now reveal something that was not previously apparent: becoming silent brings a hidden benefit. Silent males do not merely survive the fly at the expense of their love life.

They also reach adulthood faster, regaining some of the reproductive opportunities lost when they stop singing.

The broader opportunity is to observe adaptation taking place on a human timescale, something that is usually impossible.

Most evolutionary change is pieced together from fossils or ancient DNA. In this case, scientists watched a signal collapse and begin to rebuild in barely two decades, while the genes and wing structures were still visibly changing.

For Walker’s team, each new silent form prompts the same question.

“This variety of song-loss morphs is found across the Hawaiian archipelago, making us wonder about the upper limit on how many independent solutions there can be to the evolutionary ‘problem’ of the flies,” said Walker.

The research was presented at the Society for Experimental Biology Annual Conference.