New research finds that the "silent" mutant male crickets of Hawaii, first observed over 20 years ago, have now become well-established across the Hawaiian islands, and that the reproductive challenges caused by a lack of courtship song may be offset by a much earlier maturation into adulthood, providing a wider window for breeding opportunities. This research also reveals the existence of multiple different sound-reducing morphs, all with their own unique mutations that disrupt the cricket's ability to create songs.
Crickets are synonymous with the loud, chirping courtship songs produced by males attempting to attract females, but a population of Hawaiian field crickets (Teleogryllus oceanicus) have relatively recently produced a mutated "flatwing" morph that are missing the wing structures that allow for sound production.
The silent cricket phenomenon was first observed on the island of Kauaʻi in 2003 and has since proliferated across the other southeastern Hawaiian islands due to widespread pressure from the parasitoid fly, Ormia ochracea, who uses the wild-type cricket's courtship songs to locate and parasitise them.
"Multiple other sound-reducing morphs have also recently evolved, suggesting rapidly evolving underlying gene regulatory networks," says Jae Walker, a PhD student from the University of St Andrews, UK. "It's like these crickets have the acoustic equivalent of invisibility powers!"
This project, presented at the Society for Experimental Biology conference in Florence, Italy, aimed to understand the genetic influences behind these rapid morphological changes and learn more about the variety of different sound-reducing morphs that they have recently discovered.
"We explored the hypothesis that core developmental genes like doublesex interact with a broader network of venation specification genes as T. oceanicus' wings develop, such that numerous slight adjustments to this network result in convergent song-loss venation," says Mx Walker.
Mx Walker and their team used microscopy and wing-tissue-specific RNA sequencing to analyse the morphology and wing-specific genetic pathways that contribute to this range of quiet morphs.
The major finding that the Mx Walker and their team revealed is that it took the wild-type males around a week longer than the non-singing flatwing males and females of either morph to become an adult.
"This was surprising as it suggests a developmental trade-off allows the non-singing males to overcome the advantage lost from their inability to call mates to them," says Mx Walker. "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."
The genetic analysis has also started to reveal some of the key genetic pathways involved in these stark developmental changes. "Transcriptional profiling indicates the sex-differentiation pathway gene doublesex is involved," says Mx Walker. "This supports our hypothesis that there are changes in the well conserved sex-determination genetic pathway, which we will explore further in the future."
In addition to the flatwing morph, Mx Walker and their team have discovered that there is not just one sound-reducing male morph and they are currently exploring all of the other morph's anatomical and genetic differences. These other morphs vary in the way that they modify the cricket's wings, but they all silence or reduce the male's songs and provide protection from the flies.
"We've given them names based on how they alter the wings - such as 'curlywing', which curls up the wing edges, and 'Smallwing', as shrinks the wings to about half their normal size," says Mx Walker. "This parallel evolution towards silenced song reveals similar but independent solutions to the same problem, leading us to ask how this variety of changes occurred."
The most recent morph the team have discovered is named 'defiled', because it disrupts a vital wing vein called the stridulatory file and results in song loss.
"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," says Mx Walker.
