The Very Quiet Crickets of Hawaii : Rapid Convergent Evolution

The Very Quiet Crickets of Hawaii : Rapid Convergent Evolution

Reading Time: 8 minutes

Crickets in the Hawaiian island of Kauai have, over the past twenty years, fallen silent 1. A mutation has changed the structure of the male crickets’ wings, so that they are now born without the ability to chirp. Since cricket mating happens at night in the dark, and the chirp is a necessary way for the male to advertise itself, one would, justifiably, fear for the survival of the Hawaiian crickets. Surprisingly, that hasn’t happened, and the crickets of Kauai flourish. Nerdruid tries to find out how.

One day a tiny cricket is born and meets a big cricket who chirps his welcome. The tiny cricket tries to respond, but there is no sound. The quiet cricket then makes his way into the world, meeting one insect after another, each of whom greets the little cricket with a cheery hello–the hum of a bee, the whirr of a dragonfly, the whisper of a praying mantis. The cricket rubs his wings together each time, but nothing happens, not a sound. Until the day he meets another cricket, a female, and something different happens . . .

This is the summary of The Very Quiet Cricket, a children’s book by Eric Carle, master picture-book maker. The story catches our attention simply because, as we all know, there is no such thing as a quiet cricket. The whole concept is absurd! Crickets are one of the noisiest insects on the planet, and, while a few crickets in unison makes for a wonderful balcony evening, too many ensures a sleepless night. Which is why a silent cricket sounds so…abnormal. While they may certainly be used in fiction, the chances of encountering peace and quiet (okay, maybe just quiet, since cricket chirps can be peaceful at times) in the vicinity of  actual crickets seems quite far out.

Book cover of “The Very Quiet Cricket” by Eric Carle.

Or does it?

Ormia ochracea is a parasitic fly 2 native to mainland North America. The fly uses its acute directional hearing to locate male crickets by following their chirping 3. Once located, the fly deposits a clutch of maggots on the back of the cricket. The maggots would burrow inside the cricket and emerge, much fattened, about a week later, killing the cricket in the process. This had almost wiped out the cricket population in the island of Kauai by the turn of the century. What saved them was silence.

Marlene Zuk has been studying the Kauai crickets (Teleogryllus oceanicus) since the nineties. She, along with her colleagues, started noticing a fall in the cricket population and traced the reason to the Ormia flies. By the turn of the century, Zuk et al report 4, there was almost total silence in Kauai, a stark contrast to the constantly buzzing nights from a decade back. She naturally assumed that the Ormia flies had finally managed to kill off the crickets, and that was that. However, what she hadn’t expected was a thriving cricket population, all silent.

This was extremely odd behaviour for crickets, who tend not to get up one day and decide not to chirp any more. So she dissected the crickets and found that the reason why the crickets had, all of a sudden, gone mute wasn’t because they did not want to chirp, but because they couldn’t.

The wing on the right makes the file section of the tegminal while the left wing makes the scraper section. When the wings move back and forth (bottom of the figure) the file strikes the scraper which generates the call that we hear from the cricket. (caption reproduced from source)

Stridulation is the act of producing sounds by rubbing body parts together. This is most notably seen in male crickets 5, the back of whose wings have two features — a vein with several evenly spaced teeth which acts as the file and a raised ridge which acts as the scraper 6. When these two rub together, a thrrrp sound is produced. This is one pulse. The crickets vibrate their wings rapidly enough so that a number of such pulses are generated in a short interval of time, giving rise to the distinctive cricket-y chirp. Zuk found that the crickets of Kauai had lost these features, and the resultant flatwing 7 crickets could no longer chirp even if they wanted to. By 2003, almost the entire Kauai male cricket populations consisted of flatwing mutes, and there were no more chirpers. However, the silence meant that the Ormia flies could no longer locate the males, and crickets in Kauai flourished. And all this happened because of genetic mutations that gave rise to flatwing crickets and, in a span of just 20 generations 8 they had taken over 7.

 

The teeth on both the file and the scraper generate the sound that is heard when they are scraped over each other. We can think of this as a type of harp, as fingers run over the strings of the harp sound is generated through the vibration. In the same way as the teeth of the file run across the teeth of the scraper sound is generated through their vibrations. (caption reproduced from source)

Two questions arise.

  1. Why, and how, would the females mate with silent males? The chirping is a necessary mating ritual, and one would expect that the mute flatwings would be at an evolutionary disadvantage.
  2. How is the mutation passing on to the offspring of the silent ones in such stable fashion? Usually, such a phenotypic anomaly requires mutations in several genes, and these are often broken up during meiosis — that is, not all the mutations are passed on to the offspring.

In answer to the why of (1), Marlene Zuk et al found 4 that the Kauai females were, to put it plainly, less stringent about marriage…I mean, mating requirements. Essentially, the females did not overmuch care if the males were excellent chirpers, and were equally fine with the “strong, silent types” 9. This of course might imply that this particular phenomenon might not be observable in parts of the world where the females are more…finicky. However, this gives rise to yet another question : why are female Kauai crickets less choosy? The answer can be gleaned using the first principles of evolution : a large, diverse population (crickets, rabbits, humans) encourage greater competition in mating, and consequently females (maybe not humans) have greater latitude in being picky. It’s a bit like shopping in a mall, to use a very politically incorrect analogy. Conversely, in a small largely (genetically) homogeneous population, beggars cannot be choosers, and thus the females must relax their stipulations if the species has to survive. Such is the hypothesis, that the cricket population is Kauai is low and mostly genetically homogeneous. Is it supported by data? Indeed it is 10 11 . Turns out that the Hawaiian crickets are descendants of Australian crickets who, by hitching rides with master mariners from the Polynesian islands, populated several Pacific islands and archipelagos before finally landing on Hawaii. While Australian crickets show sufficient genetic heterogeneity, the spreading around meant that each time a portion of the hitchhiking population were dropped off, they took to shore some of the genetic variation of the parent (Australian) population. If genetic variation is currency, then the Hawaiian crickets were left rather destitute.

In answer to the how of (2), Susan Balenger and Marlene Zuk hypothesized 12 that, without sound to guide females to them, male Kauai flatwings have no option other than to simply leg it. This strategy is both energy inefficient and dangerous, for, in their amorous wanderings, males crickets could conceivably enter within striking distance of the tongue of a cane toad. Granted, being a cane toad’s quick dinner is probably a better fate than being eaten from the inside out by fly maggots.

Undersides of the right forewings from normal male, mutant male, and female crickets. The corresponding SEM (scanning electron microscope) micrographs show the part of the wings where noise is generated. Normal male wings have a toothy vein that is scraped to make sound. In mutant males, that vein is smaller and repositioned. Females don’t have this toothed vein at all. (caption reproduced from source almost unchanged)

In answer to (2), experiments confirmed that the silent wing arose due to a single mutation in the X chromosome of the males 7, and was thus less messy to pass on to the offspring. This explains how the mutation rose to such a high frequency in a mere blink of the evolutionary eye.

Had the story ended there, it would still have been quite an extraordinary example of evolution where an organism almost completely reverses its primary aspect of survival and still flourishes. One would expect, given advances in modern transportation 13, the Kauai flatwing crickets might conceivably have hitched rides on boats, much like what their ancient ancestors once did, and spread to neighbouring islands. Given how closely spaced islands in the Hawaiian archipelago are, they could have just flown there or, since crickets aren’t fantastic fliers, been carried along by strong winds 14. In fact, that is exactly what happened when, in 2005, four flatwings were found in the neighbouring island of Oahu. By a process similar to Kauai, these then proceeded to dominate the besieged Oahu male chirpers, and by 2007 half of the Oahu crickets were flatwings 14. From an evolutionary standpoint, this is unsurprising, and one would suspect, quite confidently, that the Oahu crickets attained their mutation through gene flow 15. Which would mean that a close inspection of the wings of the Oahu flatwings would reveal the same structure as those of the Kauai flatwings. In 2014, Sonia Pascoal et al did just that 16.

Normal wings versus flatwings in Kauai and Oahu. Credit: Nathan Bailey. (caption reproduced from source almost unchanged)

And found that the wings of the Oahu flatwings were quite a bit different from those of their supposed ancestors.

The differences existed both in the phenotypic, or body-structural, and genotypic, or gene-makeup regimes of the crickets. The Oahu flatwings have greater remnants of the toothy vein than their Kauai counterparts, and are thus phenotypically closer to the normal chirpers. Genetically, the mutations in the Oahu and Kauai flatwings arose in different versions of the X chromosome, quite possibly in different parts of the same gene or even in different genes 9. Out of 7000 genetic markers, only 22 were found to be common between these two variants 14. This is a clear example of convergent evolution 17. Paired with the fact that this evolution was also extremely rapid, one might safely add it to yet another situation where Darwin’s dangerous idea 18 keeps throwing up unexpected surprises.

The map shows Hawaiian islands on which flatwing males are found and the year they were first documented. Although several flatwing males have recently been found on the “Big Island,” Hawaii, the lab population derived from that island was established prior to 2012 and did not contain flatwing males at the time. (caption reproduced from source)

References

1.
Interview with Marlene Zuk. Strange Cricket Silence (2018). Available at: http://askabiologist.asu.edu/explore/strange-cricket-silence. (Accessed: 18th January 2018)
2.
Actually a parasitoid, an organism that spends a large portion of its life attached to or inside a host organism, and the host is ultimately killed.
3.
Cade, W. Acoustically Orienting Parasitoids: Fly Phonotaxis to Cricket Song. S 190, 1312–1313 (1975). [Source]
4.
Zuk, M., Rotenberry, J. T. & Tinghitella, R. M. Silent night: adaptive disappearance of a sexual signal in a parasitized population of field crickets. B 2, 521–524 (2006). [Source]
5.
Cicadas uses a different method of producing sound. https://en.wikipedia.org/wiki/Cicada#Song.
6.
Stridulation. Use of Sound to Attract a Mate in Crickets and Cicadas (2018). Available at: https://attractingamatewithsound.weebly.com/stridulation—the-crickets.html. (Accessed: 18th January 2018)
7.
Tinghitella, R. M. Rapid evolutionary change in a sexual signal: genetic control of the mutation ‘flatwing’ that renders male field crickets (Teleogryllus oceanicus) mute. H 100, 261–267 (2007). [Source]
8.
Crickets live for about three months. So 20 generations is anywhere between 2.5 to 5 years. This is lightning quick in evolutionary terms.
9.
Lax sexual selection of female crickets in Kauai. Quick evolution leads to quiet crickets (2016). Available at: https://evolution.berkeley.edu/evolibrary/news/061201_quietcrickets. (Accessed: 18th January 2018)
10.
TINGHITELLA, R. M., ZUK, M., BEVERIDGE, M. & SIMMONS, L. W. Island hopping introduces Polynesian field crickets to novel environments, genetic bottlenecks and rapid evolution. Journal of Evolutionary Biology 24, 1199–1211 (2011). [Source]
11.
Spread of the cricket population. Tropical crickets hitchhike their way to rapid evolution (2011). Available at: https://beacon-center.org/blog/2011/04/04/beacon-researchers-at-work-tropical-crickets-hitchhike-their-way-to-rapid-evolution/. (Accessed: 18th January 2018)
12.
Balenger, S. L. & Zuk, M. Roaming Romeos: male crickets evolving in silence show increased locomotor behaviours. A 101, 213–219 (2015). [Source]
13.
Especially in contrast with the seafaring Polynesians who, it must be said, travelled widely but slowly.
14.
Yong, E. The Silence of the Crickets, The Silence of the Crickets. Phenomena (2014). Available at: http://phenomena.nationalgeographic.com/2014/05/29/the-silence-of-the-crickets-the-silence-of-the-crickets/. (Accessed: 18th January 2018)
15.
The movement of genes between populations through the migration of organisms or gametes.
16.
Pascoal, S. et al. Rapid Convergent Evolution in Wild Crickets. C 24, 1369–1374 (2014). [Source]
17.
Process in which two distinct lineages evolve a similar characteristic independently of one another. This often occurs because both lineages face similar environmental challenges and selective pressures.
18.
Hope Dennett doesn’t mind.
Facebook Comments

2 Replies to “The Very Quiet Crickets of Hawaii : Rapid Convergent Evolution”

Leave a Reply

Your email address will not be published. Required fields are marked *