BEACON Researchers at Work: Tropical crickets hitchhike their way to rapid evolution

This week we are introducing a new feature on the BEACON Blog: BEACON Researchers at Work! Please enjoy the first post from Michigan State University postdoc Robin Tinghitella.

Robin Tinghitella on KauaiWhat would happen if all the lions suddenly lost their manes, or all of the peacocks suddenly lost their tails? Equally as strange, but perhaps not as obvious to the casual observer, is the recent (and rapid!) evolutionary loss of song in Polynesian field crickets on the Hawaiian island of Kauai.

As a graduate student I studied the Polynesian field cricket, whose scientific name is Teleogryllus oceanicus. They live in grassy areas in coastal parts of Australia, and on Pacific Islands, including Hawaii. Between 1999 and 2003, a puzzling thing happened in the fields of Kauai. Imagine walking your dog in your neighborhood at night and noticing that over the course of the last few years the level of cricket noise has gone from almost deafening to near silence. What happened? Did they leave? Move to another neighborhood? That’s what we thought, but we were wrong, and the real story is much more interesting.

When you hear chirping crickets, it’s always the males making the noise. Females can’t sing, but they pay attention to males’ songs and use them to find males – they also use the information in the song to decide who to mate with, just like female peahens pay attention to the “sexy” eye spots on a peacock’s tail feathers. So, cricket songs are really critical for mating. It turns out that in Hawaii, female crickets aren’t the only ones paying attention to this cricket’s song. A fly that only encounters this cricket in Hawaii also uses the song to find a host. The fly has ears that are specially attuned to the crickets’ song. Pregnant females locate calling male crickets and spray maggots on them, which will burrow into the cricket and basically eat him from the inside out. So, singing helps you find a mate, but it’s very risky! What’s a guy to do? Here’s what evolution did: a rare mutation occurred, called ‘flatwing’, that eliminates the structures on the wing that males use to produce the song. The crickets were still there, but they had lost the ability to sing. In fly-free areas (Australia and islands outside of Hawaii) we’d expect a silent flatwing male – who would be less attractive to females – would get fewer chances to mate, and would leave fewer offspring. On fly-infested islands, mutant flatwings have the advantage – the flies can’t find them, while their singing counterparts get attacked by flies and eaten by maggots (yum).  The silent guys, meanwhile, survive to mate another day. If you traveled to Kauai today you would find that more than 95% of the males there are silent flatwings.

Fly (Ormia ochracea) on the cricket (picture by M. Read)

In my most recent paper, published with co-authors Marlene Zuk, Maxine Beveridge, and Leigh Simmons, we used genetic tools called microsatellites to answer the question of how the crickets got to Hawaii from Australia in the first place. We were also interested how long they’ve co-existed with the fly. It’s an important question, because the crickets were introduced to Hawaii by humans and we know that rapid evolution is common when new populations are founded. New populations are typically made up of very few individuals.  Think about it – how many crickets do you think might make it to a small Pacific Island from Australia with the vast open ocean in between? In addition, the environment in a new location may be very different from that of the source population (for instance, it may contain novel selection pressures, like the fly in this case).  Both of these can contribute to rapid evolutionary change. When a new colony is started by a few members of the original population, this small population size means that the colony may have reduced genetic variation (relative to the original population) and a non-random sample of the genes in the original population. It’s called a founder effect. Check out this website to learn more about founder effects and population bottlenecks.

Polynesian field crickets are not great flyers, and there are records of them in Hawaii as early as 1877. One intriguing hypothesis we had was that the crickets may have been introduced to Hawaii by Polynesian settlers who traveled around the Pacific on canoes settling on oceanic islands during the Polynesian Expansion. Polynesian folklore suggests that the calls of crickets represent the cries of dead ancestors, so Polynesians may even have purposefully moved the crickets along with them!

To answer our question, we first had to collect DNA samples from 19 populations across the crickets’ range (including eight in Australia, eight Pacific islands outside of Hawaii, and three Hawaiian Islands). We extracted DNA from the femur muscles of 5-25 crickets from each of those locations and “looked” for microsatellites, which are little pieces of repetitive DNA. Microsatellites mutate quickly, so they are a handy tool for researchers who are trying to understand relationships between groups of organisms that only became separated relatively recently – like hundreds to thousands of years ago. In a population there may be many alleles (versions) of a single microsatellite locus (location on a chromosome). We can use microsatellites to infer information about things like which populations are most closely related (another way to think about that is to ask which population the original founding Kauai crickets came from?) by looking at the proportion of shared alleles between any two populations. Lots of shared alleles means the populations are probably pretty closely related.

So, what did we find? It looks like Hawaiian T. oceanicus are most closely related to those from the Society Islands and the Cook Islands. Intriguingly, both locations are consistent with the crickets traveling with Polynesian settlers. During the Polynesian Expansion, humans colonized Hawaii at least twice and scholars agree that one of those trips started near the Societies/Cooks. Whether they hitched a ride as stowaways or were invited along with the intrepid explorers, we’ll never know, but it appears that these island-hopping crickets were introduced to Hawaii by humans, where they later encountered a deadly fly, setting the stage for the story of “how the cricket lost its song.”

Now, you’re probably asking yourself some of the very same questions that I did: Why can’t they call? Without song, how do females find mates? Why would a female mate with a male who can’t sing? All fascinating questions – but these are topics for another post!

For more information on Robin’s work, please contact her at hibbsr at msu dot edu.

About Danielle Whittaker

Danielle J. Whittaker, Ph.D. Managing Director of BEACON
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