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Cicadas Have an Existential Problem

Cicadas, like us, have come to rely on an interconnected ecosystem of their own creation that becomes more unwieldy and fragile with time, and that they can barely control.

"Cicada" by balharsh, licensed under CC BY-NC 2.0

When the cicadas of Brood X start to swarm the United States in their billions, try to look beyond their overwhelming numbers. Instead, focus on just one of them. Despite appearances, that individual cicada will be a swarm unto itself—the insect and a community of organisms living inside it. Their lives have been so tightly entwined that they cannot survive alone. Their fates have been so precariously interlinked that their future is uncertain. And their relationship is so unusual that when John McCutcheon first stumbled upon it in 2008, he had no idea what he had found. Sitting in a basement laboratory and staring at the data, his reaction was less Eureka! he told me, and more How did I mess this up?

Many insects harbor beneficial bacteria called endosymbionts, which live permanently inside their cells. Cicadas usually have two—Sulcia and Hodgkinia. Between them, they produce 10 amino acids that are missing from the cicadas’ diet of plant sap. Because those amino acids are essential, so too are the bacteria. Without them, the cicadas can’t survive. The opposite is also true: Inside the cushy confines of their insect hosts, endosymbionts eventually lose the genes they’d need to exist independently. They become forever tethered to their insects, and their insects to them.

McCutcheon began studying this partnership in 2008. He remembers his boss, Nancy Moran, an endosymbiont expert at the University of Texas at Austin, leaning into a freezer and fishing out a brown paper bag full of dead cicadas, which had been collected during the previous emergence of Brood X. McCutcheon thawed them, dissected them, and tried to sequence the genomes of their endosymbionts. Normally, sequencing a genome is like solving a jigsaw puzzle—you end up with many small DNA fragments that must be assembled into a single picture. But with the cicada endosymbionts, McCutcheon simply couldn’t get the pieces to fit. It was as if he was trying to solve several jigsaws at once, all of which were missing pieces. “It was all weird and broken—tiny little pieces of junk,” he said. “I told Nancy that I messed up.” It took him years to realize that he actually hadn’t.

In 2014, McCutcheon was running his own lab, and still studying cicadas. He had shown that most of these insects contain Sulcia and Hodgkinia. But his student James van Leuven discovered that in one South American species, Hodgkinia had somehow split into two distinct microbes. Think of them as Hodg and kinia—two halves of a former whole, each containing a subset of its ancestor’s genes. Only together can these two half bacteria furnish the cicada with the essential amino acids that the full original could produce.

After analyzing other cicadas, McCutcheon realized that Hodgkinia splits readily and profusely. Some cicada species have two versions. Others have three, or four, or six. His student Matthew Campbell found that the periodical cicadas have at least 20. The 17-year cicadas of Brood X have 26 to 42, and probably many more; at some point, things got so complicated that the team stopped counting. That’s why McCutcheon’s data didn’t make any sense back in 2008: Without knowing, he really was trying to solve dozens of incomplete and jumbled jigsaws.

Every 17-year cicada, then, is effectively dozens of organisms in a single body—the cicada, Sulcia, and who knows how many versions of Hodgkinia. The multiple versions are always just small slivers of the ancestral one—Hodgodgkiodggkiniadggkkininiina, and so on. None of these is useful on its own, and the cicada needs close to the full set to get its amino-acid fix. It’s like a chef who’s trying to bake one cake using 42 tiny kitchens, each of which has only a couple of the necessary utensils and ingredients.

Of the many endosymbiotic bacteria that coexist with insects, Hodgkinia seems to be the only one that fragments in this ludicrous way. The reason is unclear, but McCutcheon suspects that it might involve cicadas’ relatively long life. Extended lifespans provide more time in which rare evolutionary events can occur, such as the splitting of a single microbe lineage. It’s probably no coincidence that the most heavily fragmented microbes exist in the 17-year cicadas, which live the longest. “It was almost like a mirror of the cicada’s life cycle, how long it took us to figure this out,” McCutcheon told me. “But I love it so much. It’s so wildly complex. The insects themselves are so cool, their endosymbionts are unbelievably messed up, and they’re all going to overwhelm the eastern U.S. It’s fantastic.”  

It’s less fantastic for the cicadas. They get no benefit from having fragmented endosymbionts. If anything, fragmentation is a curse. Because almost all of the Hodgkinias are necessary, the entire alliance is vulnerable to the loss of any one member. (If one of those 42 kitchens accidentally catches fire, they all burn down, and the chef dies.) The cicadas now have to manage a needlessly complicated set of microbes, when their ancestors did perfectly well with just one (and Sulcia). They’re stuck in what Nancy Moran once called an “evolutionary rabbit hole”—“a generally irreversible journey into a very odd world where the usual rules do not apply.”

For example, once the members of Brood X emerge and mate, females will deposit a dollop of their endosymbionts into each of their eggs, to provide their offspring with the bacteria they need. But the females must ensure that this microbial heirloom contains at least one of every kind of Hodgkinia. And because cicadas don’t seem to be able to tell the different kinds apart, their solution is to shove as many Hodgkinia cells into their eggs as possible, to improve the odds of randomly getting the full collection. This is the only option available to them, but it’s a terrible one. Furnishing each egg with so many extra microbes takes energy. And because cicada eggs are hardly spacious, all the Hodgkinias leave little room for Sulcia, the other bacterium that cicadas need. “Hodgkinia is only making two of the 10 essential amino acids,” McCutcheon said. “Sulcia is making eight, but it’s getting crowded out.”

Nature is full of messes like this. Evolution doesn’t proceed according to a plan, and often has to bootstrap its way out of problems of its own making. But McCutcheon suspects that the cicadas’ plight will only get more complicated. Hodgkinia, he thinks, will continue to fragment, and the cicadas will be forced to evolve more convoluted ways of wrangling their partners. Two outcomes are possible. The first is replacement. In 2018, McCutcheon’s colleague Yu Matsuura, who works at the University of the Ryukyus, found that some Japanese cicadas have dispensed with Hodgkinia and all its messy drama. In its place, they’ve domesticated Ophiocordyceps, the infamous fungus that normally parasitizes and zombifies insects.

The second outcome is worse. Although cicadas have existed for about 200 million years, those with fragmented Hodgkinias have been around for only a few million of those. That might be because fragmentation leads to the (literal) dead end of extinction. “The periodical cicadas aren’t going to go extinct next year,” McCutcheon said, “but we know they’re not heading into a good situation.”

Cicadas might seem like creatures with concerns quite different from our own. But like us, they have come to rely on an interconnected network of parts that becomes more unwieldy and fragile with time, and that they can barely control. After a year of straining supply chainsglobally coursing misinformation, and the layered disasters of pandemic pathogens and a changing climate, the cicadas’ plight might feel eerily familiar. In a few weeks, Brood X cicadas will emerge into a world not unlike the ones inside them.

ED YONG is a staff writer at The Atlantic, where he covers science.

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