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The Slow-Motion Symbiotic Train Wreck of the 13-Year Cicada

Round about now, in various US states, a vast swarm of cicadas will start crawling out of the ground. These black-bodied, red-eyed insects have stayed underground for 13 or 17 years, drinking from plant roots. When they greet daylight for the first time, they devote themselves to weeks of frenzied sex and cacophonous song, before dying en masse. They’ll be picked off by birds, snagged by squirrels, and crunched under shoes and tyres, but none of that will dent their astronomical numbers—which is perhaps the point of their lengthy underground stints, and their synchronous emergence.

But the cicada’s weird lifestyles have also left them with a different legacy. It involves the bacteria that live in their bodies, and it’s so weird that when John McCutcheon first discovered it, he thought he had made a technical error.

Many insects carry bacteria inside their cells. These ‘endosymbionts’ are especially common among sap-sucking bugs, like cicadas, and help their hosts to make nutrients that they can’t get through their food. They almost always have exceptionally tiny genomes. Once they get inside insect cells, they become isolated from other bacteria and restricted to small populations. This deprives them of opportunities for shuffling or acquiring genes, and allows harmful mutations to build up in their DNA. One by one, their genes break and disappear, leaving them with shrivelled minimalist genomes.

McCutcheon is one of a small cadre of scientists who, over the past 15 years, have deciphered the weird genomes of many insect symbionts. When he started his own lab at the University of Montana, he decided to look at Magicicada tredicim—one of the periodical 13-year species. He did the usual thing: he dissected out the organs where the bacteria live, pulled out their DNA, cut it into fragments, sequenced the pieces, and used a computer to assemble those portions into a coherent whole.

Except, it didn’t work. The sequences just wouldn’t assemble neatly. It was as if someone had taken several similar but incomplete jigsaw puzzles, and jumbled all the pieces together. “It was just such a mess,” he says. “I thought it was something technically wrong but I couldn’t figure out what.”

Perplexed, he moved on to a different cicada—a South American species called Tettigades undata. There, he found yet more weirdness. It contained a bacterium called Hodgkinia, which had somehow split into two distinct species inside its insect host. As I wrote last year, these daughter species are like two halves of their ancestor. They’ve each lost different genes so that individually, each is a pale shadow of the original Hodgkinia, but collectively, they complement each other perfectly.

When McCutcheon worked out what was going on in T.undata, he suddenly realised what was happening in the 13-year cicada. It also contained Hodgkinia symbionts that had split into separate lineages—and not just two.

Graduate students Matthew Campbell and James Van Leuven eventually showed that the DNA from this cicada’s symbionts form at least 17 distinct circles. It’s not clear if each of these represents a Hodgkinia chromosome, or an entire Hodgkinia genome on its own, but at least four of them are found in distinct cells You can see this in the images below, where the blue, green, purple, and orange dots all represent cells that have just one of the 17 circles.

Hodgkinia cells in cicada tissue. Credit: Campbell et al, 2015. PNAS.
Hodgkinia cells in cicada tissue. Credit: Campbell et al, 2015. PNAS.

As in the earlier discovery, these circles complement each other; they share sets of genes for making nutrients that matter to the host, but none of them has the full complement. They’re also found in other species of periodical cicadas. And they might just be the tip of the iceberg: the team could confidently identify 17 circles, but the insects likely harbour many more. “If I had to guess, I’d say there’s between 20 and 50,” says McCutcheon. “It’s incredible. It’s a mess.”

From Hodgkinia’s point of view, one lineage has clearly split into several, and irreversibly so. “That’s the baseline definition of speciation,” says McCutcheon. “It’s happening in an asexual population, but the lineage has fractured and it’s not going back.” But if you take the cicada’s perspective, the collective symbionts are still doing the same thing as the original. And while they parcelled their genes into separate cells, the total amount of bacterial DNA has increased. Each part became smaller, but collectively, their genome got bigger.

So are the Hodgkinia circles different species or lineages? Is the Hodgkinia genome the total of the circles in a single cicada, or does each distinct lineage have its own genome? It’s really hard to say. “The problem is that when we write a paper, we have to use words, and words mean something,” says McCutcheon. “It is very hard to put labels on this stuff, and I will not just give this a new name willy-nilly, because I don’t think we understand it well enough.”

There are other mysteries too. The cicada also has another bacterial symbiont called Sulcia, which shows no sign of this ridiculous fragmentation. There’s just one Sulcia and it’s the same in all cicada cells. Why has this microbe stayed whole, while its neighbour rent itself asunder? No one knows. A reasonable guess is that Hodgkinia evolves much faster than Sulcia, and more quickly builds up mutations that disable its genes.

Also, why has Hodgkinia fractured into many lineages within cicadas, when other insect symbionts have not in their respective hosts? McCutcheon thinks the answer lies in the insects’ long lives. Most sap-sucking bugs are lucky to make it past their first birthday. They lead short, fast lives, and if their symbionts developed detrimental mutations, they and their hosts would be weeded out by natural selection. Cicadas, by contrast, can live for 2 to 19 years, and for most of that time, they’re barely moving or growing. During those slow years, their symbionts aren’t that important, and are free to build up detrimental mutations without affecting their hosts or falling foul of natural selection—at least, not in the short term.

The long-term outlook may not be that rosy. Partnerships with microbes often furnish animals with incredible and valuable skills—in this case, the ability to drink plant sap without becoming deficient in important nutrients. But with great opportunity comes great risk. Once host and bacterium become dependent on each other, they can enter into a kind of symbiotic trap—or, as Nancy Moran puts it, they could jointly “spiral down the symbiosis rabbit hole”.

Take Hodgkinia. If it continues to fragment and degenerate, it—they?—may eventually be unable to sustain the cicada. “It just looks like it’s going off the rails,” says McCutcheon. “It’s like watching a train wreck or a slow-motion extinction event. It makes me think differently about symbiosis.”

Reference: Campbell, Van Leuven, Meister, Carey, Simon, and McCutcheon. 2015. Genome expansion via lineage splitting and genome reduction in the cicada endosymbiont Hodgkinia. PNAS http://dx.doi.org/10.1073/pnas.1421386112

9 thoughts on “The Slow-Motion Symbiotic Train Wreck of the 13-Year Cicada

  1. Ed — First, thanks as always for your wonderful writing. Second, I was confused by the final argument. During the “slow years” when the cicadas are “barely moving or growing”, what they are mostly doing is sucking up nutrient poor sap and subsisting on that. Since what the Hodgkinia is doing for the cicadas is providing them with “the ability to drink plant sap without becoming deficient in important nutrients” surely any mutation that prevented (or substantially impeded) Hodgkinia from doing that “incredible and valuable” job would mean curtains for the individual cicada carrying it (or substantially reduced reproductive success).

  2. I understand these relationships between microbes and their hosts. I was shocked to discover in the last few days here in Jonesboro, Illinois, a cicada I’ve never seen before. They are white! Is this a genetic mutation, or could it be something else in the life cycle that makes them this color?

  3. After reading the article, I began to wonder if the findings could be interpreted from a different angle. What if Hodgkinia has fractured into 17 different lineages in order to deal with some environmental stress? Perhaps the arrangement where nutrient-making activities are divied up between different types of the bacteria offers some survival advantage to both the bacteria and the host

  4. “They are white! Is this a genetic mutation, or could it be something else in the life cycle that makes them this color?”

    Likely one that had just shed its last nymphal exoskeleton and was still pale before the new exoskeleton sclerotized.

  5. SP: they key point is that Hodgkinia (and Sulcia) make amino acids, which are important at all times but are especially important when organisms are putting on mass. Long-lived cicadas stop putting on much mass for a number of years, but they still need to maintain their symbionts for the next generation. It may be this period that’s important, or it may just be that in long-lived cicadas Hodgkinia undergoes more rounds of genome replication, and so more mutations accumulate. Or perhaps both.

    Billy Dean: check out these images from Alex Wild, do any of these cicadas look like the ones you saw?

    http://www.alexanderwild.com/keyword/periodical%20cicadas/

  6. How does colonization happen in the first place? I assume they are inherited, like mitochondria in an egg, but could cicada sex be preventing further deterioration somehow?

  7. This is a great article although the first use of the word “circles” threw me. Yeah, what makes a species a species and how DO you write a paper on a hot mess? Wild stuff. I wonder if certain fragments of Hodgkinia are only found in certain organs, and, if so, whether having certain proteins synthesized in certain places allows them to remain almost in stasis, prolonging their buggy lives.

  8. I’ve seen a lot of comments on this research (and I’m a collaborator through http://www.magicicada.org), and I think it’s important to stress a few things: First, we are at the early stages of this discovery, and while such “fragmentation” could be a bad thing for the parties involved in this symbiosis, it could also be a good thing– or at least something that works in favor of one party. For instance, any organism that plays host to a variety of internal symbionts needs some way to keep them under control- so it’s possible that the fragmentation of the Hodgkinia is part of a “divide and conquer” strategy that benefits the host cicadas. If so, that hypothesis prompts a whole series of interesting tests and modeling of coevolution. Secondly, there are seven species of periodical cicadas, and they are all doing roughly the same thing. The most basal split in the lineage is several million years ago, so under the assumption that ancestry is the source of their common internal architecture, this odd internal arrangement seems fairly stable. Thirdly, longitudinal studies on the development of internal diversity have not been conducted, but if that diversity is generated de novo each generation by the accumulation of mutations in the Hodgkinia, than that should be demonstrable, given some time, a shovel (nymphs live underground but are easy to find), and patience. Lastly, if it is true that internal symbiont diversity is a product of long life cycle, then given that there are two life cycles in the periodical cicadas, the 17-year species might be expected to have greater internal diversity than the 13-year species– given allowances for those species (e.g. M. neotredecim) that have undergone relatively recent life cycle switches. There are some fairly explicit predictions buried in all this, so it’s just a matter of working them out and getting the data– not always easy with periodical cicadas.

  9. Circles because Bacteria have circular DNA structure. For anyone else confused on the mention of Circles. If this happened to any other organism with a more complicated DNA structure like Mammals. It would probably take decades to figure out what had happened when the DNA was being sequenced.

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