[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.] [[link removed]]

CICADAS HAVE AN EXISTENTIAL PROBLEM  
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Ed Yong
May 5, 2021
The Atlantic
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_ 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
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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
[[link removed](14)01037-X]. 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
[[link removed]]. 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
[[link removed](17)31311-8].
The 17-year cicadas of Brood X have 26 to 42
[[link removed](17)31311-8],
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—_Hodg_, _odgki_, _odg_, _gkinia_, _dg_, _gk_, _kin_, _ini_, _in_, _a_,
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
[[link removed]]”—“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
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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_
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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 chains
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coursing misinformation
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and the layered disasters
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pathogens
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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 [[link removed]] is a staff
writer at The Atlantic, where he covers science._

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