What Insects Go Through Is Even Weirder Than We Thought

“For me, it was a road-to-Damascus type of moment,” James Truman, an entomologist, told me, recalling an encounter when he was sixteen. “My family had a summer place, a trailer, on the shores of Lake Erie. I was walking through the trailer park when I looked up and I saw an insect up in a tree. It was a parasitic wasp, with an abdomen three inches long.” He thought, What the heck is that? That curiosity “caused me to get a book,” Truman said. It was “Field Book of Insects,” by Frank E. Lutz, first published in 1918, with detailed drawings by the scientific illustrator Edna Libby Beutenmüller. “I had always known I wanted to be a biologist, but I had flipped from one interest to another: birds, mammals, whatever,” Truman said. Then he was transformed. He knew he would study insects.

Insects are small, sure, but they represent more than eighty per cent of animal species. They also have a special magic: most of them undergo complete metamorphosis. The ladybug begins life as a spiky black crawler; the garden tiger moth starts out life as an extravagantly furred caterpillar. Some fish and amphibians also metamorphose (mammals never!), but because insects have exoskeletons—their metamorphic transformation happens out of sight—when the adult creature emerges, fully formed, the effect can be as astonishing as Athena transforming a falling Perdix into a partridge, or Daphne being turned into a laurel tree.

As a freshman at Notre Dame, Truman worked in a mosquito-genetics lab, run by the renowned entomologist George Craig, who spent time with his arms over mesh-covered paper boxes that were filled with mosquitoes, which would feed—suck his blood—while he ate his lunch. When Truman arrived, Craig’s lab, which mostly focussed on identifying mutations that might aid in ameliorating mosquito-borne diseases, had a side project looking at a pheromone called matrone. During mating, the male mosquito releases matrone, and as a result the female mosquito no longer wants to mate. “She just wants blood,” Truman said. Female mosquitoes therefore mate only once. “That was so amazing to me,” Truman noted, “that a hormone could cause such a dramatic behavioral change.”

Truman did his graduate work in the lab of the biologist Lynn Riddiford, at Harvard. She was also interested in hormonal and other factors affecting how insects grew and behaved. (The two later married, though Riddiford told Truman that she wouldn’t marry him until he graduated.) This line of inquiry continued to shape Truman’s research. “I was working with giant silk moths,” Truman said, a creature with a life cycle as shape-shifting as that in any Ovid story. At first, it’s a tiny caterpillar, about six to seven millimetres long. It then molts four times—during which it grows to nearly a thousand times its original size—wraps itself in a cocoon of silk, emerges as a large moth that has no functional mouth, and cannot eat, and therefore will die before even seven days have passed, and so aims to mate immediately. Truman studied the hormones that regulate these shifts and “got hooked on metamorphosis, and interested in the behavior in metamorphosis,” he said. “These interests coalesced into wanting to understand how the brain, specifically, changes in metamorphosis. I wanted to understand how the brain of a caterpillar changes into the brain of a moth.”

During a sabbatical at Cambridge University, Truman and Riddiford took a break from working on moths and started to look at Drosophila, more commonly known as fruit flies. “There were no genetic tools for these giant silk moths, but there were good genetic tools for Drosophila,” Truman said. Scientists have an extraordinarily detailed knowledge of fruit flies’ genetic makeup. Tools exist to knock out specific genes and alter how or when a gene expresses itself. You can easily order fruit flies with all manner of mutations—you can even order one with a gene mutation that causes the flies to grow legs where they normally grow antennae. Such research dates back to work done nearly a century ago by the biologist Thomas Hunt Morgan, who ran what was termed the Fly Room at Columbia University. Nowadays, researchers have access to more than two million lines of Drosophila; this allows for precise manipulation of pretty much any biological aspect you can conceive of in either the larval or the adult stage. “In fruit flies, we are only imagination limited, not technically limited,” Truman said.

Truman and his team wanted to know, in great anatomical detail, how much of the brain of a larva persists in that of an adult fly. “We can imagine with a little grasshopper that the experiences it has growing up could shape how its brain works,” Truman said, using the example of grasshoppers because they do not undergo complete metamorphosis. “But what about when the change that happens to an insect is so massive,” as with complete metamorphosis? “Do you then come out a tabula rasa? Or is your adult life biased somehow by your life as a larva?” In a recent paper published in the journal eLife, Truman’s team tracked how the neural connections were altered in the transition from Drosophila larva to adult—what was remodelled, what was destroyed, what was generated anew.

Truman’s team looked at a neural center of the larval brain, known as the mushroom body, that mediates olfactory learning. For an insect, smell is by far the most important sense. A larva might learn to associate a certain smell with something positive or negative. But does an adult fruit fly remember that connection formed in youth? We might think of this as a Pavlov’s fruit-fly question. What Truman’s team did was find a way, in anatomical detail, to see whether any of those neuronal connections were stable through metamorphosis, “to see if there was any continuity,” Truman said. “There was none. I mean, the brain is a complicated place. But, at the simplest level, those neuronal relationships were scrambled, they were gone.”

We often think of our “self” as situated in our brains. Truman’s work reminds me of the classic question of whether the ship of Theseus remains the same if each board and part of it gets replaced; it is a kind of identity koan for metamorphosing arthropods. “It is the ultimate ‘me, myself, and I’ situation,” Bertram Gerber, the head of the Genetics of Learning and Memory Department at the Leibniz Institute for Neurobiology, said. Gerber described Truman’s work as the “deepest look yet at what happens to the brain” in metamorphosis, noting that it shows, with “unprecedented detail, precision and experimental elegance” how the connections in the insect brain are so dramatically pruned and regrown.

Though we swat and stomp them—if we’re not trying to ignore them—insects collectively have a biomass larger than humans’. They were not always so dominant. During the early Carboniferous period (some three hundred and seventy-five million years ago), when there were metre-long scorpions and six-metre-long crocodile-like creatures, insects somehow developed wings. “No one else could fly for about fifty million years—the insects had the air all to themselves,” Truman said. However, fossils show that the little wings of very young insects were vulnerable to damage; one evolutionary solution was to have the wings develop inside of a protected wing pad. The wings could then emerge when the insect was an adult, a pattern of growth we see today in grasshoppers and cicadas, among others. It’s a change—a metamorphosis—but it is termed “incomplete.” It’s not as dramatic as the classic example of a caterpillar becoming a butterfly, a change so intuitively implausible that in the nineteenth century a naturalist was arrested in Chile for leaving caterpillars with a girl and telling her that if she fed them they would become butterflies; the townsmen in power deemed it a heresy.

Tens of millions of years after the development of wings, complete metamorphosis emerged. “It happened, and then the insects exploded in terms of diversification, numbers,” Truman said. Ants, bees, flies, mosquitoes, moths—these very successful orders all undergo complete metamorphosis, and all have a common ancestor.

The practical benefits of metamorphosis are not immediately clear to a nonbiologist. Metamorphosis seems excessively magnificent, elaborate. What reward could merit the labor of transforming one’s body so radically? Truman recalled, “My old instructor Carroll Williams used to say, ‘A caterpillar is a gut on caterpillar treads, which then changes into a flying machine dedicated to sex.’ ” Metamorphosis allows for extreme specialization: feeding and growing in the larval stage, then mating in the adult stage. “If you look at an example of incomplete metamorphosis, like grasshoppers—the baby grasshopper and the adult grasshopper eat the same thing, and so are competing for resources,” Truman said. “Suddenly, with metamorphosis, you can separate the resources.” A caterpillar will eat leaves; a butterfly will feed on nectar. What’s more, a short-lived larva can adapt to eat food sources that are ephemeral, like fruit flies on a rotting half-orange, or dung beetles on deer droppings.

Part of what stands out in the work done by Truman and Riddiford over the years is their well-supported conjecture that, in insects with complete metamorphosis, the early stage of the animal evolved later than the adult form. This is the opposite of the view of evolution we get—somewhat flawed, but suggestive—when we watch a tadpole, a fishy thing, grow into a frog, a creature that can go on land. The life cycle of the frog resembles a recapitulation of fish becoming amphibians, over eons. With insect metamorphosis, the time line runs, so to speak, backward, with the more recent development, the larva, appearing first and then proceeding as if reversing in time, to become the conventional adult. It is the youth that is a wild invention.

When the German botanist and entomologist Maria Sibylla Merian was thirteen, she had a paper house in which she raised silkworms and watched them make their cocoons. Merian was born in 1647, the year before the Treaty of Westphalia, which ended the Thirty Years’ War, and she apprenticed under her stepfather, a painter. As an artist, she depicted the life cycles of silkworms, caterpillars, and other changing creatures, and her work was noted for showing the creatures in their environment, with their food sources—for seeing them in their realms. Later, she left her husband and joined a religious commune for three years, then, following the death of her mother, went to Amsterdam with her two daughters and supported herself by running a painting studio and selling prints and unusual plants and insects. At the age of fifty-two, she travelled to Suriname with her daughters, and spent around two years there documenting wonders others doubted, such as a tarantula large enough to eat a hummingbird, and ants that used their bodies as bridges for other ants to cross. People who were enslaved helped Merian in Suriname in seeking out flora and fauna.

Merian may also have been the first person to document the life cycle of the parasitic wasp that so struck Truman when he was a teen. She described how some cocoons, from which she expected butterflies to emerge, instead revealed wasps. Darwin also observed parasitic wasps, saying of them that he could not convince himself that “a beneficent and omnipotent God would have designedly” created them. ♦

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