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Two-Faced Insect is Both Sheep and Wolf in Sheep’s Clothing

I’m laughing.

I’m laughing because I’m reading a paper about an aphid that’s occasionally a vampire—more on this later—and the caption for Figure 1 begins: “Simplified diagram of the biannual life cycle of P. Cimiciformis”. And this is Figure 1:

Credit: Salazar et al, 2015.
Credit: Salazar et al, 2015.

Simplified, indeed.

This is the absurdly complicated life cycle of the aphid Paracletus cimiciformis which includes at least 9 different bodies (or morphs), two host plants, and at least two full years. Bear in mind that aside from one tiny part of the cycle (bottom-left in the diagram), this creature reproduces asexually—the females give birth to genetically identical clones of themselves, without any need for males.

Let’s start at the top-left. In summer, the aphids live on the terebinth tree, where they trigger the growth of large tumour-like swellings called galls. Living inside, they produce clones that cycle through three distinct body shapes. As summer ends, the third of these morphs, equipped with wings, flies off in search of grasses. It burrows towards the roots and produces two more morphs—a round, olive-green one and a flat, yellowish-white one.

The aphid spends autumn, winter, and spring in these guises. Both the green and yellow morphs can convert into one another, and both have some kind of relationship with ants. The following summer, the yellow morph produces two kinds of winged clones. One flies off to find more grasses and creates more green and yellow morphs. The other seeks out terebinth trees and produces two more morphs—a male and a female, which then mate. The female lays eggs that hatch the following spring, producing gall-making morphs that start the cycle all over again.

Aphids are famed for their ability to make many distinct bodies from a single genome. But even by their standards, P.cimiciformis is extreme, and scientists keep on finding new depths to its ludicrous complexity.

For example, Adrian Salazar from the University of Valencia has now found that the yellow and green root-dwelling forms enjoy very different relationships with ants.

When a green morph feels the strum of an ant’s antennae, it responds by secreting a sweet liquid called honeydew from its backside, which the ant then drinks. In exchange for this sustenance, the ants herd and protect the aphids, behaving like human farmers towards their sheep or cows.

The yellow morph behaves very differently. When it touches an ant, it sometimes makes honeydew, but more frequently stays still and pulls its legs in. The ants pick it up and carry it into their nest, depositing it in the brood chamber where their larvae live. There, the yellow aphid unfurls and turns vampire. It stabs the young ants with its mouthparts and sucks up their bodily fluids.

Why would the ants tolerate such a menace, let alone carry it towards their young? Because they can’t tell it’s a threat. Ants rely far more on chemical senses than on sight. It doesn’t matter that the yellow aphid looks very different from an ant larva; it only matters what it smells like. And Salazar found that the yellow morph, but not the green one, has three chemicals in its outer shell that are identical to those found on ant larvae. It fools the ants into thinking that it’s one of their own young, which is why they carry it into the brood chamber.

The team proved this by extracting chemicals from the two morphs and the ant larvae, and applying them to dummy aphids. The ants would ignore the dummies that smelled like the green aphids, but they always carried the yellow-scented and larva-scented dummies into their nests. This is an example of aggressive mimicry, when predators or parasites use stealth and subterfuge to sneak up on their prey or hosts.

So, the same aphid can come in two genetically identical but wildly different forms: one that feeds ants so it can suck the sap of plants in peace; and another that tricks ants so it can suck the blood of their young in peace. It’s both the sheep and the wolf in sheep’s clothing.

Salazar’s team thinks that the vampiric yellow morph is an adaptation against harsh environments. They originally evolved to mimic ant larvae so that ants would carry them into their cushy nests, which are steadier in temperature and shielded from predators. But there are no plants inside the nests, so the aphids used their stabbing sucking mouthparts to access the only food around—the blood of the larvae.

Reference: Salazar, Furstenau, Quero, Perez-Hidalgo, Carazo, Font & Martinez-Torres. 2015. Aggressive mimicry coexists with mutualism in an aphid. PNAS http://dx.doi.org/10.1073/pnas.1414061112