(A) Ants with a round aphid excreting honeydew. (B) Flat aphids (arrows) in a brood chamber among ant larvae. (C) Flat aphid probing an ant larva. (D) Hemolymph leaking from an ant larva subjected to probing by an aphid (arrow) / A. Salazar et al., PNAS
Janet Fang 13 Jan 2015, 02:35

Wingless, root-dwelling aphids from the same species can come in two different shapes: round or flat. While the round sapsuckers maintain a peaceful, mutually beneficial relationship with ants, the flat aphids mimic ant larvae, and once they’re carried into the ant nest, they feed on the real larvae. The findings were published in Proceedings of the National Academy of Sciences this week. 

The best known aphid-ant relationship is a mutualistic one: Aphids excrete honeydew droplets for ants, and the ants clean and protect them in return. Some ant species even bring aphids or aphid eggs into their nests over the winter to help ensure the continuity of this relationship. But the evolutionary transition between interspecific cooperation and exploitation is a tenuous one, and this new work highlights a complex system that exists right at the interface between the two.

An international team led by David Martínez-Torres of Universitat de València studying two distinct but genetically identical morphs of Paracletus cimiciformis—a flat, yellowish white one and a round, olive-green one—have discovered a second, vampiric relationship between aphids and ants. They raised a dozen colonies of ants and watched how they responded to flat and round aphids presented to them on a shoot of wheat in a plastic container connected to the ant nests. 

The round morph maintains a conventional relationship with ants. The flat aphids, on the other hand, chemically imitate the cuticles (or outer shell) of Tetramorium semilaeve ants. That way, they’re transported by the ants into a brood chamber, where they’re cared for as adopted young. But once there, the flat aphids use their mouthparts to pierce the actual ant larvae and suck their hemolymph (a vital internal fluid that’s equivalent to blood for us). "According to our observations, ants that adopt flat aphids do not realize they are being parasitized by the aphids," Martínez-Torres tells New Scientist

The team used a technique called gas chromatography-mass spectrometry to analyze the chemicals (hydrocarbons, in particular) that are produced in the cuticles of aphids. The innate cuticular hydrocarbon profile of the flat, mimic morph resembles the profile of ant larvae—more than that of the genetically identical round, non-mimic morph. Few arthropods are known to biosynthesize cuticular chemicals of their deceived hosts to exploit their resources. 

This simultaneous existence of two very different evolutionary strategies in a single species is the first known case of "aggressive mimicry" in aphids. 

And in this tale of two aphids, the sneaky instance of parasitism could be helping the insects survive in the wintertime. The round aphids produce a generation of flat ones, which are carried into the warm, underground nests of ants. In the spring, New Scientist explains, the ants bring the flat aphids back to the surface (like they would with their own), and there, round aphids are produced again to keep the mutually beneficial relationship going. 

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