An aphid that simultaneously cooperates and fights ants

Experts in ecological chemistry at the CSIC have participated in a study that unveils, in aphids, the first case of aggressive mimicry against ants. The scientists have found out that the aphid mimics the cuticular chemicals -and therefore the smell- of the ant larvae in order to be transported to the nest, where it will feed on the hemolymphs of ant larvae.   

Images obtained during research.  Top to bottom  and left to right: ants approximate to the flat aphid; the brood chamber in the nest, with aphids (red arrow) already inside; an aphid pierces an ant larva to suck its hemolymph; afterwards the attack: hemolymph leaking from an ant larva.Paracletus cimiformis is an aphid which, as most aphids, has a mutualistic relationship  with ants, where both get benefits: the ants feed on the honeydew excreted by aphids and the aphids receive the protection and cleaning services from ants.
 
Now, a scientific study has unveiled another surprising interaction between this aphid and ants: aggressive mimicry. One of the morphs of the aphid imitates the hydrocarbon molecules that larvae have on the cuticle. Therefore, the ants ‘recognize’ the aphids by the smell, transport them to the nest and care for them as if they were true ant larvae. Once the aphid is in the brood chamber, it pierces the larvae and feed on their hemolymph.

This is the first case described of aggressive mimicry combined with mutualistic relationship in aphids, and it has been discovered in a study led by the Institut Cavanilles of Biodiversity and Evolutive Biology of the Universitat de València. The work has counted on the contribution of the CSIC’s Institut de Química Avançada de Catalunya (IQAC).

The flat morphs of the aphid mimic the hydrocarbon molecules of the larva; therefore, the ants ‘recognize’ the aphids, and transport them to the nest and care for them

P. cimiformis is a case of poliphenism: within the descendants there are several different morphs, which are genetically identical but have different phenotype, so they are  physically different. At certain moment of the biannual and complex life cycle of P.cimiformis, there are simultaneously two morphs of the aphid: one which is round and establish a mutualistic association with the ants, and another morph, which is flat and establish an aggressive  relationship with the ants, as the scientists have unveiled in this study.  

12 ants - aphids communities analyzed

Scientists have analyzed 12 ant colonies, each one with hundreds of ants, and their relationship with the aphids. As they saw, the round aphids were never transported into the nest by the ants. On the contrary, the flat aphids, which have the aggressive behavior against ants, were always introduced into the nest by the ants and, most of the times, into the brood chamber.

In order to know whether this behavior was caused or not by the smell, scientists analyzed and compared extracts from the cuticles of the two aphid morphs (round and flat) and of the ant larvae. This part of the work was carried out by Carme Quero, CSIC researcher at the Institut de Química Avançada de Catalunya (IQAC) and Benjamin Fürstenau, also at the IQAC at the moment of the study. Both were working in the Ecological Chemistry group, specialized in the study of pheromones and in the development of biological methods for controlling plagues.

Firstly, the scientis analyzed the extracts using gas chromatography coupled with mass spectrometry and saw that most of the molecules identified were present in the three extracts, although in different concentrations, with the exception of three compounds, which were only present in the flat aphid and the larvae ant extracts.  
 
Complementary analyses were carried out with electro-antennogram (a specific technique to study odoriferous molecules in insects) coupled with gas spectrometry, with similar results. Six out of the 31 identified compounds  provoked responses on the antennae of adult ants and, again, tree of the compounds were found only in ant larvae and flat aphids extracts.

Dummies impregnated with the molecules

Then, the scientists impregnated with extracts from round aphids several dummies, which were placed with the other aphids. Similarly, other dummies were impregnated with the extracts from ant larvae. In both cases, ants transported -almost always- the dummies to the nest. Other dummies were impregnated with extracts from round aphids, but they were never taken to the nest.  

Results show that ants are capable of differentiating between the cuticle profiles and that the flat aphid mimics the cuticle molecules in order to be transported to the nest an to the brood chamber.

The study adds a new dimension to the classical ant-aphid relationship and unveils a complex system which arise new questions about evolution between cooperation and exploitation behaviors. The coexistence of these two evolutionary strategies in the same species –on one hand, collaboration and, on the other hand, aggression- is unusual and intriguing.

Videos recorded in this research work can be seen in the PNAS magazine web site .

Adrián Salazar, Benjamin Fürstenau, Carmen Quero, Nicolás Pérez-Hidalgo, Pau Carazo, Enrique Font, David Martínez-Torres. Aggressive mimicry coexists with mutualism in an aphid. Proceedings of the National Academy of Sciences (PNAS). DOI: 10.1073/pnas.1414061112