The ecological relationship between ants and aphids is one of the most celebrated example of mutualism. On the surface, it seems like a fairly simplistic interaction: the aphids give food (honeydew) to the ants; the ants protect the aphids from predators.
But the more research is done, the more it’s revealed that their interaction is actually far more complex than just food for protection. For example, even when no predators are around, the mutualism persists with the aphids benefiting from a variety of effects, from increased reproduction and longevity (Flatt & Weisser, 2000) to bigger sizes (Morales & Beal, 2006). Occasionally, their relationship stops being a mutualism and the ants eat the aphids (Offenberg, 2001).
A new paper in PNAS, Aggressive mimicry coexists with mutualism in an aphid by Salazar et al. (2015), provides a new example of unexpected complexity in this mutualism.
The researchers collected 12 ant colonies from Spain and Poland. These were Tetramorium semilaeve, T. caespitum, and two unidentified species. They also collected two Spanish Paracletus cimiciformis aphids and allowed two colonies to grow parthenogenetically in the lab.
The reason for choosing this particular species is twofold. It’s been observed for some time that the nymphs live inside ant nests (Zhang et al., 1987), indicating a deeper relationship with the ants than just food – protection. The species is also very polyphenic, producing a variety of forms under different conditions (read more about phenotypic plasticity here and here). Important for this research are the two morphs that can come up during the root-dwelling phase of its life cycle.
The morph that was most known is a whitish, flat one. In 2009, Ortiz-Rivas et al. discovered the other morph, a green, round one. The conditions underlying the emergence of the forms are not elucidated completely; suffice it to say that the forms are not hardwired: a round morph can later give rise to a flat morph, and vice versa.
So with the beasts all gathered, the researchers proceeded to do a classic observational study, cataloging how the ants react to individual aphids of each morph. This is where the differences between the two morphs shone through.
With the round morph, contact with an ant causes the aphid to immediately to produce honeydew from its anal region. The ant milks the aphid and then leaves it alone… 75% of the time. 25% of the time, the ant will eat the aphid. Tough luck.
With the flat morph,something very different happened. On contact with an ant, the aphid plays dead. Then, the ants pick the aphids up and take them inside the nest, where they are licked by workers. And that’s not the end of it. After that, they are picked up by the ants and deposited where no hostile organism should dare to enter: the brood chamber.
Once there, the aphid wakes up, pierces the ant larvae, and sucks out their fluids. Infiltration mission complete. This was doubly confirmed by the researchers finding ant DNA inside these aphids.
There is only one realistic way for the aphid to pull off such a feat: chemical camouflage. Ants feel each other up with their antennae all the time. Chemicals on their cuticle allow for quick identification. For the flat aphids to be able to pass off as an ant, it has to produce a pretty much identical cocktail to fool the ants.
And indeed, it is so that the cuticle of the flat aphids is chemically more similar to that of the ants than even to that of the round ones, with three compounds in particular provoking the exact neurological response in the ant, as if that ant was touching larvae from is own nest.
This is a great little paper showing the value of classical natural history observations. The discovery of such chemical mimicry is cool in and of itself, and it opens up a new project for investigating the details of the evolution of such an intricate mimicry scheme involving two morphs of the same species obtaining distinct behaviours and morphologies. Whatever comes next from the group of researchers will surely be fascinating!
If it were me, I would start by finding out how many Tetramorium species the flat aphid is successful at infiltrating, investigating it at a population level. The two Tetramorium species that responded to the aphid in this study are fairly close. A robust phylogeny of Tetramorium species does not exist (to my knowledge!), but I do know that T. hungaricum is more closely related to T. caespitum than T. semilaeve. If T. hungaricum reacts the same way to the aphid, then this would provide a strong reason to investigate this mimicry in a coevolutionary context. To be fair, the researchers thought of this already by doing a quick a phylogeny of the two unknown species they collected, and its results are discouraging for this idea. I would still like a taxonomically and biogeographically comprehensive look at the hypothesis.
Just my two cents. Read this paper in an evolutionary biology journal club and see what else you can come up with!
- Flatt T & Weisser WW. 2000. The effects of mutualistic ants on aphid life history traits. Ecology 81, 3522-3529.
- Morales MA & Beal ALH. 2006. Effects of Host Plant Quality and Ant Tending for Treehopper Publilia concava. Annals of the Entomological Society of America 99, 545-552.
- Offenberg J. 2001. Balancing between mutualism and exploitation: the symbiotic interaction between Lasius ants and aphids. Behavioral Ecology and Sociobiology 49, 304-310.
- Ortiz-Rivas B, Martínez-Torres D & Hidalgo NP. 2009. Molecular phylogeny of Iberian Fordini (Aphididae: Eriosomatinae): implications for the taxonomy of genera Forda and Paracletus. Systematic Entomology 34, 293-306.
- Salazar A, Fürstenau B, Quero C, Pérez-Hidalgo N, Carazo P, Font E & Martinez-Torres D. 2015. Aggressive mimicry coexists with mutualism in an aphid. PNAS 112, 1101-1106.
Zhang T-Z, Zhang G-X, Wang J-Z, Lu C-L, Shi R-Z. 1987. Studies on the bionomics of Paracletus cimiciformis von Heyden (Aphidoidea: Pemphigidae). Acta Entomologica Sinica 30, 186–192.