Some days ago I received a twit from Marleen Roelofs suggesting me a paper published in Nature Communications and related to aphids. The paper, entitled “An insect-induced novel plant phenotype for sustaining social life in a closed system” is extremely intriguing and deals about the evolution of aphids living inside galls.
Gall aphids (in the photo from the Yavapai County Homepage) represent a primitive insect social society based on the construction of a completely closed gall on a plant and from hundreds to thousands of aphids grow inside this unusual nest and reproduce for several months in isolation.
Due to their diet enriched in sugars, aphids generally need to produce honeydew that is excreted forming a sticky coating on leaves and many gall-forming social aphids have small openings in their galls through which soldier nymphs actively dispose honeydew droplets and other colony wastes. Surprisingly, some gall aphids live within completely closed galls… but why these aphids are not drowned by accumulated honeydew? This is a good question since it could be expected that the large quantity of honeydew excreted by hundreds of aphids would quickly ﬁll up the closed gall cavity. Furthermore, when the same aphids were placed on an artificial feeding system consisting of a liquid artificial diet sandwiched by Paraﬁlm membranes, a number of honeydew droplets soon appeared around the insects.
Where is honeydew? Mayako Kutsukake and colleagues identified the sophisticated biological solution that aphids evolved to the waste problem in the closed gall system.
The gall-forming insects manipulate the plant growth and morphogenesis for their own sake in a sophisticated manner, thereby inducing elaborate plant structures as ‘extended phenotypes’ of the insects. During their nest construction, the gall inner surface is specialized for absorbing water, whereby honeydew is promptly removed via the plant vascular system. This plant-mediated waste removal is an efficient mechanism of nest cleaning, which can be regarded as ‘extended phenotype’ and ‘indirect social behavior’ of the social aphids , but seems also to be a sort of trade-off between plants and aphids since plants can al least recover a portion of the sugars that aphids have stolen by feeding. By contrast, no such water absorption was observed for the open galls where honewdew can be eliminated without any problem.
Interestingly, the aphid species examined in this study represent the tribes Nipponaphidini, Hormaphidini and Cerataphidini and the analysis of the complete set of data indicated that water-absorbing closed galls evolved at least twice independently among social aphids.
I found this paper simply amazing since it shows an elegant strategy for social insect colonies to persist for a considerable period in complete isolation. This is not an easy goal since (except for the inactive hibernation period), insects constantly require a large amount of food from the environment and also produce a large amount of wastes to be disposed outside. By contrast, in gall forming aphids, the plant-made nests directly provide a constant and high-quality food supply, a physical barrier against predators and parasites, mitigated environmental stresses and a mechanism for cleaning galls, the latter enabling them to evolve a unique strategy of social living in completely closed galls.
Kutsukake, M., Meng, X., Katayama, N., Nikoh, N., Shibao, H., & Fukatsu, T. (2012). An insect-induced novel plant phenotype for sustaining social life in a closed system Nature Communications, 3, 1187-1192 DOI: 10.1038/ncomms2187