Large interclone differences in melezitose secretion in the facultatively ant-tended black bean aphid Aphis fabae

Many aphids are known to engage in a trophic mutualism with ants, whereby the aphids secrete sugary-rich honeydew which is collected by the ants for food, and the ants, in exchange, protect the aphids against natural enemies. Previous results, however, suggest that the production of some of the honeydew sugars, such as the ant-attractant trisaccharide melezitose, may induce an indirect cost to the aphids. This led us to believe that large differences in the nature of the secreted honeydew might exist, due to some clones capitalizing more or less on their mutualistic interaction with ants, or due to some “cheater” clones foregoing the production of particular sugars, instead taking advantage of the ant-attracting effect of other non sugar-deficient clones, co-occurring on the same plant. Here we present data on clonal variation in the composition of honeydew of the black bean aphid Aphis fabae which confirm this prediction. In particular, our results show that there was large interclone variation in the amount of glucose, melezitose and total sugar produced. The variation in the production of melezitose, however, showed particularly large differences, with 54% (7 out of 13) of the clones screened being virtually deficient for the production of this sugar, irrespective of whether the aphid colonies were ant-tended or not. The consequences of this finding in the context of the evolution and maintenance of the ant–aphid mutualism, as well as the adaptive benefits of oligosaccharide synthesis in aphids and other insects are discussed.

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► Aphids excrete sugary-rich honeydew and in exchange ants protect aphids against predators.
► We provide the first evidence of large interclonal variation in the composition of aphid honeydew.
► Half of aphid clones were deficient for the production of the ant-attractant sugar melezitose.
► We discuss this in relation to ant–aphid mutualism and oligosaccharides synthesis in insects.