The parasitoid wasps of aphids belong to the sub-family Aphidiinae (Hymenoptera: Ichneumonoidea: Braconidae) and to the genus Aphelinus (Hymenoptera: Chalcidoidea: Aphelinidae) and, as a whole, they consist in more than 400 species able to inject their eggs into the aphid body. The parasitoid larva hatches soon after oviposition and develops through three larval instars inside the still active host, which they kill prior to pupation.
Since the successful development of the parasitoid is always fatal to the parasitized host, aphids have evolved both behavioral defenses (such as kicking or dropping off the plant to avoid parasitoid oviposition) and physiological defenses to prevent parasitoid development after oviposition. According to literature data, behavioral resistance reduces parasitoid oviposition rate, whereas physiological resistance is fatal to the parasitoid’s egg or larva.
As never thought for several decades physiological resistance to parasitoids in aphids is due to the presence of defensive symbionts rather than to genes encoded by the aphid genome. The first evidences of the occurrence of defensive symbionts have by published by Oliver et al. (2003) reporting that experimental infection with the two species of facultative bacterial symbionts Hamiltonella defensa and Serratia symbiotica increased the resistance of pea aphids Acyrthosiphon pisum to the parasitoid Aphidius ervi. As recently revised by Christoph Vorburger in Insect Science, there is now a wide set of papers reporting that symbiont-conferred resistance to parasites and pathogens is an important and widespread phenomenon not only in aphids but also in other insects.
Interestingly, the protective mechanism of H. defensa is based is not due to the bacteria alone, but the major role is played by temperate bacteriophages called Acyrthosiphon pisum secondary endosymbionts (APSEs) that infect the aphid symbiont. according to different experimental evidences, APSEs encode toxins that kill the parasitoid egg or larva and thereby protect the aphid host (Moran et al 2005).
Recently, a third bacterial species able to confer a protection against the parasitoid Aphidius ervi has been identified and this species (named Regiella insecticola) seems to be involved also in the protection against entomopathogenic fungi making defensive symbiosis more and more intriguing from an evolutionary point of view. Surprisingly, sequencing of R. insecticola genome revealed that the APSE phages were absent in this bacterial species and that the resistance was due to five categories of pathogenicity factors so that it appears that different symbionts have found different solutions to the same evolutionary challenge. At presence it is not clear how S. symbiotica protect aphids but it would be not surprising to discover that a third mechanism occurs.
Considering the strong selective advantage of an increased resistance to parasitoids, it is really surprising that most of the surveys found these bacteria to occur at low or intermediate frequencies so that aphids possessing defensive symbionts do not go to fixation in natural populations. As Vorgurger explained in his recent review, this result could be due to the balance of selective benefits and costs conferred by the symbionts as well as the balance between symbiont losses and gains that determine their frequency in a population. Different elements could be part of this balance and, for instance, it has been observed that symbiont-conferred resistance against parasitoids is reduced under heat stress suggesting that defensive symbionts of aphids may be suppressed or even eliminated during hot summer days. In view of the near-perfect fidelity of the vertical transmission of symbiotic bacteria in the parthenogenetic generations, the loss of defensive symbionts could be due to the cost of harboring these bacterial species. In particular, we can speculate a relevant cost since these bacteria provide aphids with a strong protection against parasitoid wasps. As reported in some papers defensive synbiosis shortened aphid lifespan probably as a consequence of the metabolic demands imposed by the presence of a large bacterial population in the host or in view of the costs of immune activation in the presence of symbionts, or it may be due to “collateral damages” to the host resulting from the symbiont’s production of toxins.
At the same time it is now quite clear that some parasitoid species, such as Aphidius ervi, are able to detect the presence of H. defensa (in the left photo from bacmap) in pea aphids and respond by laying two or more eggs in infected aphids to increase the chance of successful parasitism despite the defensive symbiont. Similarly A. ervi and Ephedrus plagiator are able to distinguish infected from uninfected Sitobion avenae aphids and they may reduced attacks on aphids possessing H. defensa.
The establishment of defensive symbiosis is therefore an intriguing research field not only from an evolutionary point of view, but afor its implication for biological control. Indeed this symbiosis could reduce/affect the use of parasitoid waps for biological control of pest aphids so that we have to hope that parasitoid may have the ability to rapidly evolve counteradaptations to symbiont-conferred resistance.
Vorburger C (2014). The evolutionary ecology of symbiont-conferred resistance to parasitoids in aphids. Insect science, 21 (3), 251-64 PMID: 24167113
Moran, N., Degnan, P., Santos, S., Dunbar, H., & Ochman, H. (2005). The players in a mutualistic symbiosis: Insects, bacteria, viruses, and virulence genes Proceedings of the National Academy of Sciences, 102 (47), 16919-16926 DOI: 10.1073/pnas.0507029102
Oliver KM, Russell JA, Moran NA, & Hunter MS (2003). Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Sciences of the United States of America, 100 (4), 1803-7 PMID: 12563031