Evidence of indirect symbiont conferred protection against the predatory lady beetle Harmonia axyridis in the pea aphid.

BACKGROUND: Defensive symbionts can provide significant fitness advantages to their hosts. Facultative symbionts can protect several species of aphid from fungal pathogens, heat shock, and parasitism by parasitoid wasps. Previous work found that two of these facultative symbionts can also indirectly protect pea aphids from predation by the lady beetle Hippocampus convergens. When aphids reproduce asexually, there is extremely high relatedness among aphid clone-mates and often very limited dispersal. Under these conditions, symbionts may indirectly protect aphid clone-mates from predation by negatively affecting the survival of a predator after the consumption of aphids harboring the same vertically transmitted facultative symbionts. In this study, we wanted to determine whether this indirect protection extended to another lady beetle species, Harmonia axyridis.

RESULTS: We fed Ha. axyridis larvae aphids from one of four aphid sub-clonal symbiont lines which all originated from the same naturally symbiont free clonal aphid lineage. Three of the sub-clonal lines harbor different facultative symbionts that were introduced to the lines via microinjection. Therefore these sub-clonal lineages vary primarily in their symbiont composition, not their genetic background. We found that aphid facultative symbionts affected larval survival as well as pupal survival in their predator Ha. axyridis. Additionally, Ha. axyridis larvae fed aphids with the Regiella symbiont had significantly longer larval developmental times than beetle larvae fed other aphids, and females fed aphids with the Regiella symbiont as larvae weighed less as adults. These fitness effects were different from those previously found in another aphid predator Hi. convergens suggesting that the fitness effects may not be the same in different aphid predators.

CONCLUSIONS: Overall, our findings suggest that some aphid symbionts may indirectly benefit their clonal aphid hosts by negatively impacting the development and survival of a lady beetle aphid predator Ha. axyridis. By directly affecting the survival of predatory lady beetles, aphid facultative symbionts may increase the survival of their clone-mates that are clustered nearby and have significant impacts across multiple trophic levels. We have now found evidence for multiple aphid facultative symbionts negatively impacting the survival of a second species of aphid predatory lady beetle. These same symbionts also protect their hosts from parasitism and fungal infections, though these fitness effects seem to depend on the aphid species, predator or parasitoid species, and symbiont type. This work further demonstrates that beneficial mutualisms depend upon complex interactions between a variety of players and should be studied in multiple ecologically relevant contexts.