Aphid-bacterial symbioses

In the last 20 years it has become increasingly apparent than many aspects of the life history of insects are influenced by symbiotic bacteria. Some symbionts are obligately associated with their hosts who can’t do without them, while others have a more ephemeral relationship.

Aphids provide examples of both types of association.  Virtually all aphids carry the obligate symbiont Buchnera which provides essential nutrients missing in the aphid diet. Buchnera is inherited strictly vertically and in many ways has become an aphid organelle with a similar status to mitochondria.

In addition to the obligate symbiont pea aphid (and other aphids) may carry further bacterial species, so-called secondary symbionts. Three species have been characterised in detail (from studies of pea aphid) and have been shown to have a range of effects on aphid biology including substituting for Buchnera after heat shock and improving resistance to parasitoids.

We became interested in secondary symbionts when studying host plant use and parasitoid resistance in a panel of aphid clones isolated from a range of different host plants.  Working with Angela Douglas’s group at York (Angela is now at Cornell) we showed a variety of non-random associations between the host plant a clone was collected on and its complement of secondary symbionts.  For example, we (and other groups) found clones collected on clover (Trifolium) nearly always carried the symbiont Regiella insecticola (1, 2) [incidentally, Regiella is named after the well-known insect physiologist, Reg Chapman].

An interesting thing about pea aphids from clover is that they show strong resistance to the common aphid fungal pathogen, Pandora neoaphidis.  Nancy Moran and Molly Hunter’s groups in Tucson, Arizona (Nancy Moran is now at the University of Texas) had shown that another secondary symbiont (Hamiltonella defensa, named after the great evolutionist Bill Hamilton) protected its aphid host from parasitoid wasps.  This prompted us to inject Regiella into aphids that carried no symbionts to see if it protected them from fungus attack.  We found it did (3); moreover, even if the fungus did kill the aphid, it was less likely to produce infectious spores and we speculated that this may reduce the probability that aphids of the same clone are infected.

In addition to Regiella and Hamiltonella, a third facultative symbiont Serratia symbiotica has long been associated with pea aphid.  More recently, another related species (X-type) as well strains of less closely relatedSpiroplasma, Rickettsia, and Rickettsiella have been shown to be common facultative symbionts.  We have found that Rickettsia, Rickettsiella and Spiroplasma (though only one of several strains) also provide protection against the fungal pathogen (Pandora) (7)

Takema Fukatsu‘s group in Tsukuba, Japan had found that removing Regiella from one clone of pea aphid reduced the insect’s ability to feed on that host plant. We asked whether the five aphid clones into which we had injected Regiella acquired the ability to utilise clover.  We found no consistent effect (4), and think that host use may be influenced by complex aphid genotype/bacterial genotype interactions.  This was supported by later work in which we cured aphids of their natural secondary symbionts using antibiotics (5).  However, it is clear that certain secondary symbionts are strongly associated with particular host-associated populations of aphids (6), and finding an explanation for these associations remains an important goal of our work.

We have several projects on aphid-bacteria interactions in the group at the moment.  We are exploring further aphid genotype/bacterial genotype interactions and how they may affect host plant use and other aspects of aphid biology.  We are also exploring the potential effects of bacterial symbionts on host plants (review in (8)), including whether presence of aphid symbionts induces a specific response from aphid food plants, and whether this impacts the wider insect community.

In collaboration with Martin Maiden‘s group, we are studying the genetic structure of symbiont communities across 1100 collections of pea aphid from throughout the world (a collaboration with Jean-Christophe Simon’s group in Rennes) and in about 100 aphid species collected in Britain.  We are exploring how phylogeny, geography and ecology combine to structure symbiont communities.

Selected publications

  • Haynes, S. , Darby, A.C., Daniell, T.J., Webster, G., van Veen, F.J.F., Godfray, H.C.J., Prosser, J.I. & Douglas, A.E. 2003 The diversity of bacteria associated with natural aphid populations. Applied and Environmental Microbiology 69, 7216-7223.
  • Ferrari, J., Darby, A.C., Daniell, T.J., Godfray, H.C.J. & Douglas, A.E. 2004 Linking the bacterial community in pea aphids with host plant use and natural enemy resistance. Ecological Entomology 29, 60-65. 
  • Scarborough, C.L., Ferrari, J. & Godfray, H.C.J. 2005 Bacterial endosymbiont increases aphid inclusive fitness after pathogen attack. Science 310, 1781.
  • Ferrari, J., Scarborough, C.L. & Godfray, H.C.J. 2007 Genetic variation in the effect of a facultative symbiont on host plant use by pea aphids. Oecologia 153, 323-329. 
  • McLean A.H.C., van Asch M., Ferrari J. & Godfray H.C.J. 2011 Effects of bacterial secondary symbionts on host plant use in pea aphids. Proceedings of the Royal Society B-Biological Sciences 278(1706), 760-766
  • Ferrari J., West J.A., Via S. & Godfray H.C.J. 2012 Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex. Evolution 66(2), 375-390.
  • Lukasik, P., Van Asch, M., Guo, H. & Godfray, H.C.J. 2012 Ecology Letters, in press.
  • Frago, E., Dicke, M. & Godfray, H.C.J. 2012 Insect symbionts as hidden players in insect-plant interactions. Trends in Ecology and Evolution 27:705-711.