Most people will be familiar with aphids as pests in their gardens or as the insect version of a cow--that ants "farm" in return for secreted honeydew--in nature documentaries. But an aphid's association with the ant isn't its only mutualistic relationship. This other relationship is microscopic and so vital that an aphid cannot survive or reproduce without it.
About 200 to 250 million years ago, a free-living bacterium infected an aphid ancestor. Over time, the bacteria established themselves within aphid cells. Once inside this comfortable and safe niche, the bacteria began shedding some of the essential genes required for free-living. And in return for its new home, the bacteria began producing essential nutrients like amino acids for its host. In this way, the aphid and its endosymbiont--such as a Buchnera species--became dependent on each other. But aside from ecological reasons for studying Buchnera, endosymbionts are excellent examples of bacterial evolution from free-living to intracellular. Buchnera may even be a snapshot of what a mitochondrion or chloroplast might have looked like before they were relegated to the status of organelles.
Aphids also have a very strange life cycle. Most aphids are parthenogenetic and some act like real-life tribbles--female aphids will be pregnant with daughters who are already pregnant before they are born. During the spring and summer, aphids continue to reproduce parthenogenetically, but in the autumn, males and sexual females are produced. After mating, eggs are left to overwinter until the next growing season when the parthenogenetic cycle begins anew.
Meanwhile, Buchnera live happily within vesicles called symbiosomes that are inside specialized cells called bacteriocytes. These endosymbionts are maternally transmitted. When the aphid reproduces, bacteriocytes migrate to the embryo and enter it. So during a parthenogenetic generation--not only are mother and daughter aphids genetically the same but also their endosymbionts. But is this the only way an endosymbiont can be transferred from host to host?
Moran and Dunbar in a recent paper in PNAS wondered about this very question: there must be another mechanism for endosymbiont transfer. Observations from the field indicate that horizontal transfer of endosymbionts--that is, the transfer of endosymbionts between different maternal lines--was fairly frequent. But aside from artificial transfers like microinjecting an uninfected aphid with the hemolymph from an infected one or feeding aphids an artificial diet composed of symbionts--there was no known natural way known for this type of endosymbionts transfer.
One possibility for horizontal transfer is during the autumn when the aphids are sexually reproducing. Moran and Dunbar hypothesized that endosymbionts might be transferred at the same time as sperm and other proteins during mating. To test this, they used the pea aphid, Acyrthosiphon pisum. In addition to Buchnera, the pea aphid can also be infected with a secondary endosymbiont which can be any number of three kinds of enterobacteria--Hamiltonella defensa, Serratia symbiotica, or Regiella insecticola. The researchers conducted aphid crosses by mating uninfected mothers with fathers infected with one of these secondary endosymbionts. In the case of R. insecticola, after monitoring the progeny for several generations, aphids in later generations still retained the paternally acquired endosymbiont. Using fluorescent in situ hybridization, the researchers were also able to locate these endosymbionts inside the male reproductive organs but not inside the sperm cells themselves.
So what possible benefit could the host aphid have for acquiring endosymbionts via horizontal transfer? One possibility is that the symbionts confer some survival advantages for the aphid--such as resistance to environmental stresses or to aphid pathogens. And what of the endosymbionts themselves? What do they get out of this transfer other than hopping from host to host? Well, there's one major implication in symbiont evolution, especially considering a situation involving coinfection. Symbionts can replicate themselves with genetic fidelity via host parthenogenesis, but when a different strain is introduced through host sexual reproduction, symbionts have the opportunity to swap genes, compete with each other for a favored niche, and influence the life cycle of their hosts.
