The pea aphid, Acyrthosiphon pisum, shows significant reproductive isolation and host plant specialization between populations on alfalfa and clover in New York. We examine whether specialization is seen in pea aphids in California, and whether fitness on alternative host plants is associated with the presence of bacterial symbionts. We measured the fitness of alfalfa-and clover-derived aphids on both types of plants and found no evidence for specialization when all aphid lineages were considered simultaneously. We then screened all aphids for the presence of four facultative bacterial symbionts: PAR, PASS, PABS and PAUS. Aphids with PAUS were host-plant specialized, having twice as many offspring as other aphids on clover, and dying on alfalfa. Other aphids showed no evidence of specialization. Additionally, aphids with PABS had 50% more offspring than aphids with PASS when on alfalfa. Thus, specialist and generalist aphid lineages coexist, and specialization is symbiont associated. Further work will resolve whether PAUS is directly responsible for this variation in fitness or whether PAUS is incidentally associated with host-plant specialized aphid lineages.

Aphids are sap-feeding insects that host a range of bacterial endosymbionts including the obligate, nutritional mutualist Buchnera plus several bacteria that are not required for host survival. Among the latter, ‘Candidatus Regiella insecticola’ and ‘Candidatus Hamiltonella defensa’ are found in pea aphids and other hosts and have been shown to protect aphids from natural enemies. We have sequenced almost the entire genome of R. insecticola (2.07 Mbp) and compared it with the recently published genome of H. defensa (2.11 Mbp). Despite being sister species the two genomes are highly rearranged and the genomes only have ∼55% of genes in common. The functions encoded by the shared genes imply that the bacteria have similar metabolic capabilities, including only two essential amino acid biosynthetic pathways and active uptake mechanisms for the remaining eight, and similar capacities for host cell toxicity and invasion (type 3 secretion systems and RTX toxins). These observations, combined with high sequence divergence of orthologues, strongly suggest an ancient divergence after establishment of a symbiotic lifestyle. The divergence in gene sets and in genome architecture implies a history of rampant recombination and gene inactivation and the ongoing integration of mobile DNA (insertion sequence elements, prophage and plasmids).

The evolution of herbivore-host plant specialization requires low levels of gene flow between populations on alternate plant species. Accordingly, selection for host plant specialization is most effective when genotypes have minimal exposure to, and few mating opportunities with individuals from, alternate habitats. Maternally transmitted bacterial symbionts are common in insect herbivores and can influence host fecundity under a variety of conditions. Symbiont-mediated effects on host life-history strategies, however, are largely unknown. Here, we show that the facultative bacterial symbiont Candidatus Regiella insecticola strikingly alters both dispersal and mating in the pea aphid, Acyrthosiphon pisum. Pea aphids containing Regiella produced only half the number of winged offspring in response to crowding and, for two out of three aphid lineages, altered the timing of sexual reproduction in response to conditions mimicking seasonal changes, than did aphids lacking Regiella. These symbiont-associated changes in dispersal and mating are likely to have played a key role in the initiation of genetic differentiation and in the evolution of pea aphid-host plant specialization. As symbionts are widespread in insects, symbiont-induced life history changes may have promoted specialization, and potentially speciation, in many organisms.

Symbioses are ubiquitous in nature. However, these interactions, in particular those which are facultative from the perspective of the host, are still poorly understood. One major question is whether facultative symbionts affect host fitness, and in particular whether they can benefit the host. In pea aphid, host plant specialization was found to be associated with the presence of Pea Aphid U-type Symbiont [Proc. R. Soc. Lond. B 270 (2003) S209]. Host and symbiont genomes are normally co-transmitted, making it difficult to determine which is responsible for causing this variation in fitness. Here antibiotic treatment is used to selectively remove the symbiont, thus partitioning symbiont and host genomes. I find that PAUS is not responsible for causing host plant specialization. Examination of aphids in which PAUS presence has been naturally manipulated also supports this conclusion. Additional work will be necessary to determine the forces maintaining this symbiont in host populations, and whether it benefits the host insect under different conditions.

Transposable elements (TEs) are genomic parasites that amplify their own representation on hosts' chromosomes by inserting into new positions. It is traditionally thought that their copy number is regulated by purifying selection that eliminates hosts with higher than average TE abundance. Here, we stress that selection due to beneficial or harmful interactions between TEs introduces a whole new dimension, with implications for TE evolutionary trajectories and TE loads on hosts. This framework poses new questions requiring conceptual and experimental advances. Considering primarily Drosophila data, we make a case for within host selection on TEs by thinking expansively about the lifecycle of several TE families.