Facultative or "secondary" symbionts are common in eukaryotes, particularly insects. While not essential for host survival, they often provide significant fitness benefits. It has been hypothesized that secondary symbionts form a "horizontal gene pool" shuttling adaptive genes among host lineages in an analogous manner to plasmids and other mobile genetic elements in bacteria. However, we do not know whether the distributions of symbionts across host populations reflect random acquisitions followed by vertical inheritance or whether the associations have occurred repeatedly in a manner consistent with a dynamic horizontal gene pool. Here we explore these questions using the phylogenetic and ecological distributions of secondary symbionts carried by 1,104 pea aphids, Acyrthosiphon pisum. We find that not only is horizontal transfer common, but it is also associated with aphid lineages colonizing new ecological niches, including novel plant species and climatic regions. Moreover, aphids that share the same ecologies worldwide have independently acquired related symbiont genotypes, suggesting significant involvement of symbionts in their host's adaptation to different niches. We conclude that the secondary symbiont community forms a horizontal gene pool that influences the adaptation and distribution of their insect hosts. These findings highlight the importance of symbiotic microorganisms in the radiation of eukaryotes.

Organisms across the tree of life form symbiotic partnerships with microbes for metabolism, protection and resources. While some hosts evolve extreme dependence on their symbionts, others maintain facultative associations. Explaining this variation is fundamental to understanding when symbiosis can lead to new higher-level individuals, such as during the evolution of the eukaryotic cell. Here we perform phylogenetic comparative analyses on 106 unique host–bacterial symbioses to test for correlations between symbiont function, transmission mode, genome size and host dependence. We find that both transmission mode and symbiont function are correlated with host dependence, with reductions in host fitness being greatest when nutrient-provisioning, vertically transmitted symbionts are removed. We also find a negative correlation between host dependence and symbiont genome size in vertically, but not horizontally, transmitted symbionts. These results suggest that both function and population structure are important in driving irreversible dependence between hosts and symbionts.

Bacterial symbiosis has played a fundamental role in the evolution of eukaryotes. However, we still know little about how cooperative relationships with bacteria originate, and why they form in some host species but not others. Facultative symbionts that are beneficial, but not essential, provide unique insights into these processes. We use data from over a hundred aphid species to test if host life history is associated with the presence of facultative symbionts. We find that aphid species that have mutualistic associations with ants that protect them from natural enemies are less likely to carry symbionts that provide similar benefits. We also find one symbiont species occurs more frequently in unrelated aphid species that specialise on certain plant genera. In addition, aphid species that attack multiple plants often carry different symbiont complements. Our findings provide evidence of the ecological conditions that facilitate stable, mutually beneficial relationships between microbes and eukaryotic hosts.

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The diversity of parasitic insects remains one of the most conspicuous patterns on the planet. The principal factor thought to contribute to differentiation of populations and ultimately speciation is the intimate relationship parasites share with hosts and the potential for disruptive selection associated with using different host species. Traits that generate this diversity have been an intensely debated topic of central importance to the evolution of specialization and maintenance of ecological diversity. A fundamental hypothesis surrounding the evolution of specialization is that no single genotype is uniformly superior in all environments. This "trade-off" hypothesis suggests that negative fitness correlations can lead to specialization on different hosts as alternative stable strategies. In this study we demonstrate a trade-off in the ability of the parasitoid, Aphidius ervi, to maintain a high level of fitness on an ancestral and novel host, which suggests a genetic basis for host utilization that may limit host-range expansion in parasitoids. Furthermore, behavioral evidence suggests mechanisms that could promote specialization through induced host fidelity. Results are discussed in the context of host-affiliated ecological selection as a potential source driving diversification in parasitoid communities and the influence of host species heterogeneity on population differentiation and local adaptation.