title: Horizontally transmitted symbionts and host colonization of ecological niches.
abstract: 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.
authors.affiliation: Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK. Electronic address: leehenrym@gmail.com.
authors.forename: Lee M
authors.initials: LM
authors.lastname: Henry
authors.forename: Jean
authors.initials: J
authors.lastname: Peccoud
authors.forename: Jean-Christophe
authors.initials: JC
authors.lastname: Simon
authors.forename: Jarrod D
authors.initials: JD
authors.lastname: Hadfield
authors.forename: Martin J C
authors.initials: MJ
authors.lastname: Maiden
authors.forename: Julia
authors.initials: J
authors.lastname: Ferrari
authors.forename: H Charles J
authors.initials: HC
authors.lastname: Godfray
mesh_terms: D017753:Ecosystem; D022761:Gene Transfer, Horizontal; D008969:Molecular Sequence Data; D010802:Phylogeny; D013559:Symbiosis