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.

Evidence for specificity in symbiont-conferred protection against parasitoids

“…Analysis of the sequence data for the H. defensa hrpA and murE genes confirm that clones collected from the different host plants have genotypes characteristic of the H. defensa strains previously associated with these plants [41]. There were two different H. defensa types associated with Medicago, one of which is extremely similar to the single H. defensa clade associated with Lotus; there was also a single H. defensa clade associated with Ononis (see electronic supplementary material, figure S1).…”

“…In each case, a single adult individual was used to establish a line of aphids that were subsequently maintained in laboratory culture on broad bean (Vicia faba). Diagnostic PCR was used to confirm that each clone carried the symbiont H. defensa and to find out whether any other known facultative symbionts of pea aphids were present, a procedure that was repeated immediately prior to our experiments (see Henry et al [41] for details of primers and PCR conditions used). Microsatellite typing was used to establish that the clones are distinct from one another and belong to biotypes known to be associated with the different plant species [39].…”

“…These genes were selected because previous studies have shown that they display greater between than within biotype variation [41]. Primers and PCR conditions are given in Henry et al [41]. In addition to the aphid clones used in the experiment, we also included seven additional samples to obtain a better understanding of genetic variation within biotypes (table 1).…”

“…Partial sequences from two housekeeping genes, murE and hrpA (855 bp and 812 bp, respectively), were used to compare the genetic distance between the H. defensa isolates from the experimental aphids. These genes were selected because previous studies have shown that they display greater between than within biotype variation [41]. Primers and PCR conditions are given in Henry et al [41].…”

Whole-genome re-sequencing of non-model organisms: lessons from unmapped reads

“…In addition, the pea aphid is associated with an obligatory endosymbiont, Buchnera aphidicola, which is found in specialized cells called bacteriocytes and provides its host with essential amino acids. The pea aphid also harbors several facultative symbionts whose distribution is strongly correlated with plant specialization of their hosts (Simon et al, 2003;Ferrari et al, 2012;Henry et al, 2013), and it has been posited that some of these symbionts could have a role in plant adaptation, although clear evidence is still lacking (Tsuchida et al, 2004;McLean et al, 2011).…”