Decoupling of Host–Symbiont–Phage Coadaptations Following Transfer Between Insect Species

Abstract

Transferring endosymbiotic bacteria between different host species can perturb the coordinated regulation of the host and bacterial genomes. Here we use the most common maternally transmitted bacteria, Wolbachia pipientis, to test the consequences of host genetic background on infection densities and the processes underlying those changes in the parasitoid wasp genus Nasonia. Introgressing the genome of Nasonia giraulti into the infected cytoplasm of N. vitripennis causes a two-order-of-magnitude increase in bacterial loads in adults and a proliferation of the infection to somatic tissues. The host effect on W. pipientis distribution and densities is associated with a twofold decrease in densities of the temperate phage WO-B. Returning the bacteria from the new host species back to the resident host species restores the bacteria and phage to their native densities. To our knowledge, this is the first study to report a hostmicrobe genetic interaction that affects the densities of both W. pipientis and bacteriophage WO-B. The consequences of the increased bacterial density include a reduction in fecundity, an increase in levels of cytoplasmic incompatibility (CI), and unexpectedly, male-to-female transfer of the bacteria to uninfected females and an increased acceptance of densely infected females to interspecific mates. While paternal inheritance of the W. pipientis was not observed, the high incidence of male-to-female transfer in the introgressed background raises the possibility that paternal transmission could be more likely in hybrids where paternal leakage of other cytoplasmic elements is also known to occur. Taken together, these results establish a major change in W. pipientis densities and tissue tropism between closely related species and support a model in which phage WO, Wolbachia, and arthropods form a tripartite symbiotic association in which all three are integral to understanding the biology of this widespread endosymbiosis.

Global Wolbachia prevalence, titer fluctuations and their potential of causing cytoplasmic incompatibilities in tsetse flies and hybrids of Glossina morsitans subgroup species

“…In the D. paulistorum species complex, backgrounds from inter-semispecies hybrids negatively influence host fitness by boosting Wolbachia -titer (Miller et al, 2010). Furthermore a twofold titer increase of native Wolbachia was reported recently in the F1 hybrids between closely related parasitoid wasps of the genus Nasonia (Chafee et al, 2011). Here we generated hybrids between members of the Glossina morsitans group and assessed their Wolbachia -infection titer in comparison to the corresponding parental generation.…”

“…In the species cluster D. paulistorum , hybrid backgrounds negatively influence host fitness by a massive increase of Wolbachia -infection (Miller et al, 2010). Another recent study demonstrated a twofold titer increase of native Wolbachia accompanied by proliferation into somatic host tissue in hybrids between closely related parasitoid wasps of the genus Nasonia (Chafee et al, 2011). In addition, Login et al (2011) have recently shown that in a beetle host from the genus Sitophilus the load of its primary endosymbiont SPE is strictly regulated by the expression of the host antimicrobial peptide Coleoptericin-A (ColA).…”

Temperature Affects the Tripartite Interactions between Bacteriophage WO, Wolbachia, and Cytoplasmic Incompatibility

“…Unidirectional incompatibility in N. vitripennis is strongly influenced by the density of Wolbachia in the male relative to that of the female and has been confirmed by multiple reports involving the same strains utilized in these experiments [8], [23]. Since temperature exposure affects Wolbachia densities in all cold treatments and in the egg heat treatment, we further explored this relationship by comparing the density of Wolbachia required to induce CI at different treatment stages relative to the control 25 C temperature.…”

The complexity of virus systems: the case of endosymbionts

“…Interestingly, altering Wolbachia environmental factors does not abolish this three-way interaction. Introgression to move the w VitA strain from its native host into a related species of wasp, N. giraulti increased Wolbachia load, decreased WO densities, and increased CI [41], while rearing insects at temperature extremes had the opposite effect [42]. In w Pip-infected Culex pipiens mosquitoes under conditions where WO is not lytic, this correlation is not seen [43].…”