Patterns, causes and consequences of defensive microbiome dynamics across multiple scales

Abstract

The microbiome can significantly impact host phenotypes and serve as an additional source of heritable genetic variation. While patterns across eukaryotes are consistent with a role for symbiotic microbes in host macroevolution, few studies have examined symbiont-driven host evolution or the ecological implications of a dynamic microbiome across temporal, spatial or ecological scales. The pea aphid, Acyrthosiphon pisum, and its eight heritable bacterial endosymbionts have served as a model for studies on symbiosis and its potential contributions to host ecology and evolution. But we know little about the natural dynamics or ecological impacts of the heritable microbiome of this cosmopolitan insect pest. Here we report seasonal shifts in the frequencies of heritable defensive bacteria from natural pea aphid populations across two host races and geographic regions. Microbiome dynamics were consistent with symbiont responses to host-level selection and findings from one population suggested symbiont-driven adaptation to seasonally changing parasitoid pressures. Conversely, symbiont levels were negatively correlated with enemy-driven mortality when measured across host races, suggesting important ecological impacts of host race microbiome divergence. Rapid drops in symbiont frequencies following seasonal peaks suggest microbiome instability in several populations, with potentially large costs of 'superinfection' under certain environmental conditions. In summary, the realization of several laboratory-derived, a priori expectations suggests important natural impacts of defensive symbionts in host-enemy eco-evolutionary feedbacks. Yet negative findings and unanticipated correlations suggest complexities within this system may limit or obscure symbiont-driven contemporary evolution, a finding of broad significance given the widespread nature of defensive microbes across plants and animals.

Aphid Heritable Symbiont Exploits Defensive Mutualism

“…Alternative explanations for X-type maintenance include improved rates of vertical transmission in superinfections relative to single infections or frequent lateral transfer, but neither of these was supported in preliminary lab trials. While X-type appears to be an atypical case, superinfections are common in many insect species (8,10,52) and this hitchhiking strategy, or similar scenarios, may occur in other systems, even among conditional beneficial symbionts not under direct selection (e.g., coinfecting antifungal HFS spread with H. defensa under parasitism pressure [11]). Of course, confirming a purely exploitative hitchhiking status of symbionts will remain troublesome, due to the difficulty in "proving a negative," as there is always the possibility that the hitchhiker confers some unknown conditional benefit.…”

“…Moreover, individual hosts are often infected with multiple inherited symbionts and antagonistic or synergistic interactions between superinfecting symbionts may enhance or reduce mutualistic services or costs, influencing symbiont spread within the host population (8)(9)(10). Instances of heritable pathogens are expected to be exceedingly rare (1), yet under some conditions, a heritable symbiont that was neither providing conditional benefits nor manipulating host reproduction could spread by "hitchhiking" alongside a beneficial symbiont (11). A hitchhiking symbiont could be maintained in host populations even when superinfection causes harm to host fitness as long as the conditional benefits provided by the mutualist in the superinfection context outweigh these costs.…”

“…This common HFS often infects up to 40% of individuals in some North American populations (8,11). Sequences of the X-type 16S rRNA gene place this HFS in the Enterobacteriaceae (Gammaproteobacteria), along with other aphid symbionts, including Buchnera and H. defensa, as well as notable human pathogens, such as Salmonella (25).…”

Symbionts modify interactions between insects and natural enemies in the field

“…; Smith et al . ). For example, the symbiont Serratia symbiotica protects its host against heat shock and is found at highest frequency in hot environments (Montllor, Maxmen & Purcell ; Henry et al .…”

Heat Stress Affects Facultative Symbiont-Mediated Protection from a Parasitoid Wasp

“…Facultative symbiont coinfections are common in aphids and X-type is rarely found in single infections [30,31]. The presence of a second symbiont potentially changes the phenotypic effect seen in a single infection, possibly because two symbionts consume more resources [22].…”