‘Drifting’Buchneragenomes track the microevolutionary trajectories of their aphid hosts

Abstract

Coevolution ofBuchnera–aphid host symbioses is often studied among species at the macroevolutionary scale. Investigations within species offer a different perspective about how eco-evolutionary processes shape patterns of genetic variation at the microevolutionary scale. Our study leverages new and publicly available whole-genome sequencing data to studyBuchnera–aphid host coevolution inMyzus persicae, the peach potato aphid, a globally invasive and polyphagous pest. Across 43 different aphid clonal lineages, we examined patterns of genomic covariation betweenBuchneraand their aphid host, and considered the distribution of mutations in protein-coding regions of theBuchneragenome. We foundBuchnerapolymorphism within aphid clones, suggesting that aphids harbour populations of differentBuchnerastrains. Genetic distance between pairs ofBuchnerasamples was positively correlated to genetic distance between their hosts, indicating shared evolutionary histories. However, there was no segregation in the genetic variation of bothM. persicaeandBuchnerawith plant host (Brassicaceae and non-tobacco Solanaceae) and there was also no isolation-by-distance within both organisms at global or regional spatial scales. Abundance patterns of non-synonymous mutations were similar to synonymous mutations, and both mutation classes had similar site frequency spectra. We hypothesize that a predominance of neutral processes results in theBuchneraofM. persicaeto simply ‘drift’ with the evolutionary trajectory of their aphid hosts. Our study presents a unique microevolutionary characterisation ofBuchnera–aphid host genomic covariation across multiple aphid clones. This provides a new perspective on the eco-evolutionary processes generating and maintaining polymorphisms in an aphid species and its obligate endosymbiont.

Ecological drift during colonization drives within-host and between-host heterogeneity in an animal-associated symbiont

“…Although we implemented our experiments using horizontal transmission, many symbioses exhibit elaborate, host-controlled mechanisms that ensure vertical transmission [ 51 – 55 ]. Despite host control, vertically transmitted symbionts, including obligate insect mutualists [ 56 ], are not immune to the effects of ecological drift, which acts on communities regardless of how they disperse. Indeed, some vertically transmitted symbionts undergo extreme transmission bottlenecks [ 57 – 59 ], exaggerating the intensity of drift, and vertically transmitted symbionts also compete for host colonization [ 59 – 62 ].…”