Abstract The mechanisms underlying within-host diversification in parasite populations are still poorly understood. Yet, diversification in parasite phenotype and genotype may have important clinical and epidemiological consequences. Our aim was to determine if the constraints associated with the infection of different host tissues lead to the emergence and co-existence of multiple parasite sub-populations with different phenotypes. We tested this hypothesis by injecting the most widespread bacterial endosymbiont, Wolbachia , isolated from three tissues of the common pill-bug Armadillidium vulgare into uninfected individuals, and by monitoring the growth rate and virulence of each bacterial sub-population in the new hosts. Our results highlighted that within-host environmental heterogeneity led to diverse phenotypes in Wolbachia . This variability did not appear to result from genomic variation, but from phenotypic plasticity. Indeed, we did not find recurrent tissue-specific genomic variation among infected individuals. Whole genome resequencing of the Wolbachia sub-populations and pedigree data from the animals used in this study demonstrated however the coexistence of two Wolbachia variants within our host lineage for almost 20 years. Our results further supported the stability of the Wolbachia genome with respect to small-scale genomic variation, in agreement with reports on other symbiotic systems.

Within-host environmental heterogeneity is associated with phenotypic but not genomic diversity in Wolbachia endosymbionts