Factors driving Wolbachia prevalence in native and invasive populations of Drosophila suzukii

Understanding the factors that drive the prevalence of endosymbionts in natural populations is a central goal of evolutionary ecology. The success of maternally transmitted symbionts can be explained by three parameters: reproductive manipulations of the host, vertical transmission rates and effects on host fitness. Those parameters can be modulated by both environmental and genetic factors. The Wolbachia strain wSuz, which infects the invasive pest species Drosophila suzukii, is a canonical example of maternally transmitted symbiont with low to intermediate prevalence in host populations and weak reproductive manipulation. For Wolbachia strains with such properties, the mechanisms inherent to the infection dynamics remain poorly understood. We investigated infection frequencies and wSuz intra-strain polymorphism in 24 natural populations of D. suzukii from both native (China and Japan) and invasive areas (Europe and America). Infection frequencies in populations from China were on average significantly higher than those in populations from invasive areas. Based on the study of an insertion sequence site and a genomic rearrangement polymorphism in wSuz genome, we could identify three wSuz variants (i.e. European, American and Asian) corresponding to the initial sample location. More in-depth investigations indicated that the European variant was also present in some Asian populations and that one population from Europe included the European and American variants. Additional analyses based on whole-genome sequencing of 70 D. suzukii population samples showed lower Wolbachia genomic diversity in invasive populations (America and Europe) than in native (Japan, Korea and China) populations, consistent with a bottleneck in invasive populations. Finally, we analyzed two types of factors that could affect Wolbachia infection frequencies in natural populations: climatic variation and Wolbachia-induced cytoplasmic incompatibility. We found that variations in the strength of cytoplasmic incompatibilities or in monthly temperatures were not sufficient to fully explain observed prevalence pattern. Overall, our results show that, despite reduced intra-strain genomic diversity, both population prevalence and phenotypic effects on host reproduction can vary greatly among Wolbachia variants, suggesting complex interactions with host genetic background and environmental factors