Search for source of invasive-range populations of a haplodiploid pest species reveals Wolbachia-driven mitochondrial selective sweep in native range

The phylogeography of invasive pests is fundamentally important for the reconstruction of invasion pathways. Infection patterns with maternally inherited endosymbionts such as Cardinium and Wolbachia may provide additional resolution power. Kelly's citrus thrips, Pezothrips kellyanus, a significant Australian-native pest of citrus, has independently colonised New Zealand and the Mediterranean region. However, the Australian source populations for these two invasive ranges are unknown. Furthermore, Australian populations have previously been found with Cardinium and Wolbachia coinfections. Surprisingly, invasive-range populations only had Cardinium but not Wolbachia, although both endosymbionts independently cause cytoplasmic incompatibility that facilitates the endosymbionts' spread in host populations. To resolve this puzzle, we examined mitochondrial diversity and endosymbiont prevalence in 59 P. kellyanus populations across the native and invasive ranges. We found that populations from Victoria in Australia were Wolbachia-free and shared mitochondrial haplotypes with invasive-range populations, suggesting they were the likely source of the founder populations in both invasive ranges. However, we also detected a linkage pattern between Wolbachia and particular haplotypes in Australia. Furthermore, populations with a high Wolbachia prevalence in eastern Australia had a substantially lower haplotype diversity than populations with low Wolbachia prevalence in other parts of Australia. This indicates a Wolbachia-driven selective sweep of mitochondria in the native range of this haplodiploid host due to maternal coinheritance. In contrast, Cardinium was associated with all haplotypes, demonstrating an older association with Cardinium than Wolbachia. Overall, while endosymbionts are informative for tracing pest invasions, the selective sweeps they cause can potentially confound phylogeographic patterns and invasion pathways.

Automated summary

The presence of maternally inherited endosymbionts in invasive pests can affect the phylogeographic patterns and invasion pathways. The study of mitochondrial diversity and endosymbiont prevalence in populations of Kelly's citrus thrips revealed that populations from Victoria in Australia were likely the source of invasive populations in both New Zealand and the Mediterranean region. Surprisingly, invasive populations lacked one of the endosymbionts, Wolbachia, despite its association with cytoplasmic incompatibility. The study also found a linkage pattern between Wolbachia and specific mitochondrial haplotypes in Australian populations. This study highlights the importance of considering endosymbionts in tracing pest invasions, but also warns about the potential confounding effects of endosymbiont-driven selective sweeps on phylogeographic patterns.