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

Abstract

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.