Dual mitochondrial haplotypes and nuclear genotypes of solanum fruit fly Bactrocera latifrons (Diptera: tephritidae) from Ryukyu Islands indicate multiple origins and inter-strain breeding of the invasive species in Japan

Highly invasive fruit fly, Bactrocera latifrons (Hendel) is one of the most serious pests worldwide, which primarily utilizes Solanaceae fruit crops. The fly species was reported to have invaded Japan twice and their distinct host preferences suggest that the two populations may be different strains derived from remote geographic origins. In this study, we surveyed various populations of B. latifrons in Okinawa by sequencing multiple mitochondrial and nuclear loci, thereby extrapolating their invasion events and phylogenetic origins. We used live, dried or ethanol-fixed specimens of B. latifrons captured from 15 islands between 2004 and 2022. Haplotype network analyses of mitochondrial genes revealed two distinct haplotypes in Ryukyu islands and the phylogenetic analyses with those from other countries indicated that the haplotypes were clustered into two major clades. The most abundant haplotype found on Okinawa Island and many other islands was closely related to those from Malaysia, suggesting that it may have invaded from Southeast Asia. On the other hand, a minor haplotype consisted of older specimens exclusively from Yonaguni Island along with those from Taiwan. In addition, sequencing cry1 fragment of the nuclear gene uncovered distinct genotypes associated with the two haplotypes. The comparative analyses of both mitochondrial and nuclear genes further indicated crosses and introgression of the two strains on Yonaguni Island recently. Our study clearly demonstrates two distinct haplotypes/genotypes of B. latifrons with alternative host preferences have likely originated from independent invasion pathways, and therefore suggests that their genetic backgrounds should be carefully considered for customized pest control measures.