Tracking genetic invasions: Genome‐wide single nucleotide polymorphisms reveal the source of pyrethroid‐resistant Aedes aegypti (yellow fever mosquito) incursions at international ports

Abstract

Biological invasions are increasing globally in number and extent despite efforts to restrict their spread. Knowledge of incursion pathways is necessary to prevent new invasions and to design effective biosecurity protocols at source and recipient locations. This study uses genome‐wide single nucleotide polymorphisms (SNPs) to determine the origin of 115 incursive Aedes aegypti(yellow fever mosquito) detected at international ports in Australia and New Zealand. We also genotyped mosquitoes at three point mutations in the voltage‐sensitive sodium channel (Vssc) gene: V1016G, F1534C and S989P. These mutations confer knockdown resistance to synthetic pyrethroid insecticides, widely used for controlling invertebrate pests. We first delineated reference populations using Ae. aegypti sampled from 15 locations in Asia, South America, Australia and the Pacific Islands. Incursives were assigned to these populations using discriminant analysis of principal components (DAPC) and an assignment test with a support vector machine predictive model. Bali, Indonesia, was the most common origin of Ae. aegypti detected in Australia, while Ae. aegypti detected in New Zealand originated from Pacific Islands such as Fiji. Most incursives had the same allelic genotype across the three Vsscgene point mutations, which confers strong resistance to synthetic pyrethroids, the only insecticide class used in current, widely implemented aircraft disinsection protocols endorsed by the World Health Organization (WHO). Additionally, all internationally assigned Ae. aegypti had Vssc point mutations linked to pyrethroid resistance that are not found in Australian populations. These findings demonstrate that protocols for preventing introductions of invertebrates must consider insecticide resistance, and highlight the usefulness of genomic data sets for managing global biosecurity objectives.

Population genomics of two invasive mosquitoes (Aedes aegyptiandAedes albopictus) from the Indo-Pacific

“…described here has implications for biosecurity and biocontrol. Recently, genomics has been used to identify source locations of Aedes incursions into Australia and New Zealand [19] (Schmidt et al 2020: submitted), which threaten not only the arrival of species themselves but also the introduction of insecticide resistance alleles (Endersby et al 2020: in press). The genomic patterns identified here can help in identifying biosecurity threats from both species.…”

“…Mosquitoes were genotyped using a pipeline that has been described elsewhere [19] and is described here in detail in S1 Appendix. Briefly, we used the double-digest restriction site-associated (ddRAD) sequencing protocol for Ae.…”

“…to disperse and to invade new regions. The findings of this study will assist biosecurity operations that aim to trace the source of invasive material [19,46] and for biocontrol operations that benefit from matching genetic backgrounds of released and local populations [47]. White lines indicate density of shipping routes.…”

“…has been observed directly [14] or inferred from the spatial distribution of close kin [15,16]. Dispersal at broader scales such as between cities is almost exclusively by passive transportation on ships, aircraft and land vehicles [17][18][19][20].…”

“…populations can spread advantageous alleles that reduce the efficacy of local control programs (Endersby et al 2020: in press). Incursions of these species are frequently found on vessels such as ships and planes [18,19] (Schmidt et al 2020: submitted), and when source locations can be identified they are often far from the point of collection [19] (Schmidt et al 2020: submitted).…”