Abstract

The Old World bollworm Helicoverpa armigera is now established in Brazil but efforts to identify incursion origin(s) and pathway(s) have met with limited success due to the patchiness of available data. Using international agricultural/horticultural commodity trade data and mitochondrial DNA (mtDNA) cytochrome oxidase I (COI) and cytochrome b (Cyt b) gene markers, we inferred the origins and incursion pathways into Brazil. We detected 20 mtDNA haplotypes from six Brazilian states, eight of which were new to our 97 global COI-Cyt b haplotype database. Direct sequence matches indicated five Brazilian haplotypes had Asian, African, and European origins. We identified 45 parsimoniously informative sites and multiple substitutions per site within the concatenated (945 bp) nucleotide dataset, implying that probabilistic phylogenetic analysis methods are needed. High diversity and signatures of uniquely shared haplotypes with diverse localities combined with the trade data suggested multiple incursions and introduction origins in Brazil. Increasing agricultural/horticultural trade activities between the Old and New Worlds represents a significant biosecurity risk factor. Identifying pest origins will enable resistance profiling that reflects countries of origin to be included when developing a resistance management strategy, while identifying incursion pathways will improve biosecurity protocols and risk analysis at biosecurity hotspots including national ports.

Highlights

  • When ascertaining the order of events that led to the incursion of a pest or pathogen, understanding the roles of propagule pressure and geographical origins is very important, especially in revealing likely incursion pathways

  • By combining multiple mitochondrial DNA (mtDNA) markers and increasing global sampling sites, we identified Asia (i.e., China, India), Africa (i.e., Madagascar, Senegal) and Europe (i.e., France) as potential origins of Brazilian H. armigera, and inferred incursion pathways by combining genetic and trade data

  • This approach may be relevant to other invasive organisms with high effective population sizes, such as the soybean stem fly (SSF) Melanagromyza sojae[53], the whitefly Bemisia tabaci cryptic species complex (e.g.54), the spotted-wing vinegar fruit fly Drosophila suzukii[55], the European Grapevine moth Lobesia botrana[56,57], and the Russian Wheat Aphid Diuraphis noxia and incorporating genetic signatures of endosymbiont bacteria (e.g.58), amongst other

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Summary

Introduction

When ascertaining the order of events that led to the incursion of a pest or pathogen, understanding the roles of propagule pressure and geographical origins is very important, especially in revealing likely incursion pathways. Commodities are likely to increase in frequency due to globalisation and increased transport networks[1] This highlights the importance of differentiating trade-related ‘unintended’ incursions from malicious introductions of pest species (sometimes described as agricultural bioterrorism). Accurate assessments that differentiate between natural and/or accidental introduction of pests and pathogens from that of malicious introductions will require analyses of international trade routes and activities, and a sound scientific knowledge of pests, including their invasive biology and evolutionary genetics. The genetic diversity of a recently invaded pest species offers clues to the number of founder lineages (e.g.5–7), and incorporating information from other parts of its geographical range will allow more accurate inference of origins and incursion pathways (e.g.6,8–10). Economic losses in Brazil from this pest incursion have been estimated at US dollars (USD$) 2 billion for 2012 to 201436

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