Multiple incursion pathways for Helicoverpa armigera in Brazil show its genetic diversity spreading in a connected world

Jonas Andre Arnemann,Karl Gordon,Tom Walsh,Wee Tek Tay,Jerson Guedes,Stephen Roxburgh,Guy Smagghe

doi:10.1038/s41598-019-55919-9

Abstract

The Old World cotton bollworm Helicoverpa armigera was first detected in Brazil with subsequent reports from Paraguay, Argentina, Bolivia, and Uruguay. This pattern suggests that the H. armigera spread across the South American continent following incursions into northern/central Brazil, however, this hypothesis has not been tested. Here we compare northern and central Brazilian H. armigera mtDNA COI haplotypes with those from southern Brazil, Uruguay, Argentina, and Paraguay. We infer spatial genetic and gene flow patterns of this dispersive pest in the agricultural landscape of South America. We show that the spatial distribution of H. armigera mtDNA haplotypes and its inferred gene flow patterns in the southwestern region of South America exhibited signatures inconsistent with a single incursion hypothesis. Simulations on spatial distribution patterns show that the detection of rare and/or the absence of dominant mtDNA haplotypes in southern H. armigera populations are inconsistent with genetic signatures observed in northern and central Brazil. Incursions of H. armigera into the New World are therefore likely to have involved independent events in northern/central Brazil, and southern Brazil/Uruguay-Argentina-Paraguay. This study demonstrates the significant biosecurity challenges facing the South American continent, and highlights alternate pathways for introductions of alien species into the New World.

Highlights

Biological invasions are major ecological phenomena that influence the worldwide distribution of species
We undertook the present study, in which we show that gene flow and spatial distribution patterns of H. armigera mtDNA haplotypes support multiple introductions of the H. armigera into South America, with the incursion(s) in the southern regions likely independent from the northern/central Brazilian incursions
All specimens from the southern/south-western regions of South America were successfully sequenced for the mtDNA COI fragment (GenBank accession numbers MG230495 -MG230526; KU255535-KU255543 from7) using the Noc-COI-F/R primer pairs

Summary

Introduction

Biological invasions are major ecological phenomena that influence the worldwide distribution of species. It is almost certain that H. armigera had been present in South America for a period of time [e.g22,32–34.] prior to its first identification in Brazil[21], remaining undetected due to its close morphology with the New World sister species H. zea, and the difficulty of detecting invasive pests at the early stages of incursions[35]. It is unknown whether the H. armigera populations detected across South America arose from a single, or multiple, original introductions, and where these were. We undertook the present study, in which we show that gene flow and spatial distribution patterns of H. armigera mtDNA haplotypes support multiple introductions of the H. armigera into South America, with the incursion(s) in the southern regions likely independent from the northern/central Brazilian incursions

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Results

Conclusion