Population structure and gene flow in the global pest, Helicoverpa armigera

Abstract

Helicoverpa armigera is a major agricultural pest that is distributed across Europe, Asia, Africa and Australasia. This species is hypothesized to have spread to the Americas 1.5 million years ago, founding a population that is at present, a distinct species, Helicoverpa zea. In 2013, H. armigera was confirmed to have re‐entered South America via Brazil and subsequently spread. The source of the recent incursion is unknown and population structure in H. armigera is poorly resolved, but a basic understanding would highlight potential biosecurity failures and determine the recent evolutionary history of region‐specific lineages. Here, we integrate several end points derived from high‐throughput sequencing to assess gene flow in H. armigera and H. zea from populations across six continents. We first assemble mitochondrial genomes to demonstrate the phylogenetic relationship of H. armigera with other Heliothine species and the lack of distinction between populations. We subsequently use de novo genotyping‐by‐sequencing and whole‐genome sequences aligned to bacterial artificial chromosomes, to assess levels of admixture. Primarily, we find that Brazilian H. armigera are derived from diverse source populations, with strong signals of gene flow from European populations, as well as prevalent signals of Asian and African ancestry. We also demonstrate a potential field‐caught hybrid between H. armigera and H. zea, and are able to provide genomic support for the presence of the H. armigera conferta subspecies in Australasia. While structure among the bulk of populations remains unresolved, we present distinctions that are pertinent to future investigations as well as to the biosecurity threat posed by H. armigera.

Mitochondrial DNA and trade data support multiple origins of Helicoverpa armigera (Lepidoptera, Noctuidae) in Brazil

“…Therefore, it is possible that these eight uniquely Brazilian haplotypes could have originated from these populations, and perhaps also populations in Uganda, Burkina Faso, and China (Suppl. Table 1), as supported also by genome-wide SNP data and pyrethroid resistance gene analysis52.…”

“…This is supported by Anderson et al 52. where Brazilian H. armigera grouped with Asian individuals for an allele for pyrethroid resistance in H. armigera sampled during this early stage of incursion.…”

Invasion origin, rapid population expansion, and the lack of genetic structure of cotton bollworm (Helicoverpa armigera) in the Americas

“…Common mtDNA haplotypes are shared among the Americas, Europe, Africa, and Asia, including the sharing of alleles associated with pyrethroid resistance (Durigan et al, ; Tay et al, ). Furthermore, H. armigera populations show weak genetic structure and high gene flow in the Old World and Australia (Anderson et al, ; Behere et al, ; Endersby, Hoffmann, McKechnie, & Weeks, ; Li et al, ; Nibouche, Bues, Toubon, & Poitout, ; Tay et al, ; Vijaykumar, Krishnareddy, Kuruvinashetti, & Patil, ; Weeks et al, ). The high diversity and weak genetic structure in the Old World make it difficult to describe with accuracy the geographical origin, routes, and the number of invasion events of H. armigera to Brazil.…”

“…The high diversity and weak genetic structure in the Old World make it difficult to describe with accuracy the geographical origin, routes, and the number of invasion events of H. armigera to Brazil. However, they also reduce the impact of this information because there is a wide transference of alleles among geographical sites in the Old World (Anderson et al, ; Behere et al, ; Nibouche et al, ; Rasool et al, ; Stokes, Mckechnie, & Forrester, ). Finally, there is consensus that the invasion of South America by H. armigera was not originated from Oceania (Anderson et al, ; Durigan et al, ; Tay et al, ).…”

“…Recent population studies revealed a high genetic diversity of H. armigera populations in Brazil and genetic similarity among Brazilian individuals with populations originating in Europe, Africa, and Asia (Anderson, Tay, McGaughran, Gordon, & Walsh, ; Leite, Alves‐Pereira, Corrêa, Zucchi, & Omoto, ; Mastrangelo et al, ; Tay et al, ). The high genetic diversity of H. armigera increases doubts surrounding an invasion process and population dynamics of H. armigera in Brazil, since high genetic diversity is not expected in invasive insects due to the founder effect of invasion processes.…”