Phylogenetic evidence for the invasion of a commercialized European Phasmarhabditis hermaphrodita lineage into North America and New Zealand.

Dana K Howe,Zhongying Zhao,Robbie G Rae,Dee R Denver,Michael Wilson,Jiří Nermut,Jenna Ross,Rory J Mc Donnell,Anh D Ha,Andrew Colton,Irma Tandingan De Ley

doi:10.1371/journal.pone.0237249

Abstract

Biological control (biocontrol) as a component of pest management strategies reduces reliance on synthetic chemicals, and seemingly offers a natural approach that minimizes environmental impact. However, introducing a new organism to new environments as a classical biocontrol agent can have broad and unanticipated biodiversity effects and conservation consequences. Nematodes are currently used in a variety of commercial biocontrol applications, including the use of Phasmarhabditis hermaphrodita as an agent targeting pest slug and snail species. This species was originally discovered in Germany, and is generally thought to have European origins. P. hermaphrodita is sold under the trade name Nemaslug®, and is available only in European markets. However, this nematode species was discovered in New Zealand and the western United States, though its specific origins remained unclear. In this study, we analyzed 45 nematode strains representing eight different Phasmarhabditis species, collected from nine countries around the world. A segment of nematode mitochondrial DNA (mtDNA) was sequenced and subjected to phylogenetic analyses. Our mtDNA phylogenies were overall consistent with previous analyses based on nuclear ribosomal RNA (rRNA) loci. The recently discovered P. hermaphrodita strains in New Zealand and the United States had mtDNA haplotypes nearly identical to that of Nemaslug®, and these were placed together in an intraspecific monophyletic clade with high support in maximum likelihood and Bayesian analyses. We also examined bacteria that co-cultured with the nematode strains isolated in Oregon, USA, by analyzing 16S rRNA sequences. Eight different bacterial genera were found to associate with these nematodes, though Moraxella osloensis, the bacteria species used in the Nemaslug® formulation, was not detected. This study provided evidence that nematodes deriving from the Nemaslug® biocontrol product have invaded countries where its use is prohibited by regulatory agencies and not commercially available.

Highlights

Biological control, ‘biocontrol’, is a human-mediated strategy used to suppress populations of pests and other undesirable species that involves the active deployment or conservation of natural enemies of the target species
Our study demonstrated that mitochondrial DNA (mtDNA) is a powerful tool for investigating within- and between-species evolutionary patterns in this nematode group, found variable bacteria associated with the three different P. hermaphrodita isolates from Oregon, and revealed strong evidence that recently discovered P. hermaphrodita isolates from California, Oregon, and New Zealand all likely derived from Nemaslug1
The phylogenetic analyses presented in this study revealed strong support for two major intraspecific mtDNA clades of P. hermaphrodita (Figs 1, 2)

Summary

Introduction

Biological control, ‘biocontrol’, is a human-mediated strategy used to suppress populations of pests and other undesirable species that involves the active deployment or conservation of natural enemies of the target species. The predatory snail Euglandina rosea has been introduced to Pacific and Indian Ocean islands for the purpose of controling giant African land snails (Lissachatina fulica), but has turned out to be ineffective against the target invasive species and damaging to island-endemic gastropods instead [8]. These classic ‘biocontrol gone awry’ and similar stories have motivated the development of rigorous regulatory policies surrounding efforts to develop new biocontrol initiatives, requiring careful environmental impact analyses and other forms of scientific scrutiny prior to biocontrol agent deployment [9,10,11,12]

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Results

Conclusion