Bridgehead Effect in the Worldwide Invasion of the Biocontrol Harlequin Ladybird

Eric Lombaert,Jean-Marie Cornuet,Benoît Facon,Thomas Guillemaud,Arnaud Estoup,Thibaut Malausa,Jerome Chave

doi:10.1371/journal.pone.0009743

Abstract

Recent studies of the routes of worldwide introductions of alien organisms suggest that many widespread invasions could have stemmed not from the native range, but from a particularly successful invasive population, which serves as the source of colonists for remote new territories. We call here this phenomenon the invasive bridgehead effect. Evaluating the likelihood of such a scenario is heuristically challenging. We solved this problem by using approximate Bayesian computation methods to quantitatively compare complex invasion scenarios based on the analysis of population genetics (microsatellite variation) and historical (first observation dates) data. We applied this approach to the Harlequin ladybird Harmonia axyridis (HA), a coccinellid native to Asia that was repeatedly introduced as a biocontrol agent without becoming established for decades. We show that the recent burst of worldwide invasions of HA followed a bridgehead scenario, in which an invasive population in eastern North America acted as the source of the colonists that invaded the European, South American and African continents, with some admixture with a biocontrol strain in Europe. This demonstration of a mechanism of invasion via a bridgehead has important implications both for invasion theory (i.e., a single evolutionary shift in the bridgehead population versus multiple changes in case of introduced populations becoming invasive independently) and for ongoing efforts to manage invasions by alien organisms (i.e., heightened vigilance against invasive bridgeheads).

Highlights

Elucidating the routes and modalities of introductions of undesirable organisms is crucial for managers who wish to prevent new invasions. [1,2]
In the large body of literature on biological invasions, a number of studies suggest that successful invasions involve a particular invasive population, which serves as the source of colonists for remote new territories [4,5,6,7,8]
The European outbreak originated from eastern North America, but with substantial genetic admixture with individuals of the European biocontrol strain

Summary

Introduction

Elucidating the routes and modalities of introductions of undesirable organisms is crucial for managers who wish to prevent new invasions. [1,2]. Using molecular and historical data, this method allows performing model-based inference in a Bayesian setting for complex demographic or evolutionary scenarios such as those related to the introduction histories of invasive species, where bottleneck, multiple introductions and/or genetic admixture events are often suspected.

Results

Conclusion