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Multiple Transatlantic Introductions of the Western Corn Rootworm

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Science  11 Nov 2005:
Vol. 310, Issue 5750, pp. 992
DOI: 10.1126/science.1115871

Abstract

The invasion of Europe by the western corn rootworm, North America's most destructive corn pest, is ongoing and represents a serious threat to European agriculture. Because this pest was initially introduced in Central Europe, it was believed that subsequent outbreaks in Western Europe originated from this area. Using model-based Bayesian analyses of the genetic variability of the western corn rootworm, we demonstrate that this belief is false: There have been at least three independent introductions from North America during the past two decades. This result raises questions about changing circumstances that have enabled a sudden burst of transatlantic introductions.

Prevention of biological invasions, as opposed to remedial eradication of invasive species, represents the most cost-effective and perhaps only hope for stemming the current homogenization of the world's biota (1). Here we describe the introduction routes into Europe of the western corn rootworm (Diabrotica virgifera virgifera, WCR), the most destructive pest of corn in the United States. Armed with this knowledge, it will be possible to better gauge the prevention strategies that might be adopted.

WCR was first detected in Europe in the former Yugoslavia in 1992 and has since spread throughout much of central and southeastern (CSE) Europe (2). Outbreaks of WCR were subsequently detected in northeast Italy in 1998 (in Veneto), 2002 (in Pordenone), and 2003 (in Udine); in northwest Italy and Switzerland in 2000; near Paris, France, in 2002 and 2004; and in eastern France, Switzerland, Belgium, the United Kingdom, and the Netherlands in 2003 (2). Although the invasion history of WCR is well documented, the source populations of the Western European outbreaks remain unknown. Because of the sequence of outbreaks, CSE Europe was generally assumed to be the source of most, if not all, the Western European populations (3). However, in principle, each outbreak could have originated from North America, CSE Europe, or one of the other Western European foci.

To discriminate between these introduction scenarios, we analyzed the genetic variation of European and American WCR populations at eight microsatellite loci (4, 5). Simple genetic statistics gave useful but qualitative insights into the origin of most European outbreaks (5) (table S1). We then used a model-based approximate Bayesian computation (ABC) method relying on computer simulations (5, 6) to quantitatively compare the different introduction scenarios for the Western European WCR populations (Fig. 1).

Fig. 1.

The most likely scenarios of invasion into Europe by WCR, deduced from the ABC analysis. For each European outbreak, a red arrow indicates its most likely origin; the PW values of the introduction scenarios are in parentheses. Gray arrows represent unresolved scenarios. Large areas where WCR is present are shown in orange. BF values supporting the most likely scenarios of 3.2 to 10 (substantial support), 10 to 100 (strong support), and >100 (decisive support) are indicated by one, two, or three asterisks, respectively; ns, not supported.

Our results are clear-cut and unexpected. Two of the Western European populations analyzed did not originate from CSE Europe but directly from North America; this scenario was supported by Bayes factors (BF) higher than 105 and posterior weights (PW) of ∼1 for the northwestern Italy and Paris 2002 populations. Moreover, these introductions were independent from each other (BF ≥ 159 and PW ≥ 0.94). According to our analysis, the northeastern Italy 2003 outbreak was the only one to originate from CSE Europe (BF = 183 and PW = 0.94), and the eastern France population was derived from the Paris 2002 population (BF = 3.9 and PW = 0.45). The only population with ambiguous origins was Paris 2004, which could have been derived either from North America (BF = 2.05 and PW = 0.70) or from Paris 2002 (PW = 0.22). The presence of unsampled European populations acting as alternative introduction sources for the three primary outbreaks (CSE Europe, northwestern Italy, and Paris 2002) could be ruled out. This was true whether the unsampled population was one of those detected in 2003 (BF > 104 and PW ∼1) or a hypothetical population founded in the 1980s (BF > 3.6 and PW > 0.68).

It has been widely assumed that the European WCR invasion was the result of a single unpredictable introduction. Our finding that there have been at least three independent transatlantic introductions of WCR suggests that incursions from North America are chronic. Prevention of future WCR invasions will require action against multiple invasion routes, which have apparently been used repeatedly and are potentially predictable. Our study also raises questions concerning the changing circumstances (such as adaptation by the insect or changes in control measures or transportation practices) that have permitted a sudden and recent burst of transatlantic introductions of WCR.

Supporting Online Material

www.sciencemag.org/cgi/content/full/310/5750/992/DC1

Materials and Methods

Table S1

References and Notes

References and Notes

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