The alfalfa weevil Hypera postica, native to the Western Palearctic, is an invasive legume pest with two divergent mitochondrial clades in its invading regions, the Western clade and the Eastern/Egyptian clade. However, knowledge regarding the native populations is limited. The Western clade is infected with the endosymbiotic bacteria Wolbachia that cause cytoplasmic incompatibility in host weevils. Our aim was to elucidate the spatial genetic structure of this insect and the effect of Wolbachia on its population diversity. We analyzed two mitochondrial and two nuclear genes of the weevil from its native ranges. The Western clade was distributed in western/central Europe, whereas the Eastern/Egyptian clade was distributed from the Mediterranean basin to central Asia. Intermediate mitotypes were found from the Balkans to central Asia. Most Western clade individuals in western Europe were infected with an identical Wolbachia strain. Mitochondrial genetic diversity of the infected individuals was minimal. The infected clades demonstrated a higher nonsynonymous/synonymous substitution rate ratio than the uninfected clades, suggesting a higher fixation of nonsynonymous mutations due to a selective sweep by Wolbachia. Trans-Mediterranean and within-European dispersal routes were supported. We suggest that the ancestral populations diversified by geographic isolation due to glaciations and that the diversity was reduced in the west by a recent Wolbachia-driven sweep(s). The intermediate clade exhibited a body size and host plant that differed from the other clades. Pros and cons of the possible use of infected-clade males to control uninfected populations are discussed.

CBGP Cirad Montpellier SupAgro INRA IRD Univ Montpellier Montpellier France

Department of Biological Control Plant Protection Research Institute Agricultural Research Center Giza Egypt

Entomological Laboratory Graduate School of Bioresource and Bioenvironmental Sciences Kyushu University Fukuoka Japan

GRBA BE LE3PI Laboratory Department of Chemical Engineering and Applied Biology Polytechnic Higher School of Dakar Dakar Senegal

Group Function of Invertebrate and Plant Biodiversity in Agro Ecosystems Crop Research Institute Drnovska Praha Czech Republic

Hungarian Natural History Museum Budapest Hungary

Institute of Biological Control Faculty of Agriculture Kyushu University Fukuoka 819 0395 Japan

Laboratory of Insect Natural Enemies Department of Bioresource Sciences Faculty of Agriculture Kyushu University Fukuoka Japan

Nata Danchi Fukuoka Japan

Research Institute of Environment Agriculture and Fisheries Osaka Prefecture Japan

School of Biological Sciences University of Queensland Brisbane Australia

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