Spatially Varying <i>Wolbachia</i> Frequencies Reveal the Invasion Origin of an Agricultural Pest Recently Introduced From Europe to North America

The introduction of non-native species across the world represents a major global challenge. Retracing invasion origin is an important first step in understanding the invasion process, often requiring detailed sampling within the native range. Insect species frequently host <i>Wolbachia</i>, a widespread endosymbiotic bacterium that manipulates host reproduction to increase infected female fitness. Here, we draw on the spatial variation in infection frequencies of an actively spreading <i>Wolbachia</i> strain <i>w</i>Cer2 to investigate the invasion origin of the European cherry fruit fly, <i>Rhagoletis cerasi.</i> This pest of cherries was introduced from Europe to North America within the last decade. First, we screen the introduced fly population for the presence of <i>Wolbachia</i>. The introduced populations lack the <i>w</i>Cer2 strain and the strongly associated mitochondrial haplotype, suggesting strain absence due to founder effects with invading individuals originating from <i>w</i>Cer2-uninfected native population(s). To narrow down geographic regions of invasion origin, we perform spatial interpolation of the <i>w</i>Cer2 infection frequency across the native range and predict the infection frequency in unsampled regions. For this, we use an extensive dataset of <i>R. cerasi</i> infection covering 238 populations across Europe over 25 years, complemented with 14 additional populations analyzed for this study. We find that <i>R. cerasi</i> was unlikely introduced from <i>w</i>Cer2-infected populations in Central and Western Europe. We propose <i>w</i>Cer2-uninfected populations from Eastern Europe and the Mediterranean region as the most likely candidates for the invasion origin. This work utilizes <i>Wolbachia</i> as an indirect instrument to provide insights into the invasion source of <i>R. cerasi</i> in North America, revealing yet another application for this multifaceted heritable endosymbiont. Given the prevalence of biological invasions, rapidly uncovering invasion origins gives fundamental insights into how invasive species adapt to new environments.