Admixture without recurrent intercontinental gene flow: contrasting patterns of genetic diversity and knockdown resistance profiles reveal independent evolution in resurgent common bed bug populations

Abstract

The common bed bug (Cimex lectularius) was largely eliminated from industrialized countries by mid-twentieth century insecticide campaigns including the widespread application of DDT. However, by the late 1990s, populations were resurging on a global scale. This rapid reemergence has been widely attributed to increased rates of international travel facilitating frequent intercontinental dispersal of insecticide-resistant populations. Because bed bugs disperse almost exclusively through human-mediated means, this scenario predicts that frequent gene flow should homogenize populations globally and enable the rapid worldwide spread of resistance alleles. We tested this prevailing hypothesis using microsatellite markers and knockdown resistance (kdr) genotyping from populations across the United States, Canada, and Europe, sampled within approximately ten years of resurgence onset. Contrary to expectations, we found strong regional genetic structure indicating limited intercontinental gene flow. U.S. populations exhibited significantly higher within-population allelic diversity than European populations, likely through admixture of historical U.S. lineages, while Europe maintained the highest regional allelic richness. Furthermore, kdr profiles differed dramatically. Specifically, while the L925I mutation is ubiquitous across regions, the V419L resistance-associated mutation was present in over 55% of USA populations (in combination with the L925I mutation) but virtually absent from Europe and Canada. These findings challenge the prevailing narrative, suggesting the resurgence reflects regional expansion of evolutionarily independent lineages that persisted in cryptic refugia rather than frequent intercontinental mixing during early resurgence, and have important implications for predicting resistance spread.