Invasive parasites are major threats to biodiversity. The honey bee ectoparasite, Varroa destructor, has shifted
host and spread almost globally several decades ago. This pest is generally considered to be the main global
threat to Western honey bees, Apis mellifera, although the damages it causes are not equivalent in all its new
host’s populations. Due to the high virulence of this parasite and the viruses it vectors, beekeepers generally rely
on acaricide treatments to keep their colonies alive. However, some populations of A. mellifera can survive
without anthropogenic mite control, through the expression of diverse resistance and tolerance traits. Such
surviving colonies are currently found throughout the globe, with the biggest populations being found in SubSaharan Africa and Latin America. Recently, genetic differences between mite populations infesting surviving
and treated A. mellifera colonies in Europe were found, suggesting that adaptations of honey bees drive mite
evolution. Yet, the prevalence of such co-evolutionary adaptations in other invasive populations of V. destructor
remain unknown. Using the previous data from Europe and novel genetic data from V. destructor populations in
South America and Africa, we here investigated whether mites display signs of adaptations to different host
populations of diverse origins and undergoing differing management. Our results show that, contrary to the
differences previously documented in Europe, mites infesting treated and untreated honey bee populations in
Africa and South America are genetically similar. However, strong levels of genetic differentiation were found
when comparing mites across continents, suggesting ongoing allopatric speciation despite a recent spread from
genetically homogenous lineages. This study provides novel insights into the co-evolution of V. destructor and
A. mellifera, and confirms that these species are ideal to investigate coevolution in newly established hostparasite systems.