In a globalized world, parasites are often brought in contact with new potential hosts. When parasites successfully shift host, severe diseases can emerge at a large cost to society. However, the evolutionary processes leading to successful shifts are rarely understood, hindering risk assessment, prevention, or mitigation of their effects. Here, we screened populations of Varroa destructor, an ectoparasitic mite of the honeybee genus Apis, to investigate their genetic structure and reproductive potential on new and original hosts. From the patterns identified, we deduce the factors that influenced the macro- and microevolutionary processes that led to the structure observed. Among the mite variants identified, we found two genetically similar populations that differed in their reproductive abilities and thus in their host specificity. These lineages could interbreed, which represents a threat due to the possible increased virulence of the parasite on its original host. However, interbreeding was unidirectional from the host-shifted to the nonshifted native mites and could thus lead to speciation of the former. The results improve our understanding of the processes affecting the population structure and evolution of this economically important mite genus and suggest that introgression between shifted and nonshifted lineages may endanger the original host.

在全球化的世界中，寄生虫经常与新的潜在宿主接触。当寄生虫成功转移宿主时，可能会出现严重疾病，给社会造成巨大损失。然而，导致成功转变的演变过程却很少被理解，这阻碍了风险评估、预防或减轻其影响。在这里，我们筛选了破坏瓦螨（蜜蜂属的一种外寄生螨）种群，以研究它们在新宿主和原始宿主上的遗传结构和繁殖潜力。从确定的模式中，我们推断出影响导致观察到的结构的宏观和微观进化过程的因素。在鉴定出的螨虫变种中，我们发现了两个基因相似的种群，但它们的繁殖能力不同，因此宿主特异性也不同。这些谱系可能会杂交，这会带来威胁，因为寄生虫对其原始宿主的毒力可能会增加。然而，从宿主转移到非转移的本地螨虫的杂交是单向的，因此可能导致前者的物种形成。这些结果提高了我们对影响这种经济上重要的螨属的种群结构和进化的过程的理解，并表明转移谱系和非转移谱系之间的基因渗入可能会危及原始宿主。