Clonal genetic variation in a Wolbachia-infected asexual wasp: horizontal transmission or historical sex?

Wolbachia are endocellular bacteria known for manipulating the reproductive systems of many of their invertebrate hosts. Wolbachia are transmitted vertically from mother to offspring. In addition, new infections result from horizontal transmission between different host species. However, to what extent horizontal transmission plays a role in the spread of a new infection through the host population is unknown. Here, we investigate whether horizontal transmission of Wolbachia can explain clonal genetic variation in natural populations of Leptopilina clavipes, a parasitoid wasp infected with a parthenogenesis-inducing Wolbachia. We assessed variance of markers on the nuclear, mitochondrial and Wolbachia genomes. The nuclear and mitochondrial markers displayed significant and congruent variation among thelytokous wasp lineages, showing that multiple lineages have become infected with Wolbachia. The alternative hypothesis in which a single female became infected, the daughters of which mated with males (thus introducing nuclear genetic variance) cannot account for the presence of concordant variance in mtDNA. All Wolbachia markers, including the hypervariable wsp gene, were invariant, suggesting that only a single strain of Wolbachia is involved. These results show that Wolbachia has transferred horizontally to infect multiple female lineages during the early spread through L. clavipes. Remarkably, multiple thelytokous lineages have persisted side-by-side in the field for tens of thousands of generations.

沃尔巴克氏体（Wolbachia）是一类以操纵多种无脊椎动物宿主生殖系统为典型特征的胞内细菌。该菌可通过母代向子代的垂直传播途径进行传递，同时也可经由不同宿主物种间的水平传播途径获得新的感染。然而，水平传播在新感染通过宿主种群扩散过程中所扮演的具体角色仍未明确。本研究旨在探究沃尔巴克氏体的水平传播能否解释长刺茧蜂（Leptopilina clavipes）自然种群中的克隆遗传变异——该寄生蜂可被诱导孤雌生殖的沃尔巴克氏体感染。我们对细胞核基因组、线粒体基因组以及沃尔巴克氏体基因组上的遗传标记开展了方差分析。结果显示，产雌孤雌生殖蜂类谱系间的细胞核与线粒体标记呈现出显著且一致的遗传变异，表明已有多个谱系被沃尔巴克氏体感染。另一种假说认为仅存在单个初始感染雌蜂，其子代雌蜂与雄蜂交配（由此引入细胞核遗传变异），但该假说无法解释线粒体DNA中存在的一致变异。所有沃尔巴克氏体标记，包括高可变wsp基因（wsp gene），均未出现变异，提示本次感染仅涉及单一沃尔巴克氏体菌株。上述结果表明，在长刺茧蜂种群的早期扩散过程中，沃尔巴克氏体通过水平传播感染了多个雌蜂谱系。值得注意的是，多个产雌孤雌生殖谱系已在野外环境中共存了数万代之久。