Department of Evolutionary Ecology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg-University, Mainz, Germany.
Department of Insect Symbiosis, Max-Planck-Institute for Chemical Ecology, Jena, Germany.
Mol Ecol. 2022 Dec;31(24):6570-6587. doi: 10.1111/mec.16717. Epub 2022 Oct 24.
The endosymbiotic Wolbachia is one of the most common intracellular bacteria known in arthropods and nematodes. Its ability for reproductive manipulation can cause unequal inheritance to male and female offspring, allowing the manipulator to spread, but potentially also impact the evolutionary dynamics of infected hosts. Estimated to be present in up to 66% of insect species, little is known about the phenotypic impact of Wolbachia within the order Coleoptera. Here, we describe the reproductive manipulation by the Wolbachia strain wSur harboured by the sawtoothed grain beetle Oryzaephilus surinamensis (Coleoptera, Silvanidae), through a combination of genomics approaches and bioassays. The Wolbachia strain wSur belongs to supergroup B that contains well-described reproductive manipulators of insects and encodes a pair of cytoplasmic incompatibility factor (cif) genes, as well as multiple homologues of the WO-mediated killing (wmk) gene. A phylogenetic comparison with wmk homologues of wMel of Drosophila melanogaster identified 18 wmk copies in wSur, including one that is closely related to the wMel male-killing homologue. However, further analysis of this particular wmk gene revealed an eight-nucleotide deletion leading to a stop-codon and subsequent reading frame shift midsequence, probably rendering it nonfunctional. Concordantly, utilizing a Wolbachia-deprived O. surinamensis population and controlled mating pairs of wSur-infected and noninfected partners, we found no experimental evidence for male-killing. However, a significant ~50% reduction of hatching rates in hybrid crosses of uninfected females with infected males indicates that wSur is causing cytoplasmic incompatibility. Thus, Wolbachia also represents an important determinant of host fitness in Coleoptera.
共生的沃尔巴克氏体是节肢动物和线虫中最常见的一种细胞内细菌。它的生殖操纵能力会导致雄性和雌性后代的不平等遗传，使操纵者得以传播，但也可能影响受感染宿主的进化动态。估计有 66%的昆虫物种携带沃尔巴克氏体，但人们对鞘翅目昆虫体内沃尔巴克氏体的表型影响知之甚少。在这里，我们通过基因组学方法和生物测定相结合，描述了锯谷盗（鞘翅目，Silvanidae）携带的沃尔巴克氏体菌株 wSur 的生殖操纵。沃尔巴克氏体菌株 wSur 属于超级群 B，其中包含昆虫生殖操纵的描述性良好的菌株，并编码一对细胞质不亲和因子（cif）基因，以及 WO 介导的杀伤（wmk）基因的多个同源物。与果蝇（Drosophila melanogaster）的 wMel 的 wmk 同源物的系统发育比较，确定了 wSur 中有 18 个 wmk 拷贝，其中一个与 wMel 的雄性杀伤同源物密切相关。然而，对这个特定的 wmk 基因的进一步分析表明，存在一个导致终止密码子和随后阅读框移码的 8 个核苷酸缺失，可能使其失去功能。相应地，利用沃尔巴克氏体缺乏的锯谷盗种群和感染和未感染的 wSur 感染的配对控制交配对，我们没有发现雄性杀伤的实验证据。然而，未感染的雌性与感染的雄性杂交的孵化率显著降低了约 50%，表明 wSur 引起细胞质不亲和。因此，沃尔巴克氏体也是鞘翅目宿主适应性的一个重要决定因素。
