Disruption of the microbiota affects physiological and evolutionary aspects of insecticide resistance in the German cockroach, an important urban pest

The German cockroach, Blatella germanica, is a common pest in urban environments and is among the most resilient insects in the world. The remarkable ability of the German cockroach to develop resistance when exposed to toxic insecticides is a prime example of adaptive evolution and makes control of this insect an ongoing struggle. Like many other organisms, the German cockroach is host to a diverse community of symbiotic microbes that play important roles in its physiology. In some insect species, there is a strong correlation between the commensal microbial community and insecticide resistance. In particular, several bacteria have been implicated in the detoxification of xenobiotics, including synthetic insecticides. While multiple mechanisms that mediate insecticide resistance in cockroaches have been discovered, significant knowledge gaps still exist in this area of research. Here, we examine the effects of altering the microbiota on resistance to a common insecticide using antibiotic treatments. We describe an indoxacarb-resistant laboratory strain in which treatment with antibiotic increases susceptibility to orally administered insecticide. We further reveal that this strains harbors a gut microbial community that differs significantly from that of susceptible cockroaches in which insecticide resistance is unaffected by antibiotic. More importantly, we demonstrate that transfer of gut microbes from the resistant to the susceptible strain via fecal transplant increases its resistance. Lastly, our data show that antibiotic treatment adversely affects several reproductive life-history traits that may contribute to the dynamics of resistance at the population level. Together these results suggest that the microbiota contributes to both physiological and evolutionary aspects of insecticide resistance and that targeting this community may be an effective strategy to control the German cockroach.

德国小蠊（Blatella germanica）是城市环境中的常见害虫，也是全球抗逆性最强的昆虫类群之一。其在接触有毒杀虫剂时产生抗药性的卓越能力，是适应性进化的典型范例，也使得对该昆虫的防控成为一项长期挑战。与多数其他生物类似，德国小蠊作为宿主，拥有多样化的共生微生物群落，这些微生物在其生理过程中发挥关键作用。在部分昆虫物种中，共生微生物群落与杀虫剂抗药性之间存在显著相关性。已有多项研究证实，多种细菌可参与包括合成杀虫剂在内的异生物质（xenobiotics）的解毒过程。尽管目前已发现多种介导蟑螂抗药性的机制，但该研究领域仍存在显著的知识缺口。本研究通过抗生素处理手段，探究了改变肠道微生物群对常见杀虫剂抗药性的影响。我们描述了一株耐茚虫威（indoxacarb）的实验室品系，经抗生素处理后，该品系对经口施用的杀虫剂敏感性显著提升。我们进一步发现，该抗药性品系的肠道微生物群落与易感品系存在显著差异，而易感品系的抗药性不受抗生素处理的影响。更为关键的是，我们证实通过粪便移植将抗药性品系的肠道微生物转移至易感品系，可显著提升后者的抗药性水平。最后，本研究的数据显示，抗生素处理会对德国小蠊的多项繁殖生活史特征产生不利影响，这些特征或可影响种群层面的抗药性动态。综合以上结果，本研究表明肠道微生物群既参与了杀虫剂抗药性的生理调控，也参与了其进化过程；靶向肠道微生物群落或可成为防治德国小蠊的有效策略。