Opposing Growth Responses of Lepidopteran Larvae to the Establishment of Gut Microbiota

Gut microbiota can have diverse impacts on hosts, the nature of which often depend on the circumstances. For insect gut microbes, the quality and nature of host diets can be a significant force in swinging the pendulum from inconsequential to functionally important. In our study, we addressed whether beneficial microbes in one species impart similar functions to related species under identical conditions. Using fall armyworm (Spodoptera frugiperda), beet armyworm (Spodoptera exigua), and other noctuid hosts, we implemented an axenic rearing strategy and manipulated gut bacterial populations and dietary conditions. Our results revealed that some gut Enterococcus and Enterobacter isolates can facilitate utilization of a poor diet substrate by fall armyworm, but this was not the case for other more optimized diets. While Enterococcus provided benefits to fall armyworm, it was decidedly antagonistic to beet armyworm (Spodoptera exigua) under identical conditions. Unique isolates and bacterial introductions at early growth stages were critical to how both larval hosts performed. Our results provide robust evidence of the roles in which bacteria support lepidopteran larval growth, but also indicate that the directionality of these relationships can differ among congener hosts. IMPORTANCE Insects have intimate relationships with gut microbiota, where bacteria can contribute important functions to their invertebrate hosts. Lepidopterans are important insect pests, but how they engage with their gut bacteria and how that translates to impacts on the host are lacking. Here we demonstrate the facultative nature of gut microbiota in lepidopteran larvae and the importance of diet in driving mutualistic or antagonistic relationships. Using multiple lepidopteran species, we uncover that the same bacteria that can facilitate exploitation of a challenging diet in one host severely diminishes larval performance of another larval species. Additionally, we demonstrate the beneficial functions of gut microbiota on the hosts are not limited to one lineage, but rather multiple isolates can facilitate the exploitation of a suboptimal diet. Our results illuminate the context-dependent nature of the gut microbiomes in invertebrates, and how host-specific microbial engagement can produce dramatically different interactions.