Microbiota-Mediated Sequential Gallery Colonization by Adults and Larvae of an Invasive Bark Beetle

Symbiotic microbes play critical roles in facilitating the rapid adaptation of invasive insects to the defense systems in host plants. The host pine, Pinus tabuliformis, contains high levels of D-pinitol, which is inherently unsuitable for Dendroctonus valens, an invasive beetle in its introduced range in China. Our previous study has reported that gallery microbiota could degrade D-pinitol to enhance the larval adaptation. However, the adaptive strategies of adults and larvae under differential D-pinitol stress are not yet fully understood. In this study, we explored the D-pinitol-degrading capacity and potential sources of gallery microbiota and compared the structures and functions of D-pinitol-degrading microbes in the guts between adults and larvae. We confirmed that gallery microbiota, rather than native pine endophytes, are responsible for D-pinitol degradation and the formation of a low-pinitol microhabitat, and we postulate that adult beetles are the major contributors to gallery microbiota. Additionally, adult guts harbored a higher abundance of Erwinia and Serratia compared with larval guts and exhibited a stronger D-pinitol-degrading capacity. Our results indicate that adults and larvae employ distinct strategies to overcome differential D‑pinitol stress from host pines. Specifically, adult beetles enrich more D‑pinitol‑degrading microbes in their guts, whereas larvae mainly rely on the external degradation of gallery microbiota. These findings provide additional evidence supporting that the adults and larvae utilize detoxifying microbes to metabolize deterrent compounds and adapt to host pines at different developmental stages.