Termite-Like Phylogenetic Conservation of Gut Microbiota in Passalid Beetles Suggests Evolutionary Convergence in Decaying Wood Degradation
Beetles of the family Passalidae are an important group of subsocial wood-decomposing (saproxylophagous) insects, spending their entire life cycle living inside and feeding on rotten logs. Decaying wood is an abundant resource, but nutritionally poor and challenging to digest. As in other saproxylophagous insects, digestion for passalids is only possible through symbiotic relationships with their gut microbiota, highlighting the critical roles of these symbionts in the evolution of wood-decomposing insects. Despite its importance, this critical symbiotic relationship remains poorly understood, hindering our ability to identify the factors shaping this association and assessing its role in the evolution of Passalidae. Using high-throughput sequencing of the microbial 16S rRNA we comparatively analyzed the composition and abundance of symbiont lineages in the anterior hindguts of passalid beetles from two independent mountain systems in the Colombian Caribbean region. We tested the influence of geographical co-occurrence and phylogenetic relatedness on gut microbial composition and structure. We posit that if shared locality was the primary driver of gut microbiome assembly, then sympatric species should harbor more similar microbiomes regardless of their phylogenetic relationships. Alternatively, if host evolutionary history is the dominant factor, congeneric species should exhibit more similar microbiomes regardless of geographic co-occurrence. Our results support that phylogenetic relatedness explained substantially more variation in both bacterial and archaeal communities than geographic locality, indicating that gut microbiome composition is primarily structured by host evolutionary history. Furthermore, bacterial and archaeal communities exhibited evidence of phylosymbiosis, although at different phylogenetic scales: bacterial communities more closely reflected relationships among genus level clades, whereas archaeal communities retained congruence mainly at deeper host lineages. We also uncovered extensive bacterial taxonomic novelty, with nearly half of bacterial reads remaining unclassified at the genus level, highlighting the large undescribed microbial diversity associated with Passalidae. These findings lead to establishing Passalidae as a promising comparative model for investigating the evolutionary processes governing gut microbiome assembly and the evolution of lignocellulose-feeding symbioses.