Comparative genomics reveal signatures of ecological specialization in the striped ambrosia beetle Trypodendron lineatum

Beetles (Coleoptera) display exceptional dietary diversity and occupy a wide range of ecological niches, often involving close associations with plants and microbes. Ambrosia beetles (Curculionidae; Scolytinae and Platypodinae) exemplify ecological specialization by cultivating mutualistic fungi within galleries excavated in their host trees' xylem, with the fungi serving as their main food source. The striped ambrosia beetle Trypodendron lineatum is a pest of conifers, relying on its nutritional mutualist Phialophoropsis ferruginea for survival. This fungiculture-based lifestyle provides a system for exploring how specialized mutualism is reflected at the genomic level. Hence, we performed a comparative genomics analysis between T. lineatum and nine other beetle species with different ecological specializations. We hypothesized that fungiculture is associated with specific genomic adaptations, including changes in gene family composition related to nutrition, detoxification, and immunity.

The small genome of T. lineatum (74.4-83.6 Mb) exhibits comparatively low levels of repetitive DNA (19.9%), including a reduced proportion of transposable elements. Annotation generated 14,830 high-quality gene predictions, most of which were supported by transcript evidence or functional domains. Comparative orthology analysis across ten beetle species identified 13,896 orthogroups, with T.lineatum having 78 species-specific orthogroups comprising 238 genes. Gene family evolution analyses revealed 33 families with significant size changes in T. lineatum, including 16 expansions and 17 contractions. Notably, gene families associated with digestion, detoxification, and immunity were contracted. These included glycoside hydrolase 28, cytochrome P450, serpin, and trypsin families, which may reflect the fungus-based, rather than plant-based, diet of T. lineatum, and reduced reliance on broad-spectrum immune defenses. In contrast, expansions in the THAP and CD80-like immunoglobulin domain families indicate diversification of genes involved in genomic regulation and immune recognition.

Our results suggest that the genome of T. lineatum is characterized by low repeat content and compact gene architecture. The observed contractions in key gene families involved in plant digestion, detoxification, and immunity may represent genomic signatures of its obligate mutualistic specialization and narrow ecological niche. Our findings provide the first insights into the genomic adaptations of fungus-farming ambrosia beetles, suggesting that co-evolved insect-microbe mutualisms may lead to reductions in a variety of gene families.