Termites digest wood using Carbohydrate-Active Enzymes (CAZymes) produced by gut bacteria with whom they have cospeciated at geological timescales. Whether CAZymes were encoded in the genomes of their ancestor's gut bacteria and transmitted to modern termites or acquired more recently from bacteria not associated with termites is unclear. We used gut metagenomes from 195 termites and one Cryptocercus, the sister group of termites, to investigate the evolution of termite gut bacterial CAZymes. We found 420 termite-specific clusters in 81 bacterial CAZyme gene trees, including 404 clusters showing strong cophylogenetic patterns with termites. Of the 420 clusters, 131 included at least one bacterial CAZyme sequence associated with Cryptocercus or Mastotermes, the sister group of all other termites. Our results suggest many bacterial CAZymes have been encoded in the genomes of termite gut bacteria since termite origin, indicating termites rely upon many bacterial CAZymes endemic to their guts to digest wood.

• MeSH
• Bacteria * enzymology   genetics   MeSH
• Bacterial Proteins metabolism   genetics   MeSH
• Phylogeny * MeSH
• Isoptera * microbiology   enzymology   MeSH
• Carbohydrate Metabolism MeSH
• Metagenome MeSH
• Evolution, Molecular MeSH
• Gastrointestinal Microbiome MeSH
• Cockroaches microbiology   enzymology   MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Names of Substances
• Bacterial Proteins MeSH

The higher classification of termites requires substantial revision as the Neoisoptera, the most diverse termite lineage, comprise many paraphyletic and polyphyletic higher taxa. Here, we produce an updated termite classification using genomic-scale analyses. We reconstruct phylogenies under diverse substitution models with ultraconserved elements analyzed as concatenated matrices or within the multi-species coalescence framework. Our classification is further supported by analyses controlling for rogue loci and taxa, and topological tests. We show that the Neoisoptera are composed of seven family-level monophyletic lineages, including the Heterotermitidae Froggatt, Psammotermitidae Holmgren, and Termitogetonidae Holmgren, raised from subfamilial rank. The species-rich Termitidae are composed of 18 subfamily-level monophyletic lineages, including the new subfamilies Crepititermitinae, Cylindrotermitinae, Forficulitermitinae, Neocapritermitinae, Protohamitermitinae, and Promirotermitinae; and the revived Amitermitinae Kemner, Microcerotermitinae Holmgren, and Mirocapritermitinae Kemner. Building an updated taxonomic classification on the foundation of unambiguously supported monophyletic lineages makes it highly resilient to potential destabilization caused by the future availability of novel phylogenetic markers and methods. The taxonomic stability is further guaranteed by the modularity of the new termite classification, designed to accommodate as-yet undescribed species with uncertain affinities to the herein delimited monophyletic lineages in the form of new families or subfamilies.

• MeSH
• Phylogeny * MeSH
• Genome, Insect MeSH
• Genomics * methods   MeSH
• Isoptera * genetics   classification   MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH

The decomposition of wood and detritus is challenging to most macroscopic organisms due to the recalcitrant nature of lignocellulose. Moreover, woody plants often protect themselves by synthesizing toxic or nocent compounds which infuse their tissues. Termites are essential wood decomposers in warmer terrestrial ecosystems and, as such, they have to cope with high concentrations of plant toxins in wood. In this paper, we evaluated the influence of wood age on the gut microbial (bacterial and fungal) communities associated with the termites Reticulitermes flavipes (Rhinotermitidae) (Kollar, 1837) and Microcerotermes biroi (Termitidae) (Desneux, 1905). We confirmed that the secondary metabolite concentration decreased with wood age. We identified a core microbial consortium maintained in the gut of R. flavipes and M. biroi and found that its diversity and composition were not altered by the wood age. Therefore, the concentration of secondary metabolites had no effect on the termite gut microbiome. We also found that both termite feeding activities and wood age affect the wood microbiome. Whether the increasing relative abundance of microbes with termite activities is beneficial to the termites is unknown and remains to be investigated. IMPORTANCE Termites can feed on wood thanks to their association with their gut microbes. However, the current understanding of termites as holobiont is limited. To our knowledge, no studies comprehensively reveal the influence of wood age on the termite-associated microbial assemblage. The wood of many tree species contains high concentrations of plant toxins that can vary with their age and may influence microbes. Here, we studied the impact of Norway spruce wood of varying ages and terpene concentrations on the microbial communities associated with the termites Reticulitermes flavipes (Rhinotermitidae) and Microcerotermes biroi (Termitidae). We performed a bacterial 16S rRNA and fungal ITS2 metabarcoding study to reveal the microbial communities associated with R. flavipes and M. biroi and their impact on shaping the wood microbiome. We noted that a stable core microbiome in the termites was unaltered by the feeding substrate, while termite activities influenced the wood microbiome, suggesting that plant secondary metabolites have negligible effects on the termite gut microbiome. Hence, our study shed new insights into the termite-associated microbial assemblage under the influence of varying amounts of terpene content in wood and provides a groundwork for future investigations for developing symbiont-mediated termite control measures.

• Keywords
• Microcerotermes biroi, Reticulitermes flavipes, bacteria, core-microbiome, ectosymbionts, endosymbionts, fungi, plant defenses, terpenoids, wood-feeding termites,
• MeSH
• Bacteria genetics   MeSH
• Wood * metabolism   MeSH
• Ecosystem MeSH
• Isoptera * microbiology   MeSH
• RNA, Ribosomal, 16S genetics   metabolism   MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• RNA, Ribosomal, 16S MeSH

Fungi are diverse organisms that occupy important niches in natural settings and agricultural settings, acting as decomposers, mutualists, and parasites and pathogens. Interactions between fungi and other organisms, specifically invertebrates, are understudied. Their numbers are also severely underestimated. Invertebrates exist in many of the same spaces as fungi and are known to engage in fungal feeding or mycophagy. This review aims to provide a comprehensive, global view of mycophagy in invertebrates to bring attention to areas that need more research, by prospecting the existing literature. Separate searches on the Web of Science were performed using the terms "mycophagy" and "fungivore". Invertebrate species and corresponding fungal species were extracted from the articles retrieved, whether the research was field- or laboratory-based, and the location of the observation if field-based. Articles were excluded if they did not list at least a genus identification for both the fungi and invertebrates. The search yielded 209 papers covering seven fungal phyla and 19 invertebrate orders. Ascomycota and Basidiomycota are the most represented fungal phyla whereas Coleoptera and Diptera make up most of the invertebrate observations. Most field-based observations originated from North America and Europe. Research on invertebrate mycophagy is lacking in some important fungal phyla, invertebrate orders, and geographic regions.

• Keywords
• biological control, fungal cultivation, fungivory, grazing, invertebrate ecology, literature data, microhabitats, secondary metabolites, spore dispersal,
• Publication type
• Journal Article MeSH
• Review MeSH

Termites (Blattodea: Isoptera) have evolved specialized defensive strategies for colony protection. Alarm communication enables workers to escape threats while soldiers are recruited to the source of disturbance. Here, we study the vibroacoustic and chemical alarm communication in the wood roach Cryptocercus and in 20 termite species including seven of the nine termite families, all life-types, and all feeding and nesting habits. Our multidisciplinary approach shows that vibratory alarm signals represent an ethological synapomorphy of termites and Cryptocercus. In contrast, chemical alarms have evolved independently in several cockroach groups and at least twice in termites. Vibroacoustic alarm signaling patterns are the most complex in Neoisoptera, in which they are often combined with chemical signals. The alarm characters correlate to phylogenetic position, food type and hardness, foraging area size, and nesting habits. Overall, species of Neoisoptera have developed the most sophisticated communication system amongst termites, potentially contributing to their ecological success.

• MeSH
• Ethology MeSH
• Phylogeny MeSH
• Isoptera * MeSH
• Communication MeSH
• Humans MeSH
• Cockroaches * MeSH
• Animals MeSH
• Check Tag
• Humans MeSH
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH

BACKGROUND: Termites primarily feed on lignocellulose or soil in association with specific gut microbes. The functioning of the termite gut microbiota is partly understood in a handful of wood-feeding pest species but remains largely unknown in other taxa. We intend to fill this gap and provide a global understanding of the functional evolution of termite gut microbiota. RESULTS: We sequenced the gut metagenomes of 145 samples representative of the termite diversity. We show that the prokaryotic fraction of the gut microbiota of all termites possesses similar genes for carbohydrate and nitrogen metabolisms, in proportions varying with termite phylogenetic position and diet. The presence of a conserved set of gut prokaryotic genes implies that essential nutritional functions were present in the ancestor of modern termites. Furthermore, the abundance of these genes largely correlated with the host phylogeny. Finally, we found that the adaptation to a diet of soil by some termite lineages was accompanied by a change in the stoichiometry of genes involved in important nutritional functions rather than by the acquisition of new genes and pathways. CONCLUSIONS: Our results reveal that the composition and function of termite gut prokaryotic communities have been remarkably conserved since termites first appeared ~ 150 million years ago. Therefore, the "world's smallest bioreactor" has been operating as a multipartite symbiosis composed of termites, archaea, bacteria, and cellulolytic flagellates since its inception. Video Abstract.

• Keywords
• Endosymbionts, Isoptera, Metagenomics, Vertical inheritance,
• MeSH
• Phylogeny MeSH
• Isoptera * MeSH
• Metagenome MeSH
• Soil MeSH
• Gastrointestinal Microbiome * genetics   MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Video-Audio Media MeSH
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• Soil MeSH

Termites feed on vegetal matter at various stages of decomposition. Lineages of wood- and soil-feeding termites are distributed across terrestrial ecosystems located between 45°N and 45°S of latitude, a distribution they acquired through many transoceanic dispersal events. While wood-feeding termites often live in the wood on which they feed and are efficient at dispersing across oceans by rafting, soil-feeders are believed to be poor dispersers. Therefore, their distribution across multiple continents requires an explanation. Here, we reconstructed the historical biogeography and the ancestral diet of termites using mitochondrial genomes and δ13C and δ15N stable isotope measurements obtained from 324 termite samples collected in five biogeographic realms. Our biogeographic models showed that wood-feeders are better at dispersing across oceans than soil-feeders, further corroborated by the presence of wood-feeders on remote islands devoid of soil-feeders. However, our ancestral range reconstructions identified 33 dispersal events among biogeographic realms, 18 of which were performed by soil-feeders. Therefore, despite their lower dispersal ability, soil-feeders performed several transoceanic dispersals that shaped the distribution of modern termites.

• Keywords
• Isoptera, biogeography, ecology, feeding group, mitogenomes, stable isotopes,
• MeSH
• Diet MeSH
• Ecosystem MeSH
• Genome, Mitochondrial * MeSH
• Isoptera * genetics   MeSH
• Soil MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• Soil MeSH

Colonies of social insects contain large amounts of resources often exploited by specialized social parasites. Although some termite species host numerous parasitic arthropod species, called termitophiles, others host none. The reason for this large variability remains unknown. Here, we report that the evolution of termitophily in rove beetles is linked to termite nesting strategies. We compared one-piece nesters, whose entire colony life is completed within a single wood piece, to foraging species, which exploit multiple physically separated food sources. Our epidemiological model predicts that characteristics related to foraging (e.g., extended colony longevity and frequent interactions with other colonies) increase the probability of parasitism by termitophiles. We tested our prediction using literature data. We found that foraging species are more likely to host termitophilous rove beetles than one-piece nesters: 99.6% of known termitophilous species were associated with foraging termites, whereas 0.4% were associated with one-piece nesters. Notably, the few one-piece nesting species hosting termitophiles were those having foraging potential and access to soil. Our phylogenetic analyses confirmed that termitophily primarily evolved with foraging termites. These results highlight that the evolution of complex termite societies fostered social parasitism, explaining why some species have more social parasites than others.

• Keywords
• nest, phylogenetic comparative analysis, sis model, social evolution, social parasitism,
• MeSH
• Coleoptera * MeSH
• Phylogeny MeSH
• Insecta MeSH
• Isoptera * MeSH
• Symbiosis MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH