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

Stylotermitidae appear peculiar among all termites, feeding in trunks of living trees in South Asia only. The difficulty to collect them limits the ability to study them, and they thus still belong to critically unknown groups in respect to their biology. We used a combination of microscopic observations, chemical analysis and behavioural tests, to determine the source and chemical nature of the trail-following pheromone of Stylotermes faveolus from India and S. halumicus from Taiwan. The sternal gland located at the 5th abdominal segment was the exclusive source of the trail-following pheromone in both S. faveolus and S. halumicus, and it is made up of class I, II and III secretory cells. Using gas chromatography coupled mass spectrometry, (3Z)-dodec-3-en-1-ol (DOE) was identified as the trail-following pheromone which elicits strong behavioural responses in workers at a threshold around 10- 4 ng/cm and 0.1 ng/gland. Our results confirm the switch from complex aldehyde trail-following pheromones occurring in the basal groups to simpler linear alcohols in the ancestor of Kalotermitidae and Neoisoptera.

• Keywords
• (3Z)-dodec-3-en-1-ol, Neoisoptera, Semiochemicals, sternal gland,
• MeSH
• Pheromones * chemistry   MeSH
• Animal Communication * MeSH
• Gas Chromatography-Mass Spectrometry MeSH
• Cockroaches * MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Names of Substances
• Pheromones * MeSH

Termites host diverse communities of gut microbes, including many bacterial lineages only found in this habitat. The bacteria endemic to termite guts are transmitted via two routes: a vertical route from parent colonies to daughter colonies and a horizontal route between colonies sometimes belonging to different termite species. The relative importance of both transmission routes in shaping the gut microbiota of termites remains unknown. Using bacterial marker genes derived from the gut metagenomes of 197 termites and one Cryptocercus cockroach, we show that bacteria endemic to termite guts are mostly transferred vertically. We identified 18 lineages of gut bacteria showing cophylogenetic patterns with termites over tens of millions of years. Horizontal transfer rates estimated for 16 bacterial lineages were within the range of those estimated for 15 mitochondrial genes, suggesting that horizontal transfers are uncommon and vertical transfers are the dominant transmission route in these lineages. Some of these associations probably date back more than 150 million years and are an order of magnitude older than the cophylogenetic patterns between mammalian hosts and their gut bacteria. Our results suggest that termites have cospeciated with their gut bacteria since first appearing in the geological record.

• Keywords
• cophylogeny, endosymbionts, isoptera, metagenomics, vertical inheritance,
• MeSH
• Bacteria genetics   MeSH
• Phylogeny MeSH
• Isoptera * MeSH
• Mammals MeSH
• Gastrointestinal Microbiome * MeSH
• Symbiosis MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH

The neotropical Apicotermitinae is a common and widespread clade of mostly soil-feeding soldierless termites. With few exceptions, species of this group were originally assigned to the genus Anoplotermes Müller, 1873. The application of internal worker morphology coupled with genetic sequencing has recently shed light on the true diversity of this subfamily. Herein, Anoplotermessusanae Scheffrahn, Carrijo & Castro, sp. nov. and four new species in four new genera are described: Hirsutitermeskanzakii Scheffrahn, Carrijo & Castro, gen. nov. et sp. nov., Krecekitermesdaironi Scheffrahn, Carrijo & Castro, gen. nov. et sp. nov., Mangolditermescurveileum Scheffrahn, Carrijo & Castro, gen. nov. et sp. nov., and Ourissotermesgiblinorum Scheffrahn, Carrijo & Castro, gen. nov. et sp. nov. Worker descriptions are based mainly on worker gut morphology, including the enteric valve, while imagoes were described based on external characters. A Bayesian phylogenetic tree of New World Apicotermitinae was constructed using the complete mitogenome to infer genera relationships and corroborate the taxonomic decisions. Distribution maps and a dichotomic key to the known Neotropical Apicotermitinae genera are provided.

• Keywords
• Enteric valve armature, Linnean shortfall, mitogenome sequencing, soil-feeder, species distribution, taxonomy,
• 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

Termites are dominant animals of tropical terrestrial ecosystems. Their success is due to their eusocial organization as well as their ability to digest dead plant tissues. While being extremely abundant, the termite diet is poor in crucial nutrients, such as fatty acids. Linoleic acid (LA) is a precursor for many vital biomolecules, and most animals depend on its dietary supply. Termites count among the exceptions known to produce LA de novo, presumably via the action of an unknown Δ12 fatty acyl desaturase (FAD) introducing the second double bond into monounsaturated oleic acid. Here, we search for the evolutionary origin of LA biosynthesis in termites. To this end, we compile the repertoire of FAD homologs from 57 species of termites and their closest relatives, the cockroaches, analyze FAD phylogeny, and identify a potential Δ12 FAD branch, which arose through duplication of a likely Δ9 FAD. We functionally characterize both paralogs and identify the Δ9 activity in the ancestral FAD-A1a and the Δ12 activity responsible for LA biosynthesis in FAD-A1b. Through the combination of homology modeling and site-directed mutagenesis, we pinpoint structural features possibly contributing to the distinct functions, regiospecificities, and substrate preferences of the two enzymes. We confirm the presence of both paralogs in all 36 studied species of the Blattoidea lineage (Blattidae, Lamproblattidae, Cryptocercidae, and termites) and conclude that we identified an evolutionary event important for the ecological success of termites, which took place in their cockroach ancestors roughly 160 My and remained conserved throughout termite diversification into 3,000 extant species.

• Keywords
• Blattodea, Isoptera, biosynthesis, fatty acyl desaturases, linoleic acid, termites,
• MeSH
• Ecosystem MeSH
• Phylogeny MeSH
• Isoptera * genetics   MeSH
• Linoleic Acid MeSH
• Fatty Acids MeSH
• Cockroaches * MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• Linoleic Acid MeSH
• Fatty Acids 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