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.

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Soil‐burrowing cockroaches (Blaberidae: Geoscapheinae) are large insects endemic to Australia. Originally thought to represent a monophyletic group, these enigmatic species have in fact evolved burrowing behaviour, associated fossorial morphological modifications, and dietary transitions to dry leaf litter feeding multiple times from the wood‐feeding Panesthiinae in a striking example of parallel evolution. However, various relationships within these two subfamilies remain unresolved or poorly understood, notably the apparent paraphyly of Panesthiinae with respect to Geoscapheinae, the position and diversification of certain species within major clades, and several aspects of the overall group's biogeography and morphological evolution. Here, we investigate the phylogeny of Australian members of these two subfamilies using whole mitochondrial genomes paired with nuclear ribosomal markers and highly conserved genes from the bacterial endosymbiont Blattabacterium. Using the resulting robust, fossil‐calibrated phylogeny from these three sources we confirm the nonmonophyly of both subfamilies and recover Geoscapheinae as polyphyletic within a paraphyletic Panesthiinae. The nonmonophyly of natural groups, at all levels from subfamily to species, has been driven by repeated, independent acquisitions of burrowing forms in Geoscapheinae from panesthiine ancestors that colonized the continent on two separate occasions during the Miocene. We additionally find morphological variation within Geoscapheinae itself is correlated with species distributions. Older soil‐burrowing clades living in comparatively arid environments have additional morphological reductions beyond obvious fossorial adaptations compared to those in younger burrowing clades from more temperate habitats. Ultimately, the results presented here demonstrate connections among phylogeny, biogeography and morphology throughout Australian representatives of these two subfamilies, factors that could not be previously consolidated using existing phylogenetic frameworks. Given the discordance between molecular data implemented here and the existing taxonomic classification, we find no support for retaining Geoscapheinae as a discrete taxonomic grouping. In closing, we discuss the taxonomic implications of these results and present a roadmap for future research on Geoscapheinae and their panesthiine relatives.

In addition to harbouring intestinal symbionts, some animal species also possess intracellular symbiotic microbes. The relative contributions of gut-resident and intracellular symbionts to host metabolism, and how they coevolve are not well understood. Cockroaches and the termite Mastotermes darwiniensis present a unique opportunity to examine the evolution of spatially separated symbionts, as they harbour gut symbionts and the intracellular symbiont Blattabacterium cuenoti. The genomes of B. cuenoti from M. darwiniensis and the social wood-feeding cockroach Cryptocercus punctulatus are each missing most of the pathways for the synthesis of essential amino acids found in the genomes of relatives from non-wood-feeding hosts. Hypotheses to explain this pathway degradation include: (i) feeding on microbes present in rotting wood by ancestral hosts; (ii) the evolution of high-fidelity transfer of gut microbes via social behaviour. To test these hypotheses, we sequenced the B. cuenoti genome of a third wood-feeding species, the phylogenetically distant and non-social Panesthia angustipennis. We show that host wood-feeding does not necessarily lead to degradation of essential amino acid synthesis pathways in B. cuenoti, and argue that ancestral high-fidelity transfer of gut microbes best explains their loss in strains from M. darwiniensis and C. punctulatus.

Almost all examined cockroaches harbor an obligate intracellular endosymbiont, Blattabacterium cuenoti. On the basis of genome content, Blattabacterium has been inferred to recycle nitrogen wastes and provide amino acids and cofactors for its hosts. Most Blattabacterium strains sequenced to date harbor a genome of ∼630 kbp, with the exception of the termite Mastotermes darwiniensis (∼590 kbp) and Cryptocercus punctulatus (∼614 kbp), a representative of the sister group of termites. Such genome reduction may have led to the ultimate loss of Blattabacterium in all termites other than Mastotermes. In this study, we sequenced 11 new Blattabacterium genomes from three species of Cryptocercus in order to shed light on the genomic evolution of Blattabacterium in termites and Cryptocercus. All genomes of Cryptocercus-derived Blattabacterium genomes were reduced (∼614 kbp), except for that associated with Cryptocercus kyebangensis, which comprised 637 kbp. Phylogenetic analysis of these genomes and their content indicates that Blattabacterium experienced parallel genome reduction in Mastotermes and Cryptocercus, possibly due to similar selective forces. We found evidence of ongoing genome reduction in Blattabacterium from three lineages of the C. punctulatus species complex, which independently lost one cysteine biosynthetic gene. We also sequenced the genome of the Blattabacterium associated with Salganea taiwanensis, a subsocial xylophagous cockroach that does not vertically transmit gut symbionts via proctodeal trophallaxis. This genome was 632 kbp, typical of that of nonsubsocial cockroaches. Overall, our results show that genome reduction occurred on multiple occasions in Blattabacterium, and is still ongoing, possibly because of new associations with gut symbionts in some lineages.