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Fossils encompassing multiple individuals provide rare direct evidence of behavioral interactions among extinct organisms. However, the fossilization process can alter the spatial relationship between individuals and hinder behavioral reconstruction. Here, we report a Baltic amber inclusion preserving a female-male pair of the extinct termite speciesElectrotermes affinis. The head-to-abdomen contact in the fossilized pair resembles the tandem courtship behavior of extant termites, although their parallel body alignment differs from the linear alignment typical of tandem runs. To solve this inconsistency, we simulated the first stage of amber formation, the immobilization of captured organisms, by exposing living termite tandems to sticky surfaces. We found that the posture of the fossilized pair matches trapped tandems and differs from untrapped tandems. Thus, the fossilized pair likely is a tandem running pair, representing the first direct evidence of the mating behavior of extinct termites. Furthermore, by comparing the positions of partners on a sticky surface and in the amber inclusion, we estimated to 67% the probability that the leader role in the fossilized tandem was performed by a male. Our results demonstrate that past behavioral interactions can be reconstructed despite the spatial distortion of body poses during fossilization. Our taphonomic approach clarifies how certain behaviors can be inferred from fossil occurrences.

Rates of nucleotide substitution vary substantially across the Tree of Life, with potentially confounding effects on phylogenetic and evolutionary analyses. A large acceleration in mitochondrial substitution rate occurs in the cockroach family Nocticolidae, which predominantly inhabit subterranean environments. To evaluate the impacts of this among-lineage rate heterogeneity on estimates of phylogenetic relationships and evolutionary timescales, we analysed nuclear ultraconserved elements (UCEs) and mitochondrial genomes from nocticolids and other cockroaches. Substitution rates were substantially elevated in nocticolid lineages compared with other cockroaches, especially in mitochondrial protein-coding genes. This disparity in evolutionary rates is likely to have led to different evolutionary relationships being supported by mitochondrial genomes and UCE loci. Furthermore, analyses using relaxed-clock models inferred much deeper divergence times compared with a flexible local clock. Our phylogenetic analysis of UCEs, which is the first genome-scale study to include all nine major cockroach families, unites Corydiidae and Nocticolidae and places Anaplectidae as the sister lineage to the rest of Blattoidea. We uncover an extraordinary level of genetic divergence in Nocticolidae, including two highly distinct clades that separated ∼115 million years ago despite both containing representatives of the genusNocticola. The results of our study highlight the potential impacts of high among-lineage rate variation on estimates of phylogenetic relationships and evolutionary timescales.

Soil-feeding termites are abundant in tropical regions and play an important role in soil bioturbation and in the organic matter cycle. The Apicotermitinae are arguably the most diverse lineage of soil-feeding termites, but they are also the most understudied, probably because many species are soldierless, which makes identification difficult. Although the backbone of the termite phylogenetic tree is now well-resolved, the relationships among representatives of Apicotermitinae are still largely unknown. Here, we present phylogenetic trees inferred from 113 mitochondrial genomes of Apicotermitinae representative of the group diversity. Our analyses confirm the monophyly of the Apicotermitinae and the basal position of soldiered taxa, within which two lineages of soldierless species are nested. We describe two new monotypic genera, whose phylogenetic position appeared of special interest: Koutabatermes gen. n., lies on a long branch among soldiered taxa, and Apolemotermes gen. n., is sister to Adaiphrotermes. We resolved, with high support, the position of Asian genera as sister group of a clade comprising the monophyletic neotropical Anoplotermes-group and the small African clade including Adaiphrotermes and Apolemotermes gen. n.. Our trees cast light on the intergeneric and interspecific relationships within Apicotermitinae and reveal the polyphyly of several genera, including Ruptitermes, Astalotermes and Anoplotermes. Biogeographic reconstructions revealed two dispersal events out of Africa, one to the Oriental realm and one to the Neotropical realm. Overall, the timing of Apicotermitinae diversification and dispersal, following the Eocene–Oligocene boundary, matches that found for other groups of Neoisoptera. Nomenclatural acts are registered in ZooBank: http://zoobank.org/urn:lsid:zoobank.org:pub:CA1A21B6-573E-4855-8C88-372453C922F7.

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.

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 studied 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. Using a multidisciplinary approach, we found that vibratory alarm signals represent an ethological synapomorphy of termites and Cryptocercus, while chemical alarms evolved independently in several cockroach groups, and at least twice in termites. Vibroacoustic alarm signaling patterns were the most complex in Neoisoptera, in which they were often combined with chemical signals. The alarm characters correlated 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.

Recent attempts to explain the evolutionary prevalence of same-sex sexual behaviour (SSB) have focused on the role of indiscriminate mating. However, in many cases, SSB involves plastically adjusting sex roles to achieve successful courtship or pairing. To evaluate this overlooked factor, we tested whether ancestral sex-role plasticity facilitated the evolution of SSB in the termite Reticulitermes speratus. Male termites follow females in paired ‘tandems’ before mating, and movement patterns are sexually dimorphic. Adaptive same-sex tandems occur in both sexes. We show that in such cases, one partner adopts the other sex’s movement patterns, resulting in behavioural dimorphism. Data-based simulations confirmed that this socially-cued plasticity contributes to pair maintenance because dimorphic movements improve reunion success upon accidental separation. Phylogenetic analysis indicated that the ancestors of modern termites lack consistent sex roles during pairing, indicating that R. speratus inherited the plasticity from the ancestor. Socio-environmental induction of ancestral behavioural potential may be of widespread importance to the evolutionary maintenance of SSB.

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 δ 13 C and δ 15 N 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.

Termites are major decomposers in terrestrial ecosystems and the second most diverse lineage of social insects. The Kalotermitidae form the second-largest termite family and are distributed across tropical and subtropical ecosystems, where they typically live in small colonies confined to single wood items inhabited by individuals with no foraging abilities. How the Kalotermitidae have acquired their global distribution patterns remains unresolved. Similarly, it is unclear whether foraging is ancestral to Kalotermitidae or was secondarily acquired in a few species. These questions can be addressed in a phylogenetic framework. We inferred time-calibrated phylogenetic trees of Kalotermitidae using mitochondrial genomes of ∼120 species, about 27% of kalotermitid diversity, including representatives of 21 of the 23 kalotermitid genera. Our mitochondrial genome phylogenetic trees were corroborated by phylogenies inferred from nuclear ultraconserved elements derived from a subset of 28 species. We found that extant kalotermitids shared a common ancestor 84 Ma (75–93 Ma 95% highest posterior density), indicating that a few disjunctions among early-diverging kalotermitid lineages may predate Gondwana breakup. However, most of the ∼40 disjunctions among biogeographic realms were dated at, We thank the DNA Sequencing Section and the Scientific Computation and Data Analysis Section of the Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan, for assistance with sequencing and for providing access to the OIST computing cluster, respectively. We also acknowledge support from the Internal Grant Agency of the Faculty of Tropical AgriSciences (CULS No. 20223112).

The Neotropical family Serritermitidae is a monophyletic group of termites including two genera, Serritermes and Glossotermes, with different way-of-life, the former being the sole obligatory inquiline among “lower” termites, while the latter is a single-site nester feeding on dry rotten red wood. Like the most advanced termite’s family, the Termitidae, the Serritermitidae is an inner group of the paraphyletic family “Rhinotermitidae”, but unlike the Termitidae, it has been poorly studied so far. In this study, we bring new insights into the chemical ecology of this key taxon. We studied the trail-following pheromone of Serritermes serrifer and we identified (10Z,13Z)-nonadeca-10,13-dien-2-one as the only component of the trail-following pheromone of this termite species, as it is the case in Glossotermes, the other genus belonging to Serritermitidae. This result makes the family Serritermitidae clearly distinct from other Rhinotermitidae, such as the termites Psammotermes and Prorhinotermes, that use (3Z,6Z,8E)-dodeca-3,6,8-trien-1-ol and/or neocembrene as trail-following pheromones.

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.

Madagascar is home to many endemic plant and animal species owing to its ancient isolation from other landmasses. This unique fauna includes several lineages of termites, a group of insects known for their key role in organic matter decomposition in many terrestrial ecosystems. How and when termites colonised Madagascar remains unknown. In this study, we used 601 mitochondrial genomes, 93 of which were generated from Madagascan samples, to infer the global historical biogeography of Neoisoptera, a lineage containing upwards of 80% of described termite species. Our results indicate that Neoisoptera colonised Madagascar between seven to ten times independently during the Miocene, between 8.4-16.6 Ma (95% HPD: 6.1-19.9 Ma). This timing matches that of the colonization of Australia by Neoisoptera. Furthermore, the taxonomic composition of the Neoisopteran fauna of Madagascar and Australia are strikingly similar, with Madagascar harbouring an additional two lineages absent from Australia. Therefore, akin to Australia, Neoisoptera colonised Madagascar during the global expansion of grasslands, possibly helped by the ecological opportunities arising from the spread of this new biome.

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.

Termites are social cockroaches. Because non-termite cockroaches are larger than basal termite lineages, which themselves include large termite species, it has been proposed that termites experienced a unidirectional body size reduction since they evolved eusociality. However, the validity of this hypothesis remains untested in a phylogenetic framework. Here, we reconstructed termite body size evolution using head width measurements of 1638 modern and fossil termite species. We found that the unidirectional body size reduction model was only supported by analyses excluding fossil species. Analyses including fossil species suggested that body size diversified along with speciation events and estimated that the size of the common ancestor of modern termites was comparable to that of modern species. Our analyses further revealed that body size variability among species, but not body size reduction, is associated with features attributed to advanced termite societies. Our results suggest that miniaturization took place at the origin of termites, while subsequent complexification of termite societies did not lead to further body size reduction.

Termites are social cockroaches. Because non-termite cockroaches are larger than basal termite lineages, which themselves include large termite species, it has been proposed that termites experienced a unidirectional body size reduction since they evolved eusociality. However, the validity of this hypothesis remains untested in a phylogenetic framework. Here, we reconstructed termite body size evolution using head width measurements of 1638 modern and fossil termite species. We found that the unidirectional body size reduction model was only supported by analyses excluding fossil species. Analyses including fossil species suggested that body size diversified along with speciation events and estimated that the size of the common ancestor of modern termites was comparable to that of modern species. Our analyses further revealed that body size variability among species, but not body size reduction, is associated with features attributed to advanced termite societies. Our results suggest that miniaturization took place at the origin of termites, while subsequent complexification of termite societies did not lead to further body size reduction.

Termites are major decomposers of organic matter in terrestrial ecosystems and the second most diverse lineage of social insects. The Kalotermitidae, the second-largest termite family, are widely distributed across tropical and subtropical ecosystems, where they typically live in small colonies confined to single wood items inhabited by individuals with no foraging abilities. How the Kalotermitidae have acquired their global distribution patterns remains unresolved. Similarly, it is unclear whether foraging is ancestral to Kalotermitidae or was secondarily acquired in a few species. These questions can be addressed in a phylogenetic framework. We inferred time-calibrated phylogenetic trees of Kalotermitidae using mitochondrial genomes and nuclear ribosomal RNA genes of ∼120 species, about 27% of kalotermitid diversity, including representatives of 22 of the 23 kalotermitid genera. We found that extant kalotermitids shared a common ancestor 81 Mya (72–91 Mya 95% HPD), indicating that a few disjunctions among early-diverging kalotermitid lineages may predate Gondwana breakup. However, most of the ∼40 disjunctions among biogeographic realms were dated at less than 50 Mya, indicating that transoceanic dispersals, and more recently human-mediated dispersals, have been the major drivers of the global distribution of Kalotermitidae. Our phylogeny also revealed that the capacity to forage is often found in early-diverging kalotermitid lineages, implying that the ancestors of Kalotermitidae were able to forage among multiple wood pieces. Our phylogenetic estimates provide a platform for a critical taxonomic revision of the family and for future comparative analyses of Kalotermitidae.

Intracellular endosymbionts have reduced genomes that progressively lose genes at a timescale of tens of million years. We previously reported that gene loss rate is linked to mutation rate in Blattabacterium, however, the mechanisms causing gene loss are not yet fully understood. Here, we carried out comparative genomic analyses on the complete genome sequences of a representative set of 67 Blattabacterium strains, with sizes ranging between 511 and 645 kb. We found that 200 of the 566 analyzed protein-coding genes were lost in at least one lineage of Blattabacterium, with the most extreme case being one gene that was lost independently in 24 lineages. We found evidence for three mechanisms influencing gene loss in Blattabacterium. First, gene loss rates were found to increase exponentially with the accumulation of substitutions. Second, genes involved in vitamin and amino acid metabolism experienced relaxed selection in Cryptocercus and Mastotermes, possibly triggered by their vertically inherited gut symbionts. Third, we found evidence of epistatic interactions among genes leading to a “domino effect” of gene loss within pathways. Our results highlight the complexity of the process of genome erosion in an endosymbiont.

The phylogenetic history of termites has been investigated using mitochondrial genomes and transcriptomes. However, both sets of markers have specific limitations. Mitochondrial genomes represent a single genetic marker likely to yield phylogenetic trees presenting incongruences with species trees, and transcriptomes can only be obtained from well-preserved samples. In contrast, ultraconserved elements (UCEs) include a great many independent markers that can be retrieved from poorly preserved samples. Here, we designed termite-specific baits targeting 50,616 UCE loci. We tested our UCE bait set on 42 samples of termites and three samples of Cryptocercus, for which we generated low-coverage highly-fragmented genome assemblies and successfully extracted in silico between 3,426 to 42,860 non-duplicated UCEs per sample. Our maximum likelihood phylogenetic tree, reconstructed using the 5,934 UCE loci retrieved from upward of 75% of samples, was congruent with transcriptome-based phylogenies, demonstrating that our UCE bait set is reliable and phylogenetically informative. Combined with non-destructive DNA extraction protocols, our UCE bait set provides the tool needed to carry out a global taxonomic revision of termites based on poorly preserved specimens such as old museum samples. The Termite UCE database is maintained at: https://github.com/oist/TER-UCE-DB/.