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/CA1A21B6-573E-4855-8C88-372453C922F7.

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.

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Termites are dominant organisms of tropical ecosystems. Their success is partly due to the diversity of their feeding substrates, from dead plant tissues to mineralised soils. The Apicotermitinae is one of the richest subfamilies of soil-feeding termites, which are traditionally classified in feeding groups according to anatomical criteria, deemed to the reveal whether species feed on organic-rich layers (group III) or on mineralised soil (group IV). Previous studies based on δ 15 N isotopic values showed that this subfamily's niche covers a broad range along the gradient of humification. We hypothesised that this broad feeding range could be reflected in the crop-gizzard (Cr-Gi) content and volume. We investigated 17 African species distributed between the two feeding groups. Our results showed a variation of Cr-Gi volume and a consistent composition of content among Apicotermitinae species. Some small-bodied species had a very large Cr-Gi volume relative to their size, indicating a difference in foraging behaviour. These species might use this enhanced storage capacity to forage for longer periods of time. Cr-Gi content was dominated by clay (kaolinite) suggesting that a dietary specialisation could be based on the quality of organic compounds from organo-mineral aggregates. Variations in crystalline solids (quartz) between species indicate either differences in the abundance of mineral grains between feeding patches or active discrimination among particles by foragers. The similar composition of Cr-Gi contents in afrotropical Apicotermitinae suggests that the anatomical criteria used to assign species to feeding groups III or IV are not appropriate.