Molecular Phylogeny Reveals the Past Transoceanic Voyages of Drywood Termites (Isoptera, Kalotermitidae)

Abstract

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 Mya (75–93 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 the ancestors of Kalotermitidae were able to forage among multiple wood pieces. Our phylogenetic estimates provide a platform for critical taxonomic revision and future comparative analyses of Kalotermitidae.

Evidence of cospeciation between termites and their gut bacteria on a geological time scale

“…We reconstructed the phylogenetic tree of termites using mitochondrial genome sequences. Termite mitochondrial contigs longer than 5000 bp and more than 90% identical to the previously published whole mitochondrial genomes of termites [29,[44][45][46][47][48][49] were identified using BLAST searches [50]. Complete or near-complete mitochondrial genomes were annotated using the MITOS web server [51].…”

The trail-following communication in Stylotermes spp. (Blattodea, Isoptera, Stylotermitidae)

“…This corroborates the estimation made by chemical analysis. In addition to the identical nature of the trail-following pheromone in Stylotermitidae and Kalotermitidae, these families also share similar way-of-life, feeding on a single piece of wood and unable to colonise additional pieces of wood (Abe 1987;Liang et al 2016;Buček et al 2022). This is also the case for the Stolotermitidae: Stolotermes, Archotermopsidae, Rhinotermitidae: Termitogeton, and Serritermitidae.…”

Termite dispersal is influenced by their diet

“…We used mitochondrial genomes to reconstruct two phylogenetic trees encompassing 324 termite colonies for which we measured stable isotope ratios. Most mitochondrial genomes used in this study have been previously published [11][12][13][14]16,[41][42][43]. We sequenced 19 additional mitochondrial genomes using two methods.…”

“…Termites are distributed between 45°N and 45°S, and their diversity is centred in the tropics [9,10]. Termites have acquired their modern distribution through tens of dispersal events among biogeographical realms [11][12][13][14][15][16]. While some recent dispersal events have been mediated by human activities [17], most predate human origin.…”

“…As modern termites appeared 140-150 million years ago (Ma) [11,[18][19][20], land dispersal followed by vicariance induced by continental drift is, in theory, a potential explanation for the distribution of early-diverging termite lineages. However, most termite dispersals occurred following the global cooling initiated approximately 34 Ma, at the Eocene-Oligocene boundary [21], long after the separation of modern continents [12][13][14]16,21]. More recent land connections, such as the Gomphotherium land bridge that connected Africa and Asia approximately 20 Ma [22], were presumably used by termites to move between continents [12,23].…”