Genomic data provide insights into the classification of extant termites

Abstract

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.

Fig. 1. Majority rule consensus summary tree produced from 30 maximum-likelihood phylogenetic reconstructions performed with IQ-TREE on concatenated sequence matrices using various nucleotide, codon, and protein models (for details, see Supplementary Data 5).

For readability, we only provided support values (UFBs, ultrafast bootstraps) for nodes representing families and subfamilies. Node labels are site concordance factors (sCFs) calculated on the majority rule consensus tree and the unfiltered UCE supermatrix. Species whose names are in bold were identified as rogue taxa by RogueNaRok (number of times under parentheses; for details, see Supplementary Data 5). The source data used for this figure can be found in the Dryad repository at 10.5061/dryad.02v6wwqbm (trees 1-30 in “File 4: trees.tar”).

Fig. 2. Majority rule consensus summary cladogram produced from 21 multi-species coalescence phylogenetic reconstructions with ASTRAL-III using various nucleotide, codon, and protein models (for details, see Supplementary Data 5).

The tree presented herein (tree 75 in File 4 on Dryad) was constructed from gene trees for which outliers were pruned with TreeShrink (trees 52–72). The summary topology without pruning outliers is identical for all but one intrasubfamilial node (see tree 74 built from trees 31–51 on Dryad: File 4). For readability, we only provided support values (LPPs, local posterior probabilities) for nodes representing families and subfamilies. Node labels are site concordance factors (sCFs) calculated on the majority rule consensus tree and the unfiltered UCE supermatrix. The source data used for this figure can be found in the Dryad repository at 10.5061/dryad.02v6wwqbm (“File 4: trees.tar”).

Fig. 3. Summary cladogram of Isoptera.

This cladogram integrates topologies summarised from analyses performed on concatenated data and coalescence analyses. The preferred topology within anomaly zones estimated from approximately unbiased topological tests is indicated in dashed grey. The biogeographic matrix indicates the realms occupied by extant members of all isopteran families and termitid subfamilies (adapted from Krishna et al. ). Here, we recognise nine realms (sensu Holt et al.): Afrotropical (including Madagascan), Neotropical (incl. Panamanian), Oriental, Australian, Oceanian, Saharo-Arabian, Sino-Japanese, Nearctic, and Palaearctic. For termitid subfamilies, we report the main diagnostic features based on workers’ digestive tubes and soldiers’ heads. These features are summarised from Supplementary Notes 1 and 3, and Supplementary Figs. 1–18. (i) For workers’ midgut-hindgut junction, we indicate: the presence of a mixed segment (square; stippled section), the presence of Malpighian nodules (circle); the presence of a Malpighian knot (full diamond) or pseudo-knot (full diamond with empty circle); the shape of the junction between the mixed segment and the ileum (P1) either elbowed (empty oval) or arched (full oval). For the hindgut, we indicate the presence of a ventral loop (star) formed under the rectum (P5) by P1; and the position (triangle) of the enteric valve (P2, indicated by an arrow) at the insertion of P1 into the paunch (P3). (ii) For termitid soldiers, we indicate the presence of a frontal projection (hexagon) and whether the fontanelle opens at the tip of the projection (full hexagon with empty circle), or at its base (full hexagon). Greyed shapes indicate that both trait states occur within the considered subfamily. Diagnostic features for all subfamilies are extensively presented in Supplementary Figs. 1–18. Soldier pictures, from left to right: (1) Microcerotermes sp. (Microcerotermitinae); (2) Termes fatalis (Termitinae); (3) Silvestritermes heyeri (Syntermitinae), (4) Genuotermes spinifer (Syntermitinae); (5) Nasutitermes sp. (Nasutitermitinae). Picture credits: M. M. Rocha (4); R. H. Scheffrahn (2,3); J. Šobotník (1,5).