The Evolutionary History of Termites as Inferred from 66 Mitochondrial Genomes

Abstract

Termites have colonized many habitats and are among the most abundant animals in tropical ecosystems, which they modify considerably through their actions. The timing of their rise in abundance and of the dispersal events that gave rise to modern termite lineages is not well understood. To shed light on termite origins and diversification, we sequenced the mitochondrial genome of 48 termite species and combined them with 18 previously sequenced termite mitochondrial genomes for phylogenetic and molecular clock analyses using multiple fossil calibrations. The 66 genomes represent most major clades of termites. Unlike previous phylogenetic studies based on fewer molecular data, our phylogenetic tree is fully resolved for the lower termites. The phylogenetic positions of Macrotermitinae and Apicotermitinae are also resolved as the basal groups in the higher termites, but in the crown termitid groups, including Termitinae + Syntermitinae + Nasutitermitinae + Cubitermitinae, the position of some nodes remains uncertain. Our molecular clock tree indicates that the lineages leading to termites and Cryptocercus roaches diverged 170 Ma (153-196 Ma 95% confidence interval [CI]), that modern Termitidae arose 54 Ma (46-66 Ma 95% CI), and that the crown termitid group arose 40 Ma (35-49 Ma 95% CI). This indicates that the distribution of basal termite clades was influenced by the final stages of the breakup of Pangaea. Our inference of ancestral geographic ranges shows that the Termitidae, which includes more than 75% of extant termite species, most likely originated in Africa or Asia, and acquired their pantropical distribution after a series of dispersal and subsequent diversification events.

Oceanic dispersal, vicariance and human introduction shaped the modern distribution of the termitesReticulitermes,HeterotermesandCoptotermes

“…In this study, we confirmed the relationship pattern and dating of the three genera as found in earlier molecular studies [10,15,25,37]. We found that the split between Reticulitermes and Heterotermes þ Coptotermes occurred around 59 Ma (49.9 -69.5 Ma 95% CI), the most recent common ancestor of the clade Heterotermes þ Coptotermes arose 36 Ma (33.9 -40.5 Ma 95% CI), and Coptotermes split from sister Heterotermes species around 24.5 Ma (21.0 -27.8 Ma 95% CI).…”

The complete mitochondrial genomes of the higher termitesLabiotermes labralisandEmbiratermes neotenicus(Termitidae: Syntermitinae)

“…The original metagenomic dataset of Embiratermes neotenicus consisted of 209,047,724 raw reads, from which 269,723 mitochondrial reads were recruited and assembled into one circular contig of 15,868 bp, with an average coverage of 2418-fold, an asymmetric nucleotide composition (42.5% A, 21.6% C, 12.1% G, 23.8% T) and an overall G þ C content of 33.7 mol% (accession number KY436202). These values are consistent with the length and nucleotide composition of other higher termite mitogenomes (Bourguignon et al 2015;Dietrich & Brune 2016).…”

“…In both cases, the gene order and orientation were identical to those of other termites, which have retained the organization of the ancestral insect mitochondrial genome (Cameron 2014). Phylogenetic analysis of protein-coding sequences yielded the same tree topology for the Syntermitinae subfamily as previously reported by Bourguignon et al (2015) using partial mitochondrial genomes of Labiotermes labralis and Embiratermes neotenicus generated by PCR amplification and Illumina sequencing (Figure 1). …”

“…The number of available arthropod mitogenomes, especially from insects, has greatly increased during the last decade (Cameron 2014). The genomic information contained in these mitogenomes not only allows inference of phylogeny and evolutionary history of insects, such as termites, with a unprecedented resolution (Bourguignon et al 2015), but also provides a phylogenetic framework for monitoring arthropod biodiversity in soils with high-throughput DNA sequencing approaches (And ujar et al 2015;Crampton-Platt et al 2015).…”

Hemimetabolous genomes reveal molecular basis of termite eusociality

“…A particularly striking case of convergent evolution occurred within the holometabolous Hymenoptera and in the hemimetabolous termites (Isoptera), which are separated by over 350 Myr of evolution 5 . Termites evolved within the cockroaches around 150 Myr ago, towards the end of the Jurassic period 6,7 , about 50 Myr before the first bees and ants appeared 5 . Therefore, identifying the molecular mechanisms common to both origins of eusociality is crucial to understanding the fundamental signatures of these rare evolutionary transitions.…”