Major alteration of the expression site of endogenous cellulases in members of an apical termite lineage

Termites are among the most important cellulose‐digesting animals on earth, and are well‐known for the symbiotic relationship they have with cellulolytic trichomonad and oxymonad flagellates (unicellular eukaryotes). Perhaps less well‐known is the fact that ∼75% of the ∼2600 described termite species — those belonging to the family Termitidae — do not harbour such flagellates. Unlike most termites from other families, the majority of termitids do not consume wood, feeding instead on soil, leaf litter, fungi, grass, or lichen. Recent years have seen the characterization of the endogenous cellulase enzymes that help termites digest cellulose, from one flagellate‐harbouring species (Reticulitermes speratus), as well as one termitid (Nasutitermes takasagoensis). The genes encoding the enzymes in these two termites are similar. However, their site of expression differs markedly — the salivary glands in R. speratus and the midgut in N. takasagoensis. To investigate this difference further, we performed a comparative study of cellulase expression in various termitid and flagellate‐harbouring species, using enzyme assays and reverse transcription polymerase chain reactions. Taxa from phylogenetically basal lineages were consistently found to express endogenous genes specifically in the salivary glands, whilst those from a relatively apical lineage containing termitids expressed cellulases solely in the midgut. Relatively low levels of cellulase activity were found in nonwood‐feeding species, while the wood‐feeding Coptotermes formosanus— arguably the most destructive pest species world‐wide — was found to have high levels of activity in all parts of the gut when compared to all other termites. In the light of these results, as well as recently accumulated phylogenetic data, we discuss scenarios for the evolution of cellulose digestion in termites.