A look at the latest research on the origins of termites, including their classification and the termite/gut symbiont relationship.
Latest termite evolution research
Lower termites and higher termites – is this terminology correct?
Most people involved in termite management will have heard the terms ‘lower termites’ and ‘higher termites’. But do you know what these terms refer to? Well, don’t rush out to brush up on your termite terminology just yet, as a number of leading termite researchers are suggesting we drop this dated terminology altogether.
The terms ‘lower’ and ‘higher’ generally refer to the position of the termite species on the perceived evolutionary pathway, with the older, more primitive species being labelled lower termites and the more recently evolved species labelled higher termites. Lower termites include Mastotermes, drywood termites, dampwood termites and Rhinotermitidae (Coptotermes, Heterotermes, Schedorhinotermes and Reticulitermes) as well as others. Higher termites include Macrotermitidae, (fungus-growing termites), Nasutitermes and Microcerotermes amongst others.
More specifically, this means that the higher termites include the entire Termitidae family, which have lost their flagellated protist symbionts; all the other termites, which retained their dependence on eukaryotic symbionts in their hindguts for cellulose digestion, are labelled lower termites. The researchers believe the terms ‘lower’ and ‘higher’ create an unhelpful perception as to the biology of the individual species and indeed with such a large variation between the different species within each group, the groups are too broad in any case.1
The researchers suggest dropping the term higher termites and replacing it with ‘Termitidae’ or the common name ‘Termitids’, as this group is fairly well defined. However, the large variation between the species within the lower termites is such that they suggest not grouping them together at all. The only exception would be when referring to their symbionts, when they could be called ‘protist-dependent termites’ or ‘non-Termitidae termites’.
Identifying Termite Species is Difficult – There May Be More Than You Think!
Reticulitermes species are one of the key termite pests in the western United States, with the recognised species present being R. hesperus and R. tibialis. However, differences in behaviour, particular swarming times, genetics and cuticular hydrocarbon profiles, suggested that R. hesperus itself may comprise two or more species. To gain further understanding, researchers have completed a comprehensive analysis of a large number of Reticulitermes samples collected in California.2
The research determines that in fact at least five species of Reticulitermes are present, of which three are undescribed. With no reliable definitive morphological characteristics to differentiate these species visually, it demonstrates the challenge in termite identification in the field. It is also likely that a similar scenario could exist for other pest species globally, whereby species identification based solely on visual characteristics may be misleading. This in turn could cause differences in behaviour to be labelled as variations within a species, rather than the behaviour of different species.
References
1 Carrijo, T.F et al. (2023). A call to termitologists: it is time to abandon the use of “lower” and “higher” termites. Insectes Sociaux (2023) 70:295–299. https://doi.org/10.1007/s00040-023-00929-0
2 Tseng, S-P. et al. (2023). Phylogenetic analyses of Reticulitermes (Blattodea: Rhinotermitidae) from California and other western states: multiple genes confirm undescribed species identified by cuticular hydrocarbons. Journal of Economic Entomology, 116(6): 2135–2145. https://doi.org/10.1093/jee/toad182
Where do Coptotermes sit?
Classification of termites is somewhat problematic. Indeed, it was not until relatively recently that it was agreed that termites had evolved from an ancient line of cockroaches. For the Rhinotermitidae, the family of lower termites which includes many of the economically important subterranean termites, the classification challenges remain. Currently the family includes six generally accepted sub-families, 12 genera and 335 species. However, due to the wide-ranging morphological differences between the species, there is ongoing debate and research as to the relatedness of the species.
Typically termites have been split into lower termites and higher termites, based on their differences in gut symbionts, feeding behaviour, colony structure and development pathways. Although Coptotermes species have typically been classified as lower termites, as they still possess protozoa symbionts, they display many higher termite behaviours.
Researchers have recently reviewed ten species of the lower termite genera, including Coptotermes, Reticulitermes, Heterotermes and Schedorhinotermes and compared their morphologies and mitochondrial genes to various higher termite species.1 Their findings suggested that although Heterotermes and Reticulitermes are currently classified under the Heterotermitinae sub-family, Heterotermes appear to be more closely related to Coptotermes.
However, generally speaking the Heterotermitinae and Coptotermitinae sub-families were more closely related to each other than to other sub-families in the Rhinotermitidae. And furthermore that this Coptotermitidae-Heterotermitinae clade is actually more closely related to the higher termites (Termitidae) than to the other sub-families of the Rhinotermitidae. As such they should be considered the more evolved clade in the Rhinotermitidae family and consequently seen as a separate family. The genetic analysis supports the behavioural observations that Coptotermes (and Heterotermes) do indeed sit between lower and higher termites.
Eusociality and termite hygiene
One of the key steps in the evolution of termites was the move from nesting and foraging in dead wood to developing a central nest and foraging outside the nest for food. This change in behaviour meant termites needed protection from the large number of harmful microbes they encounter in the soil. Researchers have established that this protection was delivered by a range of social grooming and hygiene behaviours, which included the secretion of salivary enzymes that are particularly effective in dealing with the common and deleterious Metarhizium fungus.2 As this behavioural benefit of eusociality delivered hygiene benefits, the selection pressure on internal (innate) components of the immune system decreased.
References
1 Ke, Yunling & Huang, Fusheng & Wu, Wenjing & Li, Zhi-Qiang. (2021). Systematic Position of Heterotermitinae and Coptotermitinae (Blattodea: Isoptera: Rhinotermitidae). Journal of Entomological Science. 56. 10.18474/JES20-53.
2 Bulmer, Mark & Stefano, Alanna. (2022). Termite eusociality and contrasting selective pressure on social and innate immunity. Behavioral Ecology and Sociobiology. 76. 10.1007/s00265-021-03090-5.
Gut symbionts are integral to the success of termites as a group, enabling them to be one of the few groups of animals capable of successfully digesting cellulose. Ongoing studies have unravelled some of the mysteries of this symbiotic relationship and its role in the evolution of termites.
Evolution in lower termites
Lower termites are more ‘primitive’ termites and include Mastotermes as well as the dampwood and drywood termites. The Rhinotermitidae are also classed as lower termites, but they are a more recent evolution, exhibiting some higher termite behaviours.
The gut symbionts in termites die prior to the termite moulting. So how are these gut symbionts retained within a termite population and how did such a relationship evolve? Christine Nalepa from North Carolina State University in the US has proposed a new hypothesis.1
Lower termites and their closest living cockroach ancestor, the sub-social wood-feeding cockroach Cryptocercus, both contain flagellate eukaryotic protists as their gut symbionts to aid with the digestion of wood. In Cryptocercus these symbionts form cysts prior to the cockroach moulting. These cysts are viewed as an evolutionary artefact, with the flagellates in Cryptocercus having evolved from parasitic flagellates of gregarious cockroaches, which form cysts to be passed in faeces and subsequently ingested by other cockroaches.
However, in Cryptocercus these cysts play no demonstrable role in the transmission of flagellates between nestmates and between generations. Instead the gut symbionts are passed directly from parents to offspring through feeding on hindgut secretions (proctodeal trophallaxis).
The hypothesis proposes that it was the change in behaviour in ancient social cockroaches, in moving from coprophagy to proctodeal feeding, that was critical in the development of the termite lineage. Not only did this accelerate parental care and increased social behaviour, but it also drove the evolution of the flagellates from a parasitic relationship to a mutualistic one.
Evolution of higher termites
Higher termites, the Termitidae, consist of the most recent species from an evolutionary point of view, including Microcerotermes and Nasutitermes.
Whilst lower termites rely on symbiotic protists to digest wood, higher termites (Termitidae) lack these flagellates altogether. With 70% of termite species being in the Termitidae family, the loss of protists is seen as a major evolutionary step in the development of termites. Instead of protists, higher termites have a range of bacteria and other gut symbionts to aid with digestion. Researchers believe that this change in gut symbionts drove this speciation through variation in diet, behaviour and morphology, allowing higher termites to utilise a wider range of niches.2
Although the mechanisms that drove this evolution remain speculative, a review paper on the subject provides two drivers for the evolution of the higher termites. Although lower termites feed primarily on wood, 85% of higher termites are classed as soil feeders, feeding on rotten wood and decomposed vegetable matter in the soil. By switching to a soil diet it would have starved the specialist protist symbionts of their source of cellulose and therefore eliminated them from the gut.
However, within the higher termites there are two groups of wood feeders – the Macrotermitinae and Sphaerotermitinae – which have also lost their cellulose digesting protist. They manage to ‘digest’ the wood outside of their bodies using fungi (Termitomyces) in the case of Macrotermitinae (main picture, above) or bacterial combs in the case of Sphaerotermitinae.
It’s not known which of these developments occurred first or whether they occurred independently, but they certainly provided the platform for the diversification and success of the higher termites.
References
1 Nalepa, C.A., 2020. Origin of Mutualism Between Termites and Flagellated Gut Protists: Transition From Horizontal to Vertical Transmission. FRONTIERS IN ECOLOGY AND EVOLUTION 8. https://doi.org/10.3389/fevo.2020.00014
2 Chouvenc, T., Sobotnik, J., Engel, M.S., Bourguignon, T., 2021. Termite evolution: mutualistic associations, key innovations, and the rise of Termitidae. CELLULAR AND MOLECULAR LIFE SCIENCES 78, 2749–2769. https://doi.org/10.1007/s00018-020-03728-z
Further reading:
How did termites spread across the world as they started to evolve?
How did the termite gut microflora develop as termites evolved?
