Research changes genealogical tree of termite species

Scientists raise important hypotheses about the evolutionary history of one of the most abundant groups of termites in Brazil.

By Maria Fernanda Ziegler  |  Agência FAPESP – To study termites is to study diversity. In contrast with what most people believe, termites are part of a highly diversified insect order, with some 3,000 species in the world and over 300 in Brazil alone. To the surprise of any lay person, only a small proportion – about 10% – are considered pests, and most do not feed on wood. 

A team of researchers at the University of São Paulo’s Zoology Museum (MZ-USP) in Brazil, who have studied termites for several years, recently caused an upset in the taxonomic classification of some termite species and reconstructed part of the evolutionary history of these insects.

The results were published in PLOS ONE. The study was supported by FAPESP through a research grant awarded to Eliana Marques Cancello, a researcher at MZ-USP, and a postdoctoral scholarship awarded to Maurício Martins da Rocha, whose research is supervised by Cancello.

The change to the termite genealogical tree resulted from a detailed study of soldier and worker morphology. The researchers found several cases of morphological convergence – where unrelated species evolve similar features – in the soldier caste, useful for taxonomic classification and always considered important for diagnostic purposes. On the other hand, the feeding habits of each species showed signs of evolutionary significance.

According to Rocha, the many convergences can be explained by the frequent use taxonomists made in the past of similarities in external morphology for classification purposes.

Before embarking on the study, they expected soldier morphology to reflect kinship among the many termite genera or species, so that a soldier caste with a sharply pointed mandible should be more closely related to species with similar traits than to others with serrated mandibles, for example. However, this was not what the researchers found.

Termites are currently divided into nine families. Termitidae is the largest and most diverse, with almost 2,000 described species. Termitidae in turn comprises eight subfamilies, among which Syntermitinae – with 18 genera and 101 species described to date – includes some of the most abundant species found in the wild in Brazil. An example is Cornitermes cumulans, which is especially important ecologically and considered a key species in the Cerrado (Brazilian savanna) biome.

The termites they studied in the subfamily Syntermitinae do not eat the wood of living trees. “These are the mound-building species that alter the landscape in fields and on farms. The giant mounds house their nests and contain a large amount of biomass, but they also reflect the termites’ importance to the soil, which undergoes chemical and physical changes as they turn it over. Their mounds also serve as shelters for other termite species, other arthropods, snakes and even birds, which use the mounds to mark their territories,” said Cancello, curator of the Zoology Museum’s Isoptera collection.

By cross-referencing data on 92 taxonomic characters in 42 species of Syntermitinae and six species of Termitinae (another termite subfamily), the researchers changed the scientific understanding of these insects of the order Isoptera and reclassified their species.

In addition to an analysis of their external anatomy (thorax, mandibles etc.) and of their internal anatomy, especially the digestive tube in soldier and worker castes, 117 DNA sequences were also analyzed. This required field surveys to collect specimens of species underrepresented among the 28,000 lots stored in the Zoology Museum, which holds the largest termite collection in South America.

In order to be able to sift through such a huge mass of data, the researchers combined the morphological and molecular data in Bayesian inference analyses, in which uncertainties about quantity are expressed in terms of probability. The key aspects of termite biology, defense and feeding habits were discussed on the basis of the phylogenetic tree.

“During my PhD research I revised the genus Armitermes, which we almost made ‘extinct’ in South America,” Rocha told Agência FAPESP. “Studying the anatomy of all the species classified as Armitermes in greater depth, I found that most of them had striking differences in internal anatomy, although their soldiers were similar externally. As a result, I had to reallocate most of them to new genera.”

Rocha is currently doing postdoctoral research in which he has extended the analysis to other genera in the subfamily Syntermitinae and is analyzing them phylogenetically in order to reconstruct the evolutionary history of these insects.

The secret life of termites

The study showed that in the evolutionary history of Syntermitinae, a very early split occurred between lineages that feed on non-humified material (organic resources that have not decomposed), such as dead grass and wood, and those that feed on very humified plant material, such as rotten wood, humus and the mounds of other termites, which are mostly made of stercoral material – a mixture of soil, saliva and dung.

According to the researchers, this change in diet must have been reflected not just in the shape of the workers’ mandibles but also in their digestive apparatus and in the complex fauna of associated symbionts.

“There are classifications within these kinds of behavior, and it’s important to try to understand them in terms of evolution,” Cancello said. “Might these insects have originally had a single specific diet and then begun diversifying?”

The researchers concluded that Syntermitinae belong to a more recent lineage of the termite’s evolutionary history. “The evidence suggests the group diversified when South America had already broken away from the other continents, during the Oligocene [between 36 million and 23 million years ago], but there are no fossils to study. For example, Crato [a paleontological site in Ceará State] dates from the Cretaceous [between 145 million and 66 million years ago], when these termites didn’t exist,” Cancello said.

Digestive compartmentalization

During their analysis, the researchers discovered several structures that had never been described.

“The digestive tube in termites is fairly compartmentalized,” Rocha said. “One of the compartments is the gut, which houses the symbionts that aid digestion, but there are other compartments whose role in digestion isn’t well understood. We found highly diversified ornamentation never previously described on the walls of one of these other compartments.”

The ornaments were not identical in all species. “They must have something to do with digestion, but although we don’t understand their function, we can compare them morphologically and use them to refine kinship relations. We can reconstruct termite phylogeny based on fine anatomical details such as these, instead of relying on intuition,” Rocha said.

The article “Phylogenetic reconstruction of Syntermitinae (Isoptera, Termitidae) based on morphological and molecular data” by Mauricio M. Rocha, Adriana C. Morales-Corrêa e Castro, Carolina Cuezzo and Eliana M. Cancello can be read at doi.org/10.1371/journal.pone.0174366.