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The complexity of termite symbiotic relationships with fungi could hinder the control strategy against this insect pest

All species of termites are social insects, like ants. Entomologists have listed over 2000 species across the world and more than one-third of them live in Africa. This continent harbours 160 from the subfamily Macrotermitinae.

Contrary to other termites, the species of this subfamily-cannot digest either cellulose or lignin, basic constituents of their food plants, and therefore call on the services of a symbiotic relationship with a higher fungus.

Using roughly chewed and only slightly digested plant material, they make a small ventilated structure, the fungus comb or garden, on which the mycelium of a Termitomyces, a Basidiomycete fungus of the same family as the Lepiota, will grow. This fungus will gradually break down the ligneous and cellulose-bearing material amassed on the comb into substances that are easier for the termites to assimilate.

The entomologists focusing on these fascinating social insects have long considered the symbiotic relationship between the Macrotermitinae and the fungus Termitomyces was one of interaction specificity, in that one species of termite associated with a single species of fungus, following a system elaborated by co-evolution that began several tens of millions of years ago.

A study recently published by an international research team, jointly involving IRD scientists, brought proof that this symbiotic relationship is much more complex and diversified than was suspected.

With the aim of understanding better how the ties between the insect and the fungus are forged, samples of termites and associated Termitomyces were taken in South Africa and Senegal, from 101 colonies belonging to eight species divided over three different genera. Analysis of molecular variance using amplification and sequencing of highly variable genome sequences from the termites and fungi gave measurements of the level of symbiotic interaction between fungus and insect depending on hierarchical taxonomic level (genus, species, colony). Strong evidence of variability in the host-symbiont association emerged: it was high between genera, low between species and quite high between colonies of the same species.

Among the different species studied, only the termite Macrotermes natalensis established a symbiotic relation specificity with a single fungus species, whatever the colony investigated. In contrast, the three termite species of the genus Odontotermes are capable of growing several different species of Termitomyces. Further, bilaterally low specificity was found in the other species of the genus Microtermes, where several different termite species were associated with a variety of fungi. This confirmed therefore that, in most cases, no co-evolution occurred in the symbiotic relationship which brought the fungus into interaction with the termite.

The secret of this diversification could lie in Termitomyces’ capacity for fructification through fruiting bodies. The investigators advanced the hypothesis that this element of a fungus, which develops from the mycelium then reaches the surface, where it forms its visible part, would render the organism retrievable by termites from another colony which would take it back to their nest to establish a new growth site. The results indicate strongly that, rather than an intergenerational transmission mode, like the one found in fungus-growing ants, a process of horizontal transmission operates between of the same given fungus between many different colonies of termites, whether or not the latter belong to the same species.

Seeing that in Africa 90% of crop damage perpetrated by termites is the work of fungus-growing species, better understanding of the transmission mode of the symbiont fungus in these insect hosts is essential. The termites of the genus Odontotermes, which this study showed to have an aptitude for growing a variety of Termitomyces species, can for example cause yield losses of 25% in a field of sugar cane. In the northern areas of Cameroon, other species attack subsistence farmers’ staple crops of millet and sorghum. The latest control strategies implemented for limiting damage caused by these pests now target the fungus rather than the termite. By replacing insecticide by fungicide, these new methods thus employ a substance less harmful for humans. Nevertheless, these insects’ quite low interaction specificity, making them capable of growing diverse species of fungi, could keep them a step ahead of the fungicide control methods and thus hinder this new approach to termite control.

Grégory Fléchet | alfa
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