Open relationships in the castles of clay: high diversity and low host specificity of Termitomyces fungi associated with fungus-growing termites in Africa

Abstract

In the African and Asian tropics, termites of the subfamily Macrotermitinae play a major role in the decomposition of dead plant material. Their ecological success lies in the obligate mutualism of the termites with fungi of the genus Termitomyces. Before the advent of molecular studies, the interaction with these fungi was poorly understood. Here, we combined available ITS sequence data from West, Central, and South Africa with data of 39 new samples from East Africa to achieve the most comprehensive view of the diversity and host specificity of Termitomyces symbionts across Africa to date. A high amount of sequence divergence in the ITS sequences was found; 11 different Termitomyces lineages in East Africa and[30 lineages across Africa were identified, and the expected diversity is estimated to be about 41 lineages. The fungal lineages belong to four major clades, each almost exclusively associated with one termite host genus. Analysis of molecular variance revealed that 40% of the ITS sequence variation occurred between host genera, indicating close co-evolution at this level. However, within host genera, fungal lineages and haplotypes were frequently shared among host species and sampling localities, except for fungal symbionts of Odontotermes. Horizontal transmission of fungal symbionts may facilitate the transfer of haplotypes and species among hosts. However, at present, we have little understanding of the maintenance of specificity at the genus level. Possible explanations range from substrate specificity of fungi to an active selection of fungi by termites.

Diversity of Termitomyces Associated with Fungus-Farming Termites Assessed by Cultural and Culture-Independent Methods

“…compared to the larger termite diversity would suggest the association of relatively small number of Termitomyces species with their hosts [4]. But a hidden species diversity of Termitomyces has been postulated [6] since formal taxonomic descriptions of novel species are based on fruiting bodies, which are rarely found and might not even be formed at all by some Termitomyces lineages [7]. The application of ITS rDNA (internal transcribed spacer region of the ribosomal DNA) sequencing, a locus that has recently been proposed as universal fungal barcoding gene [8], evidently yields much higher diversity estimates [6], even though such sequence-based estimates are dependent on the applied distance threshold and clustering algorithm [9], [10].…”

“…Multiple interactions between termites and their fungal symbionts were reported to occur at the genus level [4], [6], [11]. Using DNA sequence analyses, one study [4] found congruence in the cladogenesis of the fungal symbionts and the termite hosts.…”

“…For example, five termite genera were broadly associated with particular cryptic Termitomyces species. However, relationships between lineages of fungi and termites are complex [4], [6], [11], [12]. Termite host switching of the fungi was observed, and that a single termite species can associate with a variety of Termitomyces species [13].…”

Diversity, population genetics, and evolution of macrofungi associated with animals

“…Horizontal transmission occurs when worker termites forage fungal basidiospores and establish new nests. The horizontal pattern can facilitate transmission of fungal haplotypes and species among hosts (Osiemo et al 2010), creating opportunities for mating and recombination. Indeed, evidence for recombination among populations was found in investigations of Macrotermes natalensis and its Termitomyces fungi (De Fine Licht et al 2006) and our studies in Yunnan, China (unpublished data) (Table1).…”

“…Evidence for the dominant role of horizontal transmission of Termitomyces genotypes has been found in sequence analyses of Termitomyces . For example, Osiemo et al (2010) found that there were 41 Termitomyces lineages in Africa and that only 40% of the internal transcribed spacer (ITS) sequence variations were due to the separations based on host genera. The remaining 60% of sequence variations were found within individual host genera.…”