The scope for nuclear selection within Termitomyces fungi associated with fungus-growing termites is limited

Abstract

BackgroundWe investigate the scope for selection at the level of nuclei within fungal individuals (mycelia) of the mutualistic Termitomyces cultivated by fungus-growing termites. Whereas in most basidiomycete fungi the number and kind of nuclei is strictly regulated to be two per cell, in Termitomyces mycelia the number of nuclei per cell is highly variable. We hypothesised that natural selection on these fungi not only occurs between mycelia, but also at the level of nuclei within the mycelium. We test this hypothesis using in vitro tests with five nuclear haplotypes of a Termitomyces species.ResultsFirst, we studied the transition from a mixture of five homokaryons (mycelia with identical nuclei) each with a different nuclear haplotype to heterokaryons (mycelia with genetically different nuclei). In vitro cultivation of this mixture for multiple asexual transfers led to the formation of multiple heterokaryotic mycelia, and a reduction of mycelial diversity over time. All heterokaryotic mycelia contained exactly two types of nucleus. The success of a heterokaryon during in vitro cultivation was mainly determined by spore production and to a lesser extent by mycelial growth rate. Second, heterokaryons invariably produced more spores than homokaryons implying that homokaryons will be outcompeted. Third, no homokaryotic ‘escapes’ from a heterokaryon via the formation of homokaryotic spores were found, despite extensive spore genotyping. Fourth, in contrast to most studied basidiomycete fungi, in Termitomyces sp. no nuclear migration occurs during mating, limiting the scope for nuclear competition within the mycelium.ConclusionsOur experiments demonstrate that in this species of Termitomyces the scope for selection at the level of the nucleus within an established mycelium is limited. Although ‘mate choice’ of a particular nuclear haplotype is possible during mating, we infer that selection primarily occurs between mycelia with two types of nucleus (heterokaryons).

Fungal evolution: cellular, genomic and metabolic complexity

“…In most cases, the fungus controls nuclear division tightly by forcing synchronization through clamp connections (Shepherd, Orlovich & Ashford, ; Iwasa, Tanabe & Kamada, ; Maheshwari, ; Raudaskoski & Kothe, ). Even so, nuclear competition and population dynamics have been described and studied in Heterobasidion (Garbelotto et al ., ; James et al ., ; James, Johansson & Johannesson, ; Garbelotto & Gonthier, ; Giordano et al ., ) and Termitomyces (Nobre et al ., ). Arbuscular mycorrhizal fungi also seem to show high levels of heterokaryosis in nature (Bever & Wang, ; Boon et al ., ; Wyss et al ., ; Mathieu et al ., ), forming nuclear populations that are mantained over time through the production of highly multinucleated spores (Bever & Wang, ; Jany & Pawlowska, ; Chagnon, ; Boon et al ., ).…”

“…In Eremothecium , however, nuclear migration is mediated by the cytoskeleton (Gladfelter, ; Anderson et al ., ; Dundon et al ., ; Gibeaux et al ., ). The ability to transport nuclei from distant regions in the network would provide a steady supply of nuclei, maintaining directed growth even if comparatively less‐fit nuclei are present, as is likely to be the case to some degree in any nuclear population (Nobre et al ., ; Anderson et al ., ). It is important to mention here that, despite cytoplasm continuity, nuclei seem to control cytoplasmic territories with considerable autonomy, a situation also known as ‘cells within cells’ (Nair et al ., ; Roper et al ., , ; Anderson et al ., ; Roberts & Gladfelter, ).…”

Multilevel Selection in the Filamentous AscomyceteNeurospora tetrasperma

“…This result is in accordance with previous reports on biased nuclear ratios in N. tetrasperma (Samils et al 2014) and in two basidiomycete species for which mating type nuclei are not constrained to propagate together, Heterobasidion parviporum (James et al 2008) and Termitomyces sp. (Nobre et al 2014). Here we further show that in N. tetrasperma, nuclear ratios can depart from evenness in the mycelium even when controlling the inoculum to be 1∶1 (figs.…”

Unholy marriages and eternal triangles: how competition in the mushroom life cycle can lead to genomic conflict

“…Heterobasidion annosum , H. parviporum , Pholiota microspora ( Pholiota nameko ) [ 32 , 36 , 38 – 40 ]). By contrast, in Termitomyces , another basidiomycete fungus with multiple nuclei per cell, no monokaryotic escapes have been found [ 41 ]. Similarly, in some of the mutualistic fungi cultivated by fungus-growing ants, multiple nuclei are present in each cell.…”