Open Access Highly Accessed Research article

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

Tania Nobre13*, Bertha Koopmanschap1, Johan JP Baars2, Anton SM Sonnenberg2 and Duur K Aanen1

Author Affiliations

1 Laboratory of Genetics, Wageningen University and Research Center, Droevendaalsesteeg 1, Radix West, Building 107, 6708 PB Wageningen, The Netherlands

2 Plant Research International – Mushrooms, Wageningen University and Research Centre, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands

3 Currently: ICAAM, University of Évora, Pólo da Mitra Apartado 94, 7002-554 Évora, Portugal

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BMC Evolutionary Biology 2014, 14:121  doi:10.1186/1471-2148-14-121

Published: 5 June 2014

Abstract

Background

We 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.

Results

First, 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.

Conclusions

Our 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).

Keywords:
Termitomyces; Ploidy; Polyploid; Levels of selection; Social evolution; Mutualism; Fungi; Mating system