Nuclear arms races: Experimental evolution for mating success in the mushroom-forming fungus Schizophyllum commune

Abstract

When many gametes compete to fertilize a limited number of compatible gametes, sexual selection will favour traits that increase competitive success during mating. In animals and plants, sperm and pollen competition have yielded many interesting adaptations for improved mating success. In fungi, similar processes have not been shown directly yet. We test the hypothesis that sexual selection can increase competitive fitness during mating, using experimental evolution in the mushroom-forming fungus Schizophyllum commune (Basidiomycota). Mating in mushroom fungi occurs by donation of nuclei to a mycelium. These fertilizing ‘male’ nuclei migrate through the receiving ‘female’ mycelium. In our setup, an evolving population of nuclei was serially mated with a non-evolving female mycelium for 20 sexual generations. From the twelve tested evolved lines, four had increased and one had decreased fitness relative to an unevolved competitor. Even though only two of those five remained significant after correcting for multiple comparisons, for all five lines we found a correlation between the efficiency with which the female mycelium is accessed and fitness, providing additional circumstantial evidence for fitness change in those five lines. In two lines, fitness change was also accompanied by increased spore production. The one line with net reduced competitive fitness had increased spore production, but reduced fertilisation efficiency. We did not find trade-offs between male reproductive success and other fitness components. We compare these findings with examples of sperm and pollen competition and show that many similarities between these systems and nuclear competition in mushrooms exist.

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

“…First, experimental evolution may provide the experimental tests of theoretical predictions, and some progress has recently been made (cf. [ 48 , 61 ]). Second, due to progress in genetic and genomic techniques, the possibilities of studying natural populations and non-model organisms will increase (cf.…”

“…R. Soc. B 371: 20150533 but generally no clear trade-offs were found with other fitness components, such as growth rate [48].…”

“…However, the major force determining the selective advantage of a mutation leading to an increased male performance in di-mon matings is the—unknown—frequency of di-mon mating events in nature. Using experimental evolution in S. commune for increased male fertility, increased male mating success could be selected, but generally no clear trade-offs were found with other fitness components, such as growth rate [ 48 ].…”

Sex, senescence, sources and sinks

“…Highly intriguingly, this is true for all forms of multicellular life only if we stretch the definition of a life cycle to the end of a long period of vegetative growth, budding, etc., that can all occur before a lineage forms gametes (as an extreme example, the ability to produce sperm has become a rather pointless trait for an invasive sea star that, via asexual fissiparity, forms 100% male populations in the Mediterranean, Karako, Achituv, Perl-Treves, & Katcoff, 2002). Also, note that sex is not necessarily temporally aligned with the single-cell stage: in mushroom-forming basidiomycete fungi, fertilization is followed by further vegetative growth, and the production of haploid is an entirely different part of the life cycle (Nieuwenhuis & Aanen, 2018).…”

On conflict and resolution in the termite-fungus symbiosis

“…First, experimental evolution may provide the experimental tests of theoretical predictions, and some progress has recently been made (cf. Clark andAnderson 2004, Nieuwenhuis andAanen 2018). Second, due to progress in genetic and genomic techniques, the possibilities of studying natural populations and non-model organisms will increase (cf.…”