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  1. Evaluation Summary:

    Unions between equal partners can be destabilized by matings with third parties. In this paper the authors demonstrated that in fungi, 'stable unions' of two nuclei (dikaryons) are predicted to experience costs to vegetative fitness from investment in such mating opportunities. 'Open unions', in which third parties have access to the resources of established partnerships, are evolutionarily highly unstable. This paper will be of general interest to those who study evolutionary conflicts and to fungal geneticists.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their name with the authors.)

  2. Reviewer #1 (Public Review):

    Auxier et al. investigate the evolutionary dynamics of nuclear level selection in dikaryons of basidiomycete fungi. This research aims at clarifying a long-standing problem in fungal genetics, namely the evolutionary significance of dikaryons, the mysterious but dominant nuclear arrangement of the zygobiotic (2N) phase in basidiomycete fungi. This arrangement occurs when the mated mycelium maintains the nuclei of the two mates in a spatially distinct, but paired, arrangement through numerous cell divisions before production of a fruiting body. The alternative is that the mated mycelium would be diploid, like most eukaryotes, but evidence for such a system is limited to a few examples. In most basidiomycetes, the gamete is the haploid nucleus, and therefore the standard dikaryotic condition maintains the potential for remating through dikaryon-monokaryon matings, and in this research, it is this particular difference that the authors focus on modeling. Another curious phenomenon that is related to the basidiomycete life cycle is that dikaryon-dikaryon pairings inevitably result in rejection and no mating, thus creating a concept that the dikaryon is individualistic and cannot be invaded. What would happen if that assumption was relaxed?

    Here the authors develop an agent-based model to test how nuclear behaviors in mated mycelia can influence selection for allocation to fitness components and population fitness. The authors contrast three distinct nuclear behaviors (diploid, standard dikaryon, and open dikaryon [scenario of constant somatic reassortment]) under a number of parameters. Importantly, they model tradeoffs between reproductive and vegetative traits (mycelial growth, mating, and sporulation). The general findings were that with the dikaryotic life cycles, populations often become heavily biased towards nuclei that behave selfishly (also referred to as parasitic) in that they maximize their own fitness to the detriment of the total population (as measured by population size). In the case of the open dikaryon, the population crashes under most conditions. The key parameter for stability of most of the simulations has to do with lambda, the number of fitness related loci.

    The conclusions of the paper are supported by the data, and the authors have done a good job of incorporating important aspects of the biology of the system into the paper. This will be a paper that impacts the field because it will be a touchstone for the numerous researchers who wonder about the subject. Perhaps the most important insight is that the individualistic behavior of dikaryotic mycelia is required to prevent the system from collapsing due to selfish nuclei; this individualistic behavior is incredibly well supported across many mushroom species. Some aspects of the paper left me quite intrigued.

    1. Much of the paper rests on the effects of the number of fitness related loci. Yet, fitness is a complicated phenotype comprised of multiple aspects of vegetative growth, sporulation, mating ability etc. Much of the stability only comes when the fitness phenotypes are inherited as a single unit. I feel that the actual model is weak in terms of what these fitness loci represent, given that clearly vegetative growth is never going to be determined by a single Mendelian locus. The authors should clarify and speak consistently about what lambda represents. How lambda influences the updating algorithm could also be better explained. Despite this weakness, this model can improve our intuition that reconciling these tradeoffs can be accomplished if they become manifested as alternative extreme strategies controlled by a single large locus as observed in the outcome of the simulations.

    2. I think this spatially explicit model is very useful, because capturing the underlying dynamics of a di-mon mating requires this spatial consideration. I wonder, however, how spatial heterogeneity might influence the outcome. If resources were distributed unevenly in space, it might favor genotypes that invested more in reproduction over mating as there may be dispersal limitations. I also am interested in what would happen if you incorporated size of a dikaryotic/diploid mycelium in reproductive output. It might be that you get a strong positive relationship between the two. I can imagine that a selfish nucleus could invade into recipient mycelium and establish a dikaryotic genotype, but then not actually have enough resources to reproduce sexually. It is interesting that in this context, the less promiscuous diploid fungus Armillaria is also the one known to have the largest sized individuals.

    3. As mentioned, I think the authors have done a good job of infusing realism into their model. I think it would help to add a general discussion about what factors might favor or at least permit a diploid system to emerge given that such systems exist. Another way of thinking about this would be whether a system of a standard dikaryon could be invaded by a mutation leading to diploidy; or conversely in the diploid system if a mutation led to dikaryons (exploring both cases of recessive and dominance of mutations) could be informative.

  3. Reviewer #2 (Public Review):

    The fungal mycelium is a habitat, or 'constructed niche', within which nuclei live. Nuclei from an existing dikaryon can mate with another monokaryon, to form new dikaryotic partnerships, but there are 'self-incompatibility' barriers that prevent new nuclei entering existing dikaryons.

    Auxier, Czaran and Aanens paper reports evolutionary simulations of mating behavior in basidiomycete fungi. Nuclear types in fungal dikaryons benefit from retaining the ability to form new dikaryons with monokaryons that are encountered but this has costs for the fitness of existing dikaryons. (Three fitness components-mycelial growth rate, production of meiospores by dikaryons, mating fitness-were subject to mutation. The re-normalization of fitness components after mutation ensured that there was a trade-off among the fitness components.) In the simulations in which new matings were allowed between existing dikaryons, there was a rapid collapse of fitness because of high investment in extra matings.

    The paper presents an advance in our understanding the complex evolutionary forces acting in the 'Buller phenomenon' (matings between monokaryons and dikaryons). These forces are complex and analytically intractable (For example, cubics of gene frequencies appear as soon as one has three partners). The authors approach this problem by simulations. I have mixed feelings about simulations for complex, poorly understood, biological phenomena (you get out of them what you put into them; one must always leave out many of the complexities). Simulations are best thought of as a kind of experiment in which various factors are varied. The authors approach the simulation in this light as an exploration of possible underlying processes.