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Thus, barring the narrow zone of interaction where the cells fuse, there is no exchange of mitochondria. Second, unlike the vast majority of sexual organisms, upon fertilization, the nuclei do not fuse, but remain separate in each cell of the dikaryon. Consequently, sex in basidiomycetes is separated in time from gamete fusion, which is in contrast to almost all other sexual life cycles. Third, although the dikaryon cannot be fertilized by a second haploid nucleus, it retains the potential to donate nuclei to another monokaryon [ 7 , 8 ].

We systematically explore the potential for genomic conflict in this life cycle and discuss empirical evidence for the theoretical predictions. Figure 1. The standard life cycle of mushroom-forming basidiomycetes is usually based on Schizophyllum commune , one of the best studied species of this group.

This species is obligatorily outcrossing, a reproductive system called heterothallism. In this life cycle, haploid spores germinate to form a monokaryon , a sterile hyphal network called mycelium , in which each cell contains a single haploid nucleus. Two monokaryons can fuse and if the mycelia are compatible, i.

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The nuclei migrate through the mycelium of their new partner without the exchange of cytoplasm and mitochondria. Once a migrating nucleus reaches the growing tip of the receiving monokaryon, it starts synchronous division with the other nucleus. From now on, these tip cells divide via an intriguing structure called a clamp connection , which ensures that each new fungal cell contains both nuclei.

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In most species, the dikaryon can live for many years and increase in size by mitotic divisions. Certain environmental stimuli can trigger the formation of the sexual fruiting bodies called mushrooms. These fruiting bodies mostly consist of dikaryotic hyphae. Only in specialized cells called basidia , does sex occur, i. The four haploid products of meiosis each go into individual spores, which are dispersed in the environment once they reach maturity.

In homothallic species, selfing occurs, so that a single sexual spore on its own can form fruiting bodies and basidiospores. What are the male and female gametes in the basidiomycete life cycle [ 9 ]? The answer to this question is important, since it is one of the determinants for genomic conflict. Ultimately, the donated nuclei are the male gametes as these fertilize the monokaryon without prior investment in growth.

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It is less obvious what the female gamete is. Alternatively, as each cell of the monokaryon can be fertilized, the monokaryon can also be considered as a sexual organ and each of its cells as a female gamete. This is not just a theoretical argument, since a single monokaryon can be fertilized by multiple genetically different nuclei, from multiple monokaryons [ 10 ].

However, since the monokaryon exhibits both a female and male role, i. So in essence, each cell of the monokaryon can behave as a female gamete and each nucleus as a male gamete. Although the monokaryon needs to accept another nucleus to become fertilized and reproduce sexually, by doing so it exposes itself to risks and potential costs. If the resulting dikaryon is poorly functioning, the cost is borne by the receiving monokaryon, which contributed the cytoplasm, and which now has decreased or even lost its chance to reproduce.

One example would be the invasion of selfish nuclei, which might take over the cytoplasm and eliminate the original nucleus.

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An observation in spore-trap experiments indicates that this might happen in Schizophyllum commune [ 11 ]. Also, in the genus Armillaria , it has been shown that there can be hostile takeovers of one nucleus by a different one, although this is an exceptional genus as it has diploid nuclei [ 12 , 13 ]. Similarly, in pairings between selfing and outcrossing populations of the species Stereum hirsutum , replacement of the nucleus of the outcrossing population by a nucleus of the selfing population has been demonstrated [ 14 ].

Even without selfish elements, the new nucleus might carry genes that are not well adapted to the environment or not compatible with the original nucleus. This may render the dikaryon less adapted to the environment than the original monokaryon. However, by accepting another nucleus, and forming a dikaryon, the receiving nucleus enters into competition with the nucleus it just accepted for future success in di-mon matings. So there are two potential costs of accepting a nucleus. The first arises from accepting a nucleus that results in a maladapted dikaryon.

The second cost arises from accepting a more competitive nucleus that wins in the competition for di-mon fertilizations. Both costs should promote the evolution of female choice [ 10 , 16 ]. The male role of a monokaryon is the donation of nuclei to its mating partner. However, there are also other sources of male gametes. First, sexual spores can act as male gametes if they land on an established monokaryon [ 9 , 11 , 17 ]. The recognition of the various sources of male gametes has important implications for the opportunities for sexual selection, genomic conflict and the calculation of the cost of sex.

Since the dikaryon cannot receive another nucleus, a di-mon mating is equivalent to a mating between a male and a female. The hermaphroditic nature of pairings between two monokaryons can provide the conditions for the selection of ultra-selfish genes.

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As explained above, in the regular life cycle of mushroom-forming basidiomycetes, the monokaryon simultaneously donates and accepts another nucleus. By accepting another nucleus, a monokaryon dilutes its own genetic constitution, but compensates for this genome dilution by donating a nucleus to its partner monokaryon. Since this benefit is shared with all other genes of that nucleus, there is no genomic conflict at the level of the monokaryon see [ 18 ] for a more extensive discussion.

Figure 2. While the ratio of black and white genome after pairing has changed from 1 : 1 to 2 : 1, the ratio of black and white genome in the spores has changed from 1 : 1 to 3 : 1, assuming that both parts of the mycelium produce equal numbers of spores.

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A similar argument can be made for the initial benefit of another, similar kind of mutation occurring in a dikaryon of an obligatorily outcrossing so-called heterothallic —a mating system where mating can only occur between gametes with different mating types species. If this mutation changes the outcrossing life cycle into a selfing homothallic or secondarily homothallic—a mating system where mating can occur between gametes with identical mating types or asexual life cycle, all spores produced by this dikaryon contain the mutation.


If such a mutant still allows the dikaryon to donate one of its nuclei to a monokaryon, it theoretically gains a benefit over the wild type. The exact magnitude of this benefit is hard to calculate since it depends on the frequency of di-mon matings in a population, which we do not know. The example of S. Agaricus bisporus is one of the mushroom-forming basidiomycetes in which an outcrossing mating system evolved into a partially selfing secondarily homothallic mating system [ 19 ]. In this species, there are two inter-fertile varieties that both produce dikaryotic and monokaryotic spores, but in a different ratio.

As both parental mating types are present in these dikaryotic spores, they are self-fertile. By contrast, A. As explained above, the transition from obligate outcrossing heterothallism could be explained by an initial fitness gain of the selfing homothallic variety in an outcrossing heterothallic population [ 18 ]. However, this predicted fitness gain might be severely reduced as the new life cycle will lead to inbreeding and increased homozygosity. Yet, this particular species appears to have evolved a way to minimize the effects of inbreeding by redirecting meiotic crossovers almost exclusively to its chromosome ends [ 22 , 24 ].

By having crossovers at chromosome ends, the offspring of these mushrooms have practically intact parental chromosomes. All chromosomes combined still form the same genome. Hence, genetically, the resulting mushrooms are almost identical to the parental mushroom, which limits the detrimental effects of inbreeding.

During a mating between two monokaryons, a combination of migration and nuclear division transforms the two monokaryons into a single dikaryon in terms of nuclear genomes. All cells of the dikaryon contain two nuclei, one of each monokaryon. This gives rise to possible competition among the mitochondrial haplotypes from the two original monokaryons, within the newly formed dikaryon.

Genetic contact

Figure 3.