Sexual selection in mushroom-forming basidiomycetes

Proceedings of the Royal Society B: Biological Sciences, Jan 2011

We expect that sexual selection may play an important role in the evolution of mushroom-forming basidiomycete fungi. Although these fungi do not have separate sexes, they do play female and male roles: the acceptance and the donation of a nucleus, respectively. The primary mycelium (monokaryon) of basidiomycete fungi, growing from a germinating sexual spore, is hermaphroditic, but it loses female function upon the acceptance of a second nucleus. The resulting dikaryon with two different nuclei in each cell retains a male potential as both nuclei can fertilize receptive mycelia. We tested the occurrence of sexual selection in the model species of mushroom-forming basidiomycetes, Schizophyllum commune, by pairing monokaryons with fully compatible dikaryons. In most pairings, we found a strong bias for one of the two nuclei although both were compatible with the monokaryon when paired alone. This shows that sexual selection can occur in mushroom-forming basidiomycetes. Since the winning nucleus of a dikaryon occasionally varied depending on the receiving monokaryon, we infer that sexual selection can operate through choosiness of the receiving individual (analogous to female choice). However, in other cases the same nucleus won, irrespective of the receiving monokaryon, suggesting that competition between the two nuclei of the donating mycelium (analogous to male–male competition) might also play a role.

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Sexual selection in mushroom-forming basidiomycetes

Bart P. S. Nieuwenhuis () Alfons J. M. Debets Duur K. Aanen Articles on similar topics can be found in the following collections Receive free email alerts when new articles cite this article - sign up in the box at the top right-hand corner of the article or click here Subject collections Email alerting service To subscribe to Proc. R. Soc. B go to: http://rspb.royalsocietypublishing.org/subscriptions Sexual selection in mushroom-forming basidiomycetes Droevendaalsesteeg 1, 6708 PB, Wageningen, The Netherlands We expect that sexual selection may play an important role in the evolution of mushroom-forming basidiomycete fungi. Although these fungi do not have separate sexes, they do play female and male roles: the acceptance and the donation of a nucleus, respectively. The primary mycelium (monokaryon) of basidiomycete fungi, growing from a germinating sexual spore, is hermaphroditic, but it loses female function upon the acceptance of a second nucleus. The resulting dikaryon with two different nuclei in each cell retains a male potential as both nuclei can fertilize receptive mycelia. We tested the occurrence of sexual selection in the model species of mushroom-forming basidiomycetes, Schizophyllum commune, by pairing monokaryons with fully compatible dikaryons. In most pairings, we found a strong bias for one of the two nuclei although both were compatible with the monokaryon when paired alone. This shows that sexual selection can occur in mushroom-forming basidiomycetes. Since the winning nucleus of a dikaryon occasionally varied depending on the receiving monokaryon, we infer that sexual selection can operate through choosiness of the receiving individual (analogous to female choice). However, in other cases the same nucleus won, irrespective of the receiving monokaryon, suggesting that competition between the two nuclei of the donating mycelium (analogous to male male competition) might also play a role. 1. INTRODUCTION Sexual selection is defined as the component of natural selection associated with variation in reproductive success caused by competition for access to gametes of the opposite sex [1,2]. It is reflected in competition between individuals of the same sex for mating (usually strongest in males: male male competition) and preference for some individuals as mates (usually strongest in females: female choice). Sexual selection is known to be of importance in the animal and plant kingdom [3 5], but so far this has not been recognized in fungi (but see [6]). In plants and animals the traits and behaviours associated with sexual selection are often quite elaborate, but in fungi such traits are more difficult to observe. In this paper, we show that sexual selection occurs in the basidiomycete fungus Schizophyllum commune. The life cycle of most basidiomycetes encompasses two distinct phases: those of the monokaryon and the dikaryon. Initially, a meiotic haploid spore germinates, giving rise to a mycelium with uninucleate cells, the monokaryon. This mycelium can grow vegetatively and, when it meets another monokaryon of the same species, hyphal fusions occur between the two mycelia (figure 1). At that moment fertilization of the mycelium can occur. In most mushroom-forming basidiomycetes, fusion is followed by exchange of nuclei but not cytoplasm [7,8], resulting in a mycelium with binucleate cells, the dikaryon. Nuclei migrate from the contact zone through the whole receiving mycelium [9]. The exact process of dikaryotization is unknown, but it must involve many nucleus duplications because the outcome of dikaryotization is that all cells of both receiving mycelia contain both nucleus types (figure 1b). Just like the monokaryon, the dikaryon can grow vegetatively, but it is also able to form sexual fruiting bodies (the mushrooms). In the fruiting bodies, the two nuclei fuse, directly after which meiotic spores are produced. A dikaryon can no longer accept other nuclei, but it can still donate nuclei to a monokaryon [10,11], a phenomenon called the Buller phenomenon. Even though basidiomycetous fungi are considered to have no sexes [12,13], clear male and female roles can be distinguished in their general life cycle [14,15]. Using the common criterion that male and female gametes are defined by small and large size, respectively [16], the acceptance of a nucleus by a large mycelium that contributes all cytoplasm can be seen as a femalelike function, and the donation of a nucleus as a malelike function. Previously, people have referred to mating types in basidiomycetous fungi as being different sexes (e.g. [17]). Note that we do not. We will treat mating types as sexual compatibility systems, comparable to self-incompatibility systems in plants. We will go into more detail on this topic in 4. The male- and femalelike functions imply that a monokaryon is hermaphroditic, but that it can function only once as a female during mating, while after having been fertilized it retains its male pot (...truncated)


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Bart P. S. Nieuwenhuis, Alfons J. M. Debets, Duur K. Aanen. Sexual selection in mushroom-forming basidiomycetes, Proceedings of the Royal Society B: Biological Sciences, 2011, pp. 152-157, 278/1702, DOI: 10.1098/rspb.2010.1110