Sexual selection in mushroom-forming basidiomycetes
Bart P. S. Nieuwenhuis
()
Alfons J. M. Debets
Duur K. Aanen
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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)