Introduction
Mushrooms (Agaricomycetes, Basidiomycota) disperse large quantities of
wind-borne spores (Dam, 2013), yet populations of many different species
are structured by geography (Amend, Garbelotto, Fang, & Keeley, 2010;
Branco et al., 2017; Dabao Sun et al., 2023). These geographically
isolated populations may form allopatric species if mating compatibility
ceases. Mushrooms are typically obligately sexual (heterothallic), and
mating compatibility is either tetrapolar, in which alleles at two
independent loci must differ for gametes to fuse, or bipolar, controlled
at one locus (Coelho, Bakkeren, Sun, Hood, & Giraud, 2017).
Mating-compatibility loci have high allele diversity and long allele
residence times (Skrede, Maurice, & Kauserud, 2013; van Diepen, Olson,
Ihrmark, Stenlid, & James, 2013), and this diversity is maintained
across populations by negative frequency selection that favours rare
mating types, with minimal divergence of functional parts of mating
genes that control compatibility (Peris et al., 2022). The relationship
between speciation and erosion of mate compatibility in reproductive
isolation needs better understanding to delineate populations from
species of Basidiomycota.
Mushrooms that produce psilocybin, magic mushrooms, occupy diverse
environmental niches as saprotrophs that degrade leaves, wood, and dung
(Stamets, 1996). A key diagnostic character of magic mushrooms is a
blueing reaction, due to oligomers of psilocin that form when psilocybin
is dephosphorylated and oxidised after tissue damage (Lenz et al.,
2020). Psilocin, the active metabolite of psilocybin, binds to serotonin
receptors, which are the targets hypothesised to protect magic mushrooms
against fungivory by metazoans (Reynolds et al., 2018). The etymology
behind epithets of wood-degrading magic mushrooms, e.g., P.
azurescens , P. cyanescens , and P. subaeruginosa ,
describes their strong blueing reaction and these mushrooms have some of
the highest concentrations of psilocybin (Gotvaldová et al., 2022).
The Oregon Psilocybin Advisory Board discouraged commercialisation of
wood-degrading species of Psilocybe as in some cases a side
effect temporarily paralyses users during a psilocybin experience (Abbas
et al., 2021). The cause of ‘wood lover’s paralysis’ is unknown (Dörner
et al., 2022). Dörner et al. (2022) and McTaggart et al. (2023) showedpsiH , a gene in the psilocybin pathway that converts tryptamine
into 4- hydroxytryptamine (Fricke, Blei, & Hoffmeister, 2017), is
duplicated with up to three homologs in wood-degrading species ofPsilocybe , compared to a single copy in P. cubensis .
McTaggart et al. (2023) hypothesised these gene duplications may impact
the production of psilocybin and its analogues, however, there is no
evidence that links the psilocybin pathway to wood lover’s paralysis,
and Dörner et al. (2022) suggested the symptoms are likely not linked to
tryptamines.
Psilocybe subaeruginosa was described from national parks and
natural environments in Australia (Cleland, 1927). It has taxonomic
priority in a complex of closely related, potentially conspecific
species described from Australia (P. australiana , P.
eucalypta , and P. tasmaniana ), New Zealand (P. makaroraeand P. weraroa ), and the northern hemisphere (P. allenii ,P. azurescens , and P. cyanescens ) (Borovička, Noordeloos,
Gryndler, & Oborník, 2011; Gotvaldová et al., 2022). The morphological
diversity of P. subaeruginosa in Australia encompasses phenotypes
of taxa described in the northern hemisphere (Fig. 1). Psilocybe
allenii and P. cyanescens behave as invasive taxa in the
northern hemisphere, occurring in planted garden beds rather than
undisturbed ecosystems (Borovička, Rockefeller, & Werner, 2012; Dennis
& Wakefield, 1946), and having low genetic diversity among populations
(Gießler, 2018).
Psilocybe subaeruginosa has a wide distribution across Australia,
occurring from southeast Queensland at its northernmost extent to
Tasmania, South Australia, and Western Australia. We examined
populations of P. subaeruginosa across its eastern distribution
in Australia to test hypotheses (i) that it has a centre of origin in
Australia, (ii) that it is conspecific with species in the northern
hemisphere, (iii) that populations in Australia are structured by
geography, and (iv) that selection shapes the genes in the psilocybin
pathway. To do so, we used population genomics and mating compatibility
to compare relationships among Australian populations and included
reference sequences of P. azurescens and P. cyanescens to
test conspecificity with taxa in the northern hemisphere. Our study
examines how fungal species connectivity is maintained across geographic
boundaries and provides new knowledge on the centre of origin of
wood-degrading species of Psilocybe .