The Manure Tour: Invasive Populations and Clandestine Cultivars Have Bottlenecked Magic Mushrooms Since Psilocybe cubensis Spread From Its Unknown Centre of Origin

Abstract

Psilocybe cubensis is a mushroom that grows in niches of livestock dung in the tropics and subtropics and produces a hallucinogenic compound, psilocybin. It has caused accidental poisonings since the 1940s in Australia and has been cultivated since the 1970s globally. The centre of origin of P. cubensis is unknown. We sequenced genomes of 38 isolates from Australia and compared them with 86 genomes of commercially available cultivars to determine i) whether P. cubensis is native or naturalised in Australia, and ii) how cultivation has impacted commercial cultivars. Our analyses of genome-wide SNPs and single copy orthologs showed that the Australian population is naturalised, having recovered its effective population size after a bottleneck when it was introduced, and it has maintained relatively high genetic diversity at its mating-type loci. In contrast, cultivated lineages have generally not recovered from decreased effective population sizes and have hallmarks of inbreeding and clonal propagation, including low genetic diversity, low heterozygosity, high linkage disequilibrium, and low allelic diversity of mating genes. Cultivars are founded from single genotypes or populations with low genetic diversity. The psilocybin gene cluster is homogeneous across most cultivars of P. cubensis, however, the Australian lineage, as well as specific cultivars, have unique allelic diversity that may translate to differences in biosynthesis of psilocybin and its analogues. Given the impacts of inbreeding depression, knowledge of the centre of origin of P. cubensis will benefit breeding for genetic gain in magic mushrooms.

Keywords: effective population size, fungal genomics, fungal inbreeding, magic mushrooms, population genomics, psilocybin