Domestication through clandestine cultivation constrained genetic diversity in magic mushrooms relative to naturalized populations

Domestication of the hallucinogenic mushroom Psilocybe cubensis for psilocybin production has led to inbreeding and selfing in commercial cultivars, reducing genetic diversity and heterozygosity. In contrast, a naturalized Australian population, likely introduced from an unknown origin, has recovered from a bottleneck and maintains high genetic diversity. Genome comparisons of 38 Australian isolates and 86 commercial cultivars revealed that cultivars have low effective population sizes, high linkage disequilibrium, and low allelic diversity in mating-compatibility genes, while the Australian population shows higher nucleotide and allelic diversity. The psilocybin gene cluster is nearly identical across most cultivars, but unique alleles in Australia and some cultivars may affect psilocybin biosynthesis.

Study at a glance

Abstract

Fungi that are edible or fermentative were domesticated through selective cultivation of their desired traits. Domestication is often associated with inbreeding or selfing, which may fix traits other than those under selection, and causes an overall decrease in heterozygosity. A hallucinogenic mushroom, Psilocybe cubensis, was domesticated from its niche in livestock dung for production of psilocybin. It has caused accidental poisonings since the 1940s in Australia, which is a population hypothesized to be introduced from an unknown center of origin. We sequenced genomes of 38 isolates from Australia and compared them with 86 genomes of commercially available cultivars to determine (1) whether P. cubensis was introduced to Australia, and (2) how domestication has impacted commercial cultivars. Our analyses of genome-wide SNPs and single-copy orthologs showed that the Australian population is naturalized, having recovered its effective population size after a bottleneck when it was introduced, and it has maintained relatively high genetic diversity based on measures of nucleotide and allelic diversity. In contrast, domesticated cultivars generally have low effective population sizes and hallmarks of selfing and clonal propagation, including low genetic diversity, low heterozygosity, high linkage disequilibrium, and low allelic diversity of mating-compatibility genes. Analyses of kinship show that most cultivars are founded from related populations. Alleles in the psilocybin gene cluster are identical across most cultivars of P. cubensis with low diversity across coding sequence; however, unique allelic diversity in Australia and some cultivars may translate to differences in biosynthesis of psilocybin and its analogs.