Wood-loving magic mushrooms from Australia are saprotrophic invaders in the Northern Hemisphere

Magic mushrooms, which produce the compound psilocybin, maintain sexual compatibility across geographically isolated populations despite minimal gene flow since diverging from a common ancestor. Analysis of 89 genomes shows that psilocybin genes have high allelic diversity and show signs of balancing selection. Australasia is the center of origin for wood-degrading magic mushrooms, and their intercontinental distribution likely resulted from human-assisted movement of woodchips, mulch, or plants rather than natural dispersal. The findings indicate that species connectivity persists across separated populations, with no evidence of allopatric speciation eroding mating compatibility.

Study at a glance

Abstract

Magic mushrooms are fungi that produce psilocybin, an entheogen with long-term cultural use and a breakthrough compound for treatment of mental health disorders. Fungal populations separated by geography are candidates for allopatric speciation, yet species connectivity typically persists because there is minimal divergence at functional parts of mating compatibility genes. We studied whether connectivity is maintained across populations of a widespread species complex of magic mushrooms that has infiltrated the Northern Hemisphere from a hypothesised centre of origin in Australasia. We analysed 89 genomes of magic mushrooms to examine erosion of species connectivity in disparate populations with support from gene flow, kinship, structure, allelic diversity, and mating compatibility. We used comparative genomics and synteny to test whether the genes that produce psilocybin are under selection in natural populations of magic mushrooms. Despite phenotypic plasticity and intercontinental distribution, sexual compatibility is maintained across geographically isolated populations of magic mushrooms. Psilocybin loci have high allelic diversity and evidence of balancing selection. Australasia is the centre of origin of wood-degrading magic mushrooms and geographically separated populations are fully sexually compatible, despite minimal gene flow since differentiation from a shared ancestor. Movement of woodchips, mulch, or plants has most likely facilitated invasion of these mushrooms in the Northern Hemisphere.