Not all roads lead to selfing: mating-system stability in an invasive ectomycorrhizal fungus

Abstract

Baker's rule predicts that selfing is a beneficial trait for colonizers, whose prediction in the kingdom Fungi is reinforced by recent work showing the invasive ectomycorrhizal basidiomycete Amanita phalloides with self-incompatibility (SI) system has evolved unisexual reproduction in its introduced range. Unlike in plants, the multiallelic SI system of basidiomycetes does not fully prevent selfing among the meiotic offspring of a single dikaryotic (diploid) parent. This distinction allows observation of an intermediate state of selection where selfing is preferred in a species with SI system during colonization before a change in self-incompatibility architecture. Here, we analyzed the genomes of 189 isolates of the ectomycorrhizal basidiomycete Suillus luteus collected from both its native European range and five independently introduced regions to test whether selfing rates increased and whether the SI system had degraded after introduction. Unlike the A. phalloides case, we found no evidence of unisexual reproduction or loss of the SI system in the introduced ranges of S. luteus. Rather, all introduced populations maintained outcrossing rates higher than expected under random mating as in the native population. However, selfing events were detected in three individuals from a single introduced population, representing the first documented case of selfed sporocarps of Boletales fungi. Our work in S. luteus demonstrates that although selfing is possible in this species, it is not favored during colonization, potentially due to inbreeding depression and higher population density, highlighting the complex interaction among invasion biology, genetics, and the colonizing context.